Download The effects of noise on the auditory sensitivity of the bluegill sunfish

Comparative Biochemistry and Physiology Part A 133 (2002) 43–52
The effects of noise on the auditory sensitivity of the bluegill
sunfish, Lepomis macrochirus夞
Amy R. Scholik*, Hong Y. Yan
Mechanosensory Physiology Laboratory, School of Biological Sciences, University of Kentucky, Lexington, KY 40506, USA
Received 4 December 2001; received in revised form 14 March 2002; accepted 24 March 2002
Abstract
As concerns about the effects of underwater anthropogenic noises on the auditory function of organisms increases, it
is imperative to assess if all organisms are equally affected by the same noise source. Consequently, auditory capabilities
of an organism need to be evaluated and compared interspecifically. Teleost fishes provide excellent models to examine
these issues due to their diversity of hearing capabilities. Broadly, fishes can be categorized as hearing specialists (broad
hearing frequency range with low auditory thresholds) or hearing generalists (narrower frequency range with higher
auditory thresholds). The goal of this study was to examine the immediate effects of white noise exposure (0.3–2.0
kHz, 142 dB re: 1 mPa) and recovery after exposure (1–6 days) on a hearing generalist fish, bluegill sunfish (Lepomis
macrochirus). Noise exposure resulted in only a slight, but not statistically significant, elevation in auditory threshold
compared to fish not exposed to noise. In combination with results from our previous studies examining effects of noise
on a hearing specialist fish, the fathead minnow (Pimephales promelas), this study provides evidence supporting the
hypothesis that fish’s auditory thresholds can be differentially affected by noise exposure.
䊚 2002 Elsevier Science Inc. All rights reserved.
Keywords: Auditory brainstem response; Centrarchidae; Cyprinidae; Hearing generalist fish; Hearing specialist fish; Threshold shift;
Underwater noise; White noise
1. Introduction
Recently, there has been heightened concern
about the effects of underwater noise on freshwater
and marine organisms. This is a result of the
increasing amount of noise in the underwater
acoustic environment associated with anthropogenic sources (Richardson et al., 1995; Gordon and
Moscrop, 1996). Though sounds generated from
boats and ships are considered the main sources,
there are a vast number of anthropogenic noise
夞 Part of the results was presented at the 18th International
BioAcoustic Council meeting, Cogne, Italy, 3–6 September,
2001.
*Corresponding author. Tel.: q1-859-257-7410; fax: q1859-257-1717.
E-mail address: [email protected] (A.R. Scholik).
sources, including underwater explosions, sonars,
air guns, dredges, ocean science studies, hydroelectric dams, fishing equipment with acoustic
deterrent devices, and noises associated with oil
and gas production (Richardson et al., 1995; Rich¨
ardson and Wursig,
1997). Though most of these
sources generate noise only as a by-product, many
produce it intentionally. Regardless, there are an
expansive number of potential noise sources an
aquatic or marine organism may encounter in its
environment.
Despite the amount of noise in the underwater
environment, there have been few studies directly
addressing the auditory effects of noise on aquatic
organisms. Many behavioral studies have been
conducted, but they may not give a comprehensive
1095-6433/02/$ - see front matter 䊚 2002 Elsevier Science Inc. All rights reserved.
PII: S 1 0 9 5 - 6 4 3 3 Ž 0 2 . 0 0 1 0 8 - 3
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A.R. Scholik, H.Y. Yan / Comparative Biochemistry and Physiology Part A 133 (2002) 43–52
picture of the effects of noise exposure on the
physiology of the auditory system. For example,
Myrberg (1990) reported that many fish species
have been found in the vicinity of offshore petroleum drilling platforms, which are considered quite
noisy. He brings forth a pertinent question to
consider: are the fishes assembled in this area
because they are deafened and their ability to
acoustically assess their surroundings is severely
compromised or does the noise simply not affect
their auditory system? Furthermore, fishes, as well
as marine mammals, may react differently to noises, either by fleeing the area, remaining stationary,
or even become attracted to the noise source
¨
(Richardson and Wursig,
1997). Richardson and
¨
Wursig (1997) remark that because an organism
may endure noise exposure does not necessarily
mean that the noise itself does not have any
adverse effects.
In addition, it is erroneous to think that all
organisms would be equally affected by a noise
source. This has already been demonstrated by
examining behavioral effects of noise on marine
mammals in terms of sex, age, general activity,
¨
time of year, and habitat (Richardson and Wursig,
1997). Though, one factor that is often neglected
is the organism’s general hearing ability. Different
organisms have variation in their auditory capabilities, in terms of not only hearing frequency ranges
but also auditory threshold levels. It can, therefore,
be hypothesized that hearing ability also plays an
important role in the response an organism has to
a noise source. The end result is that there are
multitudes of different noise sources in the underwater environment along with an abundance of
different organisms that can potentially be affected,
and very little information so far addressing the
effects of noise on hearing thresholds of species
with different auditory capacities.
The first step in addressing these issues is
finding appropriate animal models, and fishes provide a means of better understanding the effects
of noise on hearing. What makes fish such suitable
models, is that there is no one universal ‘fish ear’
due to the vast amount of structural and physiological diversity among the inner ear and its
peripheral structures, which causes great degrees
of differences in hearing abilities among fishes
(Platt and Popper, 1981; Schellart and Popper,
1992; Popper and Fay, 1993, 1999). Therefore,
fishes offer the unique opportunity to examine a
variety of hearing mechanisms and their responses
to noise exposure.
Essentially, a fish’s sensitivity to sound depends
on the presence of a gasbladder (von Frisch, 1938;
Coombs and Popper, 1979; Yan et al., 2000) or
gas-holding auditory ancillary structures: suprabranchial chambers (Schneider, 1941; Ladich and
Yan, 1998; Yan, 1998), otic gasbladders (von
Frisch, 1938; Stipetic, 1939; Yan and Curtsinger,
2000; Fletcher and Crawford, 2001), otic bullae
(Blaxter et al., 1979; Denton et al., 1979; Gray
and Denton, 1979; Blaxter et al., 1981) and the
degree of coupling or proximity these structures
have with the fish’s inner ear. One common type
of accessory structure is the Weberian apparatus,
of otophysan fishes (i.e. minnows and catfish),
which are modified vertebrae connecting the anterior portion of the gasbladder to the inner ear
(Evans, 1925). This accessory apparatus acts to
transduce the pressure component of sound, associated with the vibration of the gasbladder, into
particle motion which directly stimulates the sensory epithelium of the inner ear (Finneran and
Hastings, 2000). Fishes with direct coupling
devices or auditory ancillary structures are referred
to as hearing specialists because they hear over a
wide frequency range with lower auditory threshold. Conversely, fishes without these coupling
devices and that hear over a narrower frequency
range with higher auditory thresholds are referred
to as hearing generalists (Tavolga and Wodinsky,
1963; Popper and Fay, 1993, 1999). Consequently,
along with the anatomical diversity associated with
the fish’s auditory structures, there is a correlation
with anatomy and hearing capabilities (see review
in Platt and Popper, 1981). Therefore, it has been
speculated that noise may not affect every fish
equally due to the diversity of the fish ear itself
(Hastings et al., 1996).
There have been several previous studies examining the physical effects and morphological damage associated with intense noise exposure on the
inner ear of fishes (Enger 1981; Hastings, 1995;
Hastings et al., 1996). Two of the species examined were hearing generalists, the oscar (Astronotus ocellatus) and cod (Gadus morhua), though
the cod has wider hearing range than most hearing
generalist species (Sand and Karlsen, 1986; Astrup
and Møhl, 1993, 1998), while one was a hearing
specialist, the goldfish (Carassius auratus). All
the studies detected mechanical injury to the sensory hair cells after exposure to intense sound
A.R. Scholik, H.Y. Yan / Comparative Biochemistry and Physiology Part A 133 (2002) 43–52
ranging from 180 to 204 dB (re: 1 mPa), but
damage was limited in the oscar (A. ocellatus)
compared to that seen in the goldfish (C. auratus).
Hastings et al. (1996) attributed this difference in
hair cell damage to variation in overall hearing
ability (hearing generalists vs. specialists) between
the two species. All of these studies only addressed
morphological effects of noise exposure, not auditory threshold effects.
Studies examining auditory effects of noise on
fishes, have been limited and have, so far only
examined hearing specialist fishes. Popper and
Clarke (1976) investigated the effects of pure tone
noise stimuli (149 dB, re: 1 mPa) on the goldfish.
Our previous study (Scholik and Yan, 2001),
examined the effects of white noise on auditory
sensitivity of the fathead minnow (Pimephales
promelas) and indicated that the effects of intense
white noise exposure (142 dB, re: 1 mPa) was
frequency and exposure duration dependent. The
next issue of interest was to examine if white
noise exposure yielded similar results in a fish
without enhanced hearing mechanisms, a hearing
generalist fish.
The purpose of this study was to examine how
intense noise affected the auditory sensitivity of a
hearing generalist fish, the bluegill sunfish
(Lepomis macrochirus). The bluegill sunfish
(Family Centrarchidae) is considered a relatively
important sport fish in the North America. Its
natural habitats ranges from southern Canada to
northern Mexico, including the midwest and eastern regions of the USA (Trautman, 1981; Helfman
et al., 1997). Due to its wide range of distribution
in various types of aquatic habitats, the bluegill
has the potential to be exposed to a variety of
acoustic environments. Hence, it is a useful model
for the present study.
We hypothesized that since hearing generalists,
like bluegill sunfish, lack Weberian ossicles or
ancillary structures to enhance hearing sensitivity,
and thus have an auditory range that is narrower
in frequency bandwidth with higher overall auditory thresholds than hearing specialists (e.g. fathead minnows) (Scholik and Yan, 2001, 2002),
their hearing thresholds should be less affected by
noise. Specifically, the two main objectives of our
study were to (1) examine the immediate effects
of noise exposure (0.3–2.0 kHz, 142 dB re: 1
mPa) using various exposure duration (2, 4, 8 and
24 h), and to (2) assess recovery (1–6 days) of
auditory thresholds after exposure to 24 h of white
45
noise using the auditory brainstem response (ABR)
recording technique. In addition, we were interested in comparing the results from the present study,
for a hearing generalist, to those we previously
obtained (Scholik and Yan, 2001) for a hearing
specialist fish. This comparison allows us to investigate if the impacts of noise exposure can be
equally applied to fishes of different hearing
abilities.
2. Materials and methods
2.1. Subjects
Bluegill sunfish (L. macrochirus) used for this
study (72.3–105.4 mm total length (TL); 5.0–
20.6 g wet body weight) were obtained from a
local fish hatchery (Newtown, OH). In general,
hatchery ponds are relatively ‘quiet’ environments
(75–80 dB re: 1 mPa; H.Y. Yan unpublished
survey data), though actual measurements for these
specific ponds could not be obtained. These fish
were considered juveniles, approximately 6–7
months old during the experimental procedure.
While in the laboratory, fish were housed in a 320
gallon circular tub with a filtration system (average
SPL:-115 dB, re: 1 mPa, 0.3–2.0 kHz) at
25"1 8C, under 14L:10D light cycle, and fed
commercially prepared pellets (Hikari). The animal use protocol used in this study was approved
by the University of Kentucky Institutional Animal
Care and Use Committee (00217L2001).
2.2. White noise exposure
Fish were exposed to a white noise source with
a bandwidth of 0.3–2.0 kHz at 142 dB (re: 1
mPa), which was generated using Tucker–Davis
Technologies (TDT) SigGen娃 software. White
noise is defined as a noise source that has a flat
power spectrum as a result of all frequencies being
presented at an identical average intensity or pressure (Yost, 2000). The bandwidth of the noise was
particularly chosen to encompass the entire auditory range of the bluegill sunfish, excluding those
frequencies below 0.3 kHz, where lateral line
inputs could come become an extraneous factor
¨
(Munz,
1985, 1989; Popper and Fay, 1993;
Coombs and Montgomery, 1999).
Once generated, the noise was then fed through
a DA1 digital–analog converter, a PA4 programmable attenuator, and a power amplifier (QSC
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A.R. Scholik, H.Y. Yan / Comparative Biochemistry and Physiology Part A 133 (2002) 43–52
Audio Product, Model USA 370) that drove a 30cm-diameter speaker (Pioneer, frequency response
1.9–15 kHz) suspended 1 m above a plastic tub,
where the fish were housed during the noise
exposure duration.
Noise exposure of subjects, as a group, occurred
in a plastic tub (38=24.5=14.5 cm3) with 5.5cm depth of water. The fish were free to swim
about the tub during the exposure, but a fine mesh
screen was placed over the tub to prevent them
from jumping outside. The plastic tub sat upon a
vibration-free air table (Kinetic Systems, model
1201) inside a soundproof chamber (2=3=2 m3,
Industrial Acoustics Company Inc.).
The use of white noise as an acoustic stimulus
is to represent a generic sound that a fish might
encounter in its environment. Since most underwater anthropogenic noise sources are not composed of pure tones (reviewed in Urick, 1983;
Greene and Moore, 1995; Gordon and Moscrop,
¨
1996; Richardson and Wursig,
1997), the use of
white noise allows one to better understand the
auditory effects of noise exposure over a wider
frequency range and is more realistic than creating
an artificial noise of a single discrete frequency.
2.3. Auditory brainstem response (ABR) recording
technique
Hearing thresholds were obtained using the
auditory brainstem response (ABR) recording
technique, which is defined as an electrophysiological far-field recording of synchronous neural
activity of the eighth cranial nerve and associated
auditory brainstem nuclei in response to an acoustic stimulus (Yost, 2000). This recording technique
and its application on the auditory physiology of
fishes are described in great detail by several
papers including Kenyon et al. (1998), Ladich and
Yan (1998), Yan (1998), Yan et al. (2000), Yan
and Curtsinger, (2000) and Scholik and Yan (2001,
2002). Thus, only a synopsis of the technique is
given for this study.
In order to reduce myogenic noise, a fish first
was sedated with an injection of Flaxedil (gallamine triethiodide, Sigma Chemical Co., St. Louis,
MO) at a dosage ranging from 20 to 70 ml (5
mgy15 ml: 0.3 mgyml). Then it was restrained in
a mesh sling, which was attached to a glass rod
that was fixed in a micromanipulator (M330,
World Precision Instruments, Sarasota, FL). The
restrained fish was immersed in a plastic tub (34.3
cm=47.0 cm=17.1 cm), so that the nape of the
head was approximately 1 mm above the water
surface. Once sedated and immersed, a respiration
pipette was placed in the fish’s mouth and a
recording electrode, along midline of skull at
region of medulla, and a reference electrode,
approximately 5 mm anterior of reference electrode, (Teflon-insulated silver wire, 0.25 mm in
diameter with 1 mm of exposed tip) were placed
firmly against the head of the fish. In addition to
the fish being in the tub, a hydrophone (Celesco
LC-10), used to monitor the sound pressure levels
(SPL) of the auditory stimuli, was placed near the
head of the fish.
A Tucker–Davis Technologies modular rack
system running TDT BioSig娃 software was used
to present sound stimuli and measure ABR waveforms. This system was controlled by an optically
linked Pentium III, 350 MHz desktop computer
housing a TDT board. The sound stimuli consisted
of eight frequencies (0.3, 0.4, 0.5, 0.6, 0.8 1.0, 1.5
and 2.0 kHz) and were presented for 20 ms as
tone bursts of the specified frequency (2000
sweeps per test) and sound pressure level. All
stimuli for the ABR recording technique and those
used for noise exposure, were presented using a
30-cm diameter speaker (Pioneer) mounted 1 m
above the fish.
To measure auditory thresholds, the highest
sound pressure level was presented first and then
attenuated in 5 dB steps for all frequencies until a
repeatable ABR waveform was no longer obtainable, which was determined using visual inspection
of the waveform. In addition, cross-correlation
coefficient (r) examination was also used to determine threshold, where any r value of -0.3 is
considered below threshold (Yan, 1998; Yan et al.,
2000; Yan and Curtsinger, 2000; Scholik and Yan,
2001, 2002).
2.4. Experiment 1: immediate effects of white noise
exposure
To assess the immediate effects of white noise
exposure, groups of bluegill sunfish (ns6) were
exposed to various durations of noise, ranging
from 2 to 24 h at 142 dB (re: 1 mPa). Immediately
following noise exposures, thresholds were measured using the ABR recording technique. One-way
ANOVAs, with multiple comparisons (Dunnett
test) using SigmaStat software, were used to compare exposure duration effects against baseline fish
A.R. Scholik, H.Y. Yan / Comparative Biochemistry and Physiology Part A 133 (2002) 43–52
47
(those not exposed to noise) for each of the eight
auditory frequencies measured.
2.5. Experiment 2: Recovery after 24 h exposure
To examine recovery of auditory sensitivity after
24 h of noise exposure, auditory thresholds were
measured at 1, 2, 4 or 6 days (ns6 for each
condition) following exposure. During the days
following noise exposure, fish were kept in separate aquaria in an isolated room, where auditory
disturbances were kept minimal (average SPL: 103 dB re: 1 mPa, 0.3–2.0 kHz) until auditory
testing could be completed. Separate one-way
ANOVAs, with multiple comparisons (Dunnett
test), were used to compare recovery time for each
hearing frequency and day against baseline thresholds using SigmaStat software.
2.6. Comparison of audiograms
To have a more comprehensive understanding
of how noise exposure impacts auditory threshold
changes in a hearing generalist (e.g. bluegill sunfish, present study) and a specialist fish, data from
our previous study using the fathead minnow
(Scholik and Yan, 2001) are included for
comparison.
3. Results
3.1. Experiment 1: immediate effects of white noise
exposure
To assess the immediate effects of noise exposure duration on auditory thresholds, audiograms
were measured for groups of bluegill sunfish
exposed to noise for 2, 4, 8 or 24 h, with all
thresholds being compared to baseline thresholds
or those fish receiving no noise exposure. Fig. 1
(upper two traces) exhibits the results from 24 h
of noise exposure compared to baseline fish.
Though, there is a slight elevation in threshold
after noise exposure, statistically out of all the
eight frequencies tested, none were significantly
different from the baseline fish (P)0.05).
Table 1a includes data for the other exposure
duration of 2, 4 and 8 h of noise. Again, none of
the varying exposure duration yielded a statistically significant difference from the baseline group
of fish (P value range: 0.08–0.74). The overall
results shown in Table 1a and Fig. 1 demonstrate
Fig. 1. Audiograms of bluegill sunfish and fathead minnows
showing baseline and threshold shift due to 24-h white noise
exposure. Upper two traces: bluegill sunfish. Solid circles:
baseline data of groups of fish not exposed to noise. Open
circles: experimental group exposed to white noise (0.3–2.0
kHz, 142 dB re: 1 mPa). Lower two traces: fathead minnows.
Solid triangles: baseline data of groups of fish not exposed to
noise. Open triangles: experimental group exposed to white
noise (0.3–4.0 kHz, 142 dB re: 1 mPa). Fathead minnow data
are taken from Scholik and Yan (2001), and asterisks indicate
a P value -0.01. The horizontal bar (solid and dashed), at the
top of the figure, represents white noise SPL experienced by
both species, with the solid section representing the bandwidth
of exposure for the bluegill sunfish and the hatched section
representing the extended bandwidth for the fathead minnow.
Frequency range is in a log, base 10, scale.
clearly that noise exposure, of various duration,
does not significantly elevate auditory threshold at
the frequencies examined.
3.2. Experiment 2: recovery after 24 h white noise
exposure
Since there was a slight, although statistically
nonsignificant, elevation in auditory threshold after
24 h of noise exposure, the timetable of threshold
recovery was further examined. Audiograms for
fish recovering from noise exposure were obtained
from 1 to 6 days after exposure to 24 h of noise.
Again, none of the recovery days, after noise
exposure, yielded a statistical significant difference
from the baseline group of fish (P value range:
0.13–0.83). Though, there is an overall trend
demonstrating a decrease in auditory threshold
from day 1 to 6, indicating that recovery may
possibly be occurring (Table 1b).
A.R. Scholik, H.Y. Yan / Comparative Biochemistry and Physiology Part A 133 (2002) 43–52
48
3.3. Comparison with hearing specialist fish
Though the results from this study are notable
alone, they become even more so when they are
compared to our previous experiment (Scholik and
Yan, 2001), in which a fathead minnow, received
the same type of white nose exposure. Both groups
of fishes were subjected to same duration (24 h)
of noise exposure (142 dB re: 1 mPa) (as indicated
by horizontal bar, solid and dashed, in Fig. 1),
however, the difference in threshold shifts between
the two group was very significant (Fig. 1). For
the fathead minnows, five (0.3, 0.8, 1.0, 1.5, 2.0
kHz) out of eight frequencies, shown, exhibited
statistically significant changes of thresholds (Fig.
1, lower two traces). On the contrary, no significant changes of threshold shifts were observed in
all eight frequencies tested in the bluegill sunfish
(Fig. 1, upper two traces).
The differential impacts of noise exposure on
two distinct species of fish can be further demonstrated by examining changes of mean threshold
in Fig. 2. For the bluegill sunfish, noise exposure
yielded less than a 5-dB threshold shift for all
auditory frequencies examined, and none of these
changes were statistically significant from baseline
thresholds. On the other hand, for the fathead
minnows, all threshold shifts were larger than 5
dB. In the fish’s most sensitive hearing range
(0.8–2.0 kHz), they ranged from 10 to 20 dB
greater than baseline thresholds. Thus, the results
in Figs. 1 and 2 indicate clearly that threshold
shifts due to noise exposure are species-dependent,
i.e. fathead minnows respond significantly, while
bluegill sunfish do not show any significant elevation of thresholds.
Fig. 2. Changes of mean threshold (dB) as a function of frequency after exposure to 24 h white noise (142 dB re: 1 mPa)
between the bluegill sunfish and the fathead minnow (fathead
minnow data are taken from Scholik and Yan, 2001). Solid
triangles: threshold shift in fathead minnow. Solid circle: bluegill sunfish. Frequency range is in a log, base 10, scale.
4. Discussion
The bluegill sunfish is one of the major game
fishes in the eastern part of North America and
has been artificially introduced into various water
bodies by many state and federal agencies (Helfman et al., 1997). Such a cosmopolitan species is
an ideal choice for an animal model to better
understand how anthropogenic noise could impact
auditory physiology. In addition, up to date, no
such noise impact study on auditory physiology
has been carried out using a hearing generalist
species, such as the bluegill sunfish. The utilization
of this species provides a unique window into
Table 1
(a) Shown are threshold values measured immediately after white noise exposure for 2, 4, 8, and 24 h and (b) threshold values measured
for 1, 2, 4, and 8 days of recovery after exposure to 24 h noise (both given with standard errors)
(a) Intermediate effects
0.3
0.4
0.5
0.6
0.8
1.0
1.5
2.0
kHz
kHz
kHz
kHz
kHz
kHz
kHz
kHz
(b) Recovery after 24 h noise
Baseline
2h
4h
8h
24 h
1 day
2 days
4 days
6 days
122.9"1.3
118.7"2.0
122.6"1.9
122.1"2.0
126.5"1.3
126.5"1.6
132.7"1.5
133.9"1.4
120.9"1.6
121.1"1.7
123.7"1.1
120.0"1.2
123.3"0.9
124.9"2.1
131.1"2.5
134.3"1.4
124.4"1.2
124.0"2.3
125.0"1.9
123.9"2.5
125.7"2.1
125.1"1.4
134.2"1.7
134.7"0.9
125.3"1.1
122.7"1.8
124.9"0.9
125.8"1.0
127.4"1.4
128.2"1.1
129.1"3.3
133.1"2.4
125.0"1.5
122.2"1.2
123.2"1.5
126.1"1.1
128.2"1.3
128.3"2.0
136.1"1.2
138.7"1.4
124.1"1.1
123.7"0.2
126.5"1.6
125.9"2.4
125.7"2.1
127.7"1.8
129.0"4.6
137.1"2.7
121.3"1.5
118.9"1.9
119.0"1.7
120.3"1.0
125.1"1.9
124.6"2.3
127.8"1.7
137.7"1.6
118.8"1.7
120.6"1.6
124.6"1.9
124.4"1.8
125.2"2.1
126.8"1.2
131.9"1.2
138.6"1.0
122.2"3.0
121.8"1.3
121.9"2.8
121.8"3.3
123.2"2.5
126.5"2.1
135.3"0.9
137.8"1.9
All data are in dB re: 1 mPa.
A.R. Scholik, H.Y. Yan / Comparative Biochemistry and Physiology Part A 133 (2002) 43–52
examining how noise impacts the majority of
fishes that are hearing generalists.
4.1. White noise exposure: immediate effects and
recovery
In this study, we demonstrated that exposure to
intense noise for various exposure durations (2–
24 h) did not result in a statically significant
elevation in auditory threshold for the eight frequencies tested (0.3–2.0 kHz). Though a slight
elevation in threshold was noticeable after 24 h of
exposure.
In addition, recovery after 24 h exposure was
examined, up to six days after noise exposure but
yielded no statistically significant results. In Table
1a,b some of the thresholds measured after noise
exposure were lower than baseline thresholds.
These few anomalies observed do not indicate that
noise exposure decreases auditory thresholds.
Instead, this can be explained by the fact that each
testing condition was done using a different group
of 6 fish and that pre-existing individual variations
in threshold might have to be considered.
4.2. Hair cell addition with growth
As noted, the bluegill sunfish used in this
experiment were juveniles, and it is a well-known
phenomenon that inner ear hair cell proliferation
occurs postembryonically in fishes (Corwin, 1983;
Popper and Hoxter, 1984, 1990; Lombarte and
Popper, 1994; Lanford et al., 1996). With this
addition, the question is whether or not auditory
thresholds change with hair cell proliferation.
Few studies have addressed this issue. Popper
(1971) and Wysocki and Ladich (2001) both
examined hearing specialist species, while Kenyon
(1996) was the first to demonstrate ontogenetic
changes in auditory sensitivity in hearing generalist
species. Using two species of bicolor damselfish
(Pomacentrus partitus and P. variablis), he found
that overall hearing ability increased with the age
and size of the fish. In an addition, Yan (unpublished data) confirmed that different sizes of bluegill
sunfish exhibited differences in hearing abilities.
In light of these findings, future studies should
examine if noise exposure could create differential
impacts on distinct size and age classes of bluegill
sunfish.
49
4.3. Differential effects of noise exposure
Taken with the results of our previous study
(Scholik and Yan, 2001), we demonstrated that
white noise can have differential auditory impacts
on fishes. The same duration of noise exposure,
24 h, resulted in statistically significant threshold
shifts in the fathead minnow, while the bluegill
sunfish was minimally affected. This phenomenon
can be explained when one considers the auditory
capabilities of these two distinct species.
The horizontal bar (solid and dashed) in Fig. 1
indicates the noise level experienced by both
bluegill sunfish and fathead minnows. For the
fathead minnow, the SPL of the noise level was
over 60 dB greater than threshold in the fish’s
most sensitive hearing frequency range. Conversely, for the bluegill sunfish, the overall noise SPL
was less than 25 dB greater than threshold in its
most sensitive auditory frequency range. It is
obvious that fathead minnows experienced a much
more significant difference in SPL between baseline thresholds and noise exposure levels than that
of the bluegill sunfish.
A point worth discussing is: did differences
between baseline thresholds and noise exposure
levels lead to differential responses to noise and
subsequently no significant elevation in the bluegill sunfish’s auditory threshold. Yan et al. (2000)
demonstrated that gasbladder deflation in a hearing
specialist fish (C. auratus) resulted in a significant
elevation of hearing thresholds, comparable to that
of a hearing generalist species. In light of this
finding, future research should be directed at
deflating the gasbladder of the fathead minnow,
followed by noise exposure, to investigate if
changes in threshold become nonsignificant, comparable to that of bluegill sunfish after noise
exposure. Additionally, experiments can be conducted providing a noise source 60 dB above
hearing threshold of the bluegill sunfish to examine
if the same degree of threshold elevation, similar
to that of the fathead minnow, can be observed.
4.4. Ecological significance
Despite 24 h noise exposure only resulted in a
statistically insignificant elevation of auditory
thresholds in juvenile bluegill sunfish, one does
not know what kind of detriments, if any, even a
slight elevation in threshold may cause a fish in
its natural daily activities. Myrberg (1981) empha-
50
A.R. Scholik, H.Y. Yan / Comparative Biochemistry and Physiology Part A 133 (2002) 43–52
sized the importance of the auditory system in
fishes for detecting predators, prey, alarm
responses, and signaling mates. In addition, hearing may be used to accurately assess the acoustic
landscape (Popper and Fay, 1993, 1999). One
could speculate, since the sense of hearing is so
important for fishes, in terms of detecting biologically significant factors, that fishes with even a
slight detriment in hearing may have a disadvantage. This is an area where further studies, addressing the relationship between diminished auditory
capabilities and behavioral effects, are needed.
Even though this study strictly examined an
artificially generated white noise source, these
results are relevant and applicable to anthropogenic
noise sources fishes may encounter in their natural
environment. Recently, we used engine noise from
55 horsepower boat outboard motor (power spectrum major peak at 1.3 kHz) to assess the immediate effects of 2 h of this noise played at 142 dB
(re: 1 Pa) on auditory sensitivity of the fathead
minnow (Scholik and Yan, 2002). It was found
that this anthropogenic noise source significantly
elevated the fathead minnow’s auditory threshold
in its most sensitive hearing frequency range, 1.0–
2.0 kHz. Based on our previous results (Scholik
and Yan, 2001, 2002) and the results of this study,
it can be speculated that the same boat engine
noise would affect auditory sensitivity of bluegill
sunfish minimally compared to fathead minnows.
Nevertheless, in their acoustic environment, all
fishes whether hearing specialists or generalists
are being exposed to the same noises. Specifically,
the response and auditory sensitivity of an individual fish species in a local assemblage should be
taken into account when sound is intentionally
used to modify behavior and prevent entrapment
(reviewed in Popper and Carlson, 1998). Our
results indicate that a bluegill sunfish may be
minimally affected, while a fathead minnow may
exhibit extensive threshold shifts when exposed to
the same noise source.
This phenomenon, of differential effects of noise
exposure on auditory sensitivity, may not be limited exclusively to fishes. Ketten (1992) explained,
in terms of anatomy and auditory sensitivity, that
the cetaceans can be divided into three main
acoustic groups. Each group equates with a specific
cochlear morphology and use of acoustical frequencies (i.e. infrasonic vs. ultrasonic). In light of
our present study and previous findings (Scholik
and Yan, 2001), it may be speculated that an
underwater noise source may not effect all marine
mammals equally.
4.5. Summary
The results of this study indicate that the bluegill
sunfish’s auditory threshold is minimally affected
by exposure to an intense noise source (142 dB
re: 1 mPa), even after as much as 24 h of duration.
In addition, combining the results obtained from
this study and a previous study (Scholik and Yan,
2001), we provide evidence to support the hypothesis that a noise source does not affect all fishes
equally. This effect is based on variation in auditory capabilities (frequency range and overall auditory threshold) of different species, which is
dependent on differences in anatomical structures
between inner ear and gasbladder. Furthermore,
this finding emphasizes the importance of considering differences in auditory abilities of fishes
when examining deleterious effects of intense
noise exposure whether behaviorally or physiologically. Consequently, this should also be a concern
when considering the effects of all sounds on any
marine or freshwater organism.
Acknowledgments
The authors would like to thank Mr Jerome J.
Schlomer for his valuable assistance in transport
and aid in general maintenance and care of the
fish used in this experiment. In addition, we would
like to thank two anonymous reviewers for their
valuable comments. This research was supported
by grants from the Kentucky Academy of Sciences
and graduate fellowship from University of Kentucky Interdepartmental Neuroscience Program,
and a predoctoral trainee fellowship from N.I.H.
Cellular and Molecular Sensory Biology training
grant to A.R.S. Financial support to H.Y.Y. was
provided by National Organization for Hearing
Research, National Institute of Mental Health
(MH-58198), and Institute of Museum and Library
Services of US Department of Education (LL90187).
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