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First published online April 18, 2008
Journal of Experimental Biology 211, 1504-1511 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.016196
Acoustic pressure and particle motion thresholds in six sciaenid fishes
1 Department of Fisheries Science, Virginia Institute of Marine Science, College
of William and Mary, Gloucester Point, VA 23062, USA
2 Cooperative Marine Education and Research Program, Northeast Fisheries Science
Center, National Marine Fisheries Service, NOAA, Woods Hole, MA, USA
3 Department of Biology, Virginia Commonwealth University, Richmond, VA,
USA
* Author for correspondence (e-mail: andrij{at}vims.edu)
Accepted 5 March 2008
 |
Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: animal communication, hearing, particle acceleration, particle velocity, Sciaenidae, soniferous
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). The
otoliths of all fishes are biological accelerometers that directly detect the
particle motion components of sound as a result of inertial differences
between sensory epithelia and otoliths (Lu
and Xu, 2002; Popper and Fay,
1999). Additionally, the pressure component of sound may be
detected indirectly by some fishes via accessory anatomical
structures that transform sound pressure waves into particle displacements
(Popper and Fay, 1993).
Fishes are categorized as hearing `specialists' and `generalists' on the
basis of anatomy, the ability to detect the pressure component of sound, and
the range of detectable bandwidth. Hearing specialist species have evolved
projections of the swim bladder or skeletal connections that enable the
indirect re-radiation of the pressure component of sound as particle
displacement capable of stimulating the inner ear
(Fay and Popper, 1974;
Popper and Fay, 1999). Thus
hearing-specialist fishes, which include groups such as clupeids, otophysans,
mormyrids and osphronemids, may use both direct (particle motion) and indirect
(pressure transduction) mechanisms to enhance their hearing sensitivity and
extend their detectable auditory bandwidth
(Mann et al., 1997;
Popper and Fay, 1993;
Yan, 1998;
Yan and Curtsinger, 2000). By
contrast, hearing generalist fishes lack such specialized structures coupling
pressure-to-displacement transducers to the otic capsule, resulting in
attenuation of the signal and reduced stimulation of the ear via
sound pressure (Casper and Mann,
2006). The unaided organs of the inner ear of hearing generalists
are thought to be fairly insensitive to the indirect transduction of sound
pressure (Sand and Karlsen,
2000; Yan et al.,
2000); direct particle motion stimulation of the otoliths is
likely more relevant to these fishes (Lu
and Xu, 2002; Casper and Mann,
2006). However, few studies have examined the hearing thresholds
of fishes with respect to both pressure and particle motion sensitivity
(Myrberg and Spires, 1980;
van den Berg, 1985;
Lovell et al., 2005;
Casper and Mann, 2006).
Sciaenid fishes are model organisms of teleost bioacoustics
(Ramcharitar et al., 2006a;
Roundtree et al., 2006), but
comparatively little is known about their auditory abilities. Sciaenid
saccular otoliths are enlarged relative to most fishes, and their morphology
and proximity to the swim bladder vary widely
(Chao, 1978;
Ramcharitar et al., 2001).
Both hearing specialists and generalists have been identified within the
family (Ramcharitar et al.,
2004; Ramcharitar et al.,
2006b). Unfortunately, the pressure detection abilities of less
than two percent of the 270 sciaenid species have been described [Atlantic
croaker, spot, weakfish, black drum, silver perch
(Ramcharitar, 2003)], and the
particle motion sensitivity of these fishes has not been examined. Comparative
work on sciaenid fishes has great potential to elucidate form-and-function
relationships in the teleost auditory system
(Ramcharitar, 2003). We
therefore performed auditory brainstem response experiments using a hydrophone
and geophone to categorize the pressure and particle acceleration detection
thresholds of six sciaenid fishes. The simultaneous recording of the pressure
and particle motion components of sound stimuli allowed us to express
audiograms with respect to both. The former allows us to compare our data to
previously published results for sciaenid fishes
(Ramcharitar and Popper, 2004;
Ramcharitar et al., 2006b);
the latter allows comparison to recent studies examining particle motion
thresholds in other fishes (Casper and
Mann, 2006; Mann et al.,
2007).
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Experimental and animal care protocols were approved by the College of
William and Mary's Institutional Animal Care and Use Committee, protocol no.
0423, and followed all relevant laws of the United States. Auditory brainstem
response (ABR) experiments were conducted on six animals of each species. All
subjects were sedated with an intramuscular (i.m.) dose of the steroid
anesthetic Saffan (Glaxo Vet, Glaxo Vet Ltd, Uxbridge, UK; 10 mg
kg–1) and immobilized with an i.m. injection of the
neuromuscular blocking drug gallamine triethiodide (Flaxedil; Sigma, St Louis,
MO, USA; 10 mg kg–1). Recording of vertebrate ABR waveforms
in anaesthetized and/or immobile subjects is a common practice to minimize the
obscuring effect of muscular noise on ABR recordings
(Hall, 1992;
Kenyon et al., 1998;
Casper et al., 2003). Sedated
and immobilized animals were suspended within a rectangular
61x31x16.5 cm Plexiglas tank using foam straps, leaving <1 mm
of the top of the head protruding from the water. Subjects were ventilated (1
l min–1) with filtered, oxygenated, and
temperature-controlled seawater (25±2°C). At the conclusion of each
experiment, fishes were euthanized with a massive i.m. dose of sodium
pentobarbital (
300 mg kg–1).
Auditory brainstem response
Auditory brainstem response (ABR) is a non-invasive recording of the neural
activity in the eighth cranial nerve and brainstem in response to synchronized
acoustic stimuli (Corwin et al.,
1982; Kenyon et al.,
1998). The ABR experimental setup and procedure followed that of
others (Kenyon et al., 1998).
A speaker (model: 40-1034, 27.5 cm in diameter, Radio Shack, Fort Worth, TX,
USA), suspended in the air, was mounted 1.5 m directly above the test subject.
Two platinum wire needle electrodes (model: F-E7, 10 mm tip, Grass
Technologies, West Warwick, RI, USA) were placed subdermally along the midline
of each subject: the active electrode was positioned above the medulla, and
the reference electrode in the dorsal musculature above the operculum. The
system was grounded to the water of the experimental tank via a 6
cmx26 cm stainless steel plate. An omnidirectional hydrophone (Reson
A/S, Slangerup, Denmark; sensitivity: –211 dB re: 1V/µPa) was
suspended with rubber straps 25 mm below the water surface (i.e. the depth of
a subject's otic capsule) and positioned within 2.5 mm of the right
opercle-preopercle margin of each subject to measure the sound pressure level
of the stimulus and ambient noise.
In the absence of an anechoic chamber, all experiments were conducted in a
concrete laboratory. We produced a stochastic differential white noise signal
to characterize the echoes resulting from all reflective surfaces at the
hydrophone positioned next to the subject. A custom Fourier/inverse Fourier
transform algorithm (MATLAB version 6.5, Mathworks, Inc., Natick, MA, USA) was
used to analyze these recordings and add to each frequency's pure tone
stimulus the appropriate signals needed to destructively interfere with any
recorded echoes. Any alteration to the sound field in the laboratory since the
last echo-cancellation (i.e. movements, small changes in the tank water level,
etc.) required us to re-echo-cancel before proceeding. Visual examination of
stimulus waveforms recorded by the hydrophone during ABR experiments
(Fig. 1) confirmed that our
echo-cancelled stimuli were very similar to pure tone waveforms used in other
fish hearing experiments (Kenyon et al.,
1998).
|
) but the polarity of stimulus artifacts is not. ABR traces of
opposite polarity were therefore summed to remove stimulus artifacts. Periodic
experiments were also conducted with euthanized fish to ensure that identified
ABR responses were not stimulus artifacts.
The two ABR responses at each frequency and sound pressure level were
overlaid to assess the response. Sound pressure levels were successively
attenuated in roughly 5 dB steps until repeatable ABR waveforms were no longer
produced; thresholds were defined as the lowest sound pressure level for which
a repeatable ABR trace could be identified visually
(Kenyon et al., 1998). Visual
threshold assignment provides results similar to quantitative
threshold-seeking algorithms (Yan,
1998) and remains the standard method of threshold determination
in fish ABRs (Kenyon et al.,
1998; Casper et al.,
2003). Visually assigned thresholds for each subject of a study
species were pooled to produce mean audiograms.
Sound pressure levels of all experimental stimuli were calculated from
hydrophone recordings (Burkhard,
1984). Cursors were placed one cycle apart (peak-to-peak) on
either side of the largest (i.e. center) cycle of a tone-burst recording of
the hydrophone (Kenyon et al.,
1998). The Bio-Sig software then calculated the root mean square
(RMS) of the waveform between the cursors, and the appropriate gain
calibration factors were applied to determine actual sound pressure level
(SPL) in dB re: 1 µPa.
Particle velocity was calibrated using an underwater acoustic
pressure-velocity probe (Mk. 2, Acoustech Corp, Philadelphia, PA, USA)
containing two built-in units: a piezoelectric, omni-directional hydrophone
(sensitivity: –200 dB re: 1V/µPa) and a bi-directional moving-coil
geophone (sensitivity: 0.112 V cm–1 s–1).
The outer housing of this probe was secured in place of the fish 25 mm
below the water surface with rubberized clamps, and the inner unit of the
probe, designed to approximate neutral buoyancy, moved freely in response to
our sound stimuli. The omnidirectional hydrophone was suspended by rubber
straps to within 2 mm of the pressure–velocity probe. This setup enabled
the simultaneous recording of the sound pressure and particle velocity
components of the entire range of our experimental stimuli. Subsequently and
separately, measurements of particle displacements were recorded in three
orthogonal orientations (sensu
Casper and Mann, 2006). The
vertical component (z axis) of particle velocity had substantially
greater amplitudes than the x (horizontal: head-to-tail) or
y axes (left to right) at each frequency and attenuation
(Table 2). This vertical axis
was therefore considered most appropriate for expressing thresholds and
plotting particle acceleration audiograms.
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The otolithic organ systems of fishes are thought to act as accelerometers,
and particle motion audiograms have been increasingly expressed in units of
acceleration (Kalmijn, 1988;
Fay and Edds-Walton, 1997;
Casper and Mann, 2006).
Therefore, particle velocity (m s–1) was quantified as above
for acoustic pressure, and velocity values were converted to particle
acceleration using Eqn 1:
 | (1) |
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). Considering responses of an individual fish to be
independent across frequencies constitutes pseudoreplication
(Hurlbert, 1984); valid
analyses of such data require that the nature of within-individual
autocorrelation is explicitly understood. Inadequate consideration of the
variance-covariance structure resulting from repeated measures may result in
biased estimates of the variance of fixed effects
(Littell et al., 2006).
Pressure and particle acceleration thresholds were therefore analyzed
separately using two-way repeated measures ANOVAs with a priori
contrasts to investigate whether hearing varied between the six sciaenid
species and among frequencies. All statistical analyses were conducted using
SAS v 9.1 (SAS Institute, Cary, NC, USA). The model for these analyses is
given in Eqn 2:
 | (2) |
i is the species
(fixed factor); βj is the frequency (fixed factor);
k is the species:frequency interaction; 
ijk
is the random error term associated with the observation at each combination
of the ith species, the jth frequency, and the kth
level of their interaction.
We fitted models with three candidate covariance structures (unstructured,
compound symmetry, and first order autoregressive [AR(1)]) to the pressure and
particle acceleration threshold data. In the unstructured model (UN), each
covariance between measures was estimated individually, allowing the data to
dictate the appropriate covariance structure. The second covariance structure,
compound symmetry (CS), assumed equal covariances between all pairs of
observations. The final covariance structure, first order autoregressive
[AR(1)], assumed that the correlation between observations is a function of
their lag in space or time; adjacent observations are more likely to be
correlated than those taken further apart
(Littell et al., 2006). As a
simple example involving the relationship between evoked potentials at 200,
300 and 900 Hz, the UN model would calculate the variance–covariance of
every pair of observations individually, the AR(1) model would assume that
evoked potentials at 200 and 300 Hz are likely more similar than responses at
200 versus 900 Hz, whereas the CS model would assume equal
covariance.
After models were fitted to data, the appropriate covariance structure was
selected using Akaike's information criterion (AICc):
 | (3) |
). The small-sample adjustment (AICc) is
recommended when the ratio of sample size to the number of parameters is less
than 40 (Burnham and Anderson,
2002). |
RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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400 Hz) or 50 ms (100–300 Hz). Waveform latency
varied inversely with frequency and sound pressure level. Sound pressure,
particle velocity, and acceleration audiograms of all species
(Fig. 3 A–C) exhibited
lowest thresholds at low frequencies (100–500 Hz). Velocity and
acceleration audiograms were notably flatter at low frequencies.
AICc values supported the selection of the first order
autoregressive [AR(1)] covariance model for both pressure and particle
acceleration analyses (Table
3), supporting the assumptions of the AR(1) model. Visual
inspection of sciaenid audiograms (Fig.
3) confirms inferences based on AICc; ABR responses at
adjacent frequencies were therefore more similar to each other than responses
at distant frequencies.
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|
Two-way repeated measures ANOVAs demonstrated significant differences between species for both pressure (F5,48.6=3.17, P<0.02) and particle motion (velocity: F5,51.4=3.85, P<0.005; acceleration: F5,52.3=3.00, P<0.02) thresholds. Sound pressure thresholds of spot were significantly higher (F1,357=5.05, P<0.03) than those of other sciaenids from 300–700 Hz. Among species with swim bladders, thresholds of those with anteriorly projecting diverticulae (weakfish, spotted seatrout and Atlantic croaker) did not differ from those species without diverticulae (red drum and spot; pressure: F1,357=2.35, P=0.13). Surprisingly, thresholds of northern kingfish were among the lowest at higher frequencies (>600 Hz) even though the swim bladder atrophies in the adults we studied. Detection thresholds varied inversely with frequencies for both pressure (F11,324=53.01, P<0.001) and particle motion (velocity: F11,317=78.47, P<0.0001 acceleration; F11,315=129.24, P<0.0001). Interactions of species and frequencies were significant for both pressure (F55,319=3.31, P<0.0001) and particle motion (velocity: F55,314=8.48, P<0.0001; acceleration F55,314=9.77, P<0.0001) and are visually evident in the crossing of species-specific curves within audiograms (Fig. 3A–C).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Few studies have examined hearing thresholds of fishes with
respect to both pressure and particle motion sensitivity (Myrberg and Spires,
1988; van den Berg, 1985;
Lovell et al., 2005;
Casper and Mann, 2006).
Moreover, direct particle motion simulation of the otoliths may be more
relevant to hearing generalist fishes than the detection of sound pressure
(Fay and Popper, 1975;
Popper and Fay, 1993). In this
study, we measured thresholds and expressed audiograms of six sciaenid fishes
in terms of both sound pressure and acceleration using an omnidirectional
hydrophone and a bi-directional geophone. Our experiments are the first to
assess particle motion thresholds in sciaenid fishes and include first reports
of pressure audiograms for spotted seatrout, red drum, and northern
kingfish.
Sound stimuli during fish audition experiments contain both pressure and
particle motion (Parvulescu,
1967; Lu et al.,
1996; Casper and Mann,
2006). Small experimental tanks can have complex particle motion
and sound pressure fields, potentially compromising laboratory investigations
unless both components of sound stimuli are measured
(Kalmijn, 1988;
Popper and Fay, 1993). Placing
stimulus-generating speakers in air rather than water purportedly reduces the
particle motion (Kenyon et al.,
1998). Our results, however, demonstrate that speakers in air can
produce notable particle motion fields
(Table 2). Similar conclusions
were reached by others (Casper and Mann,
2006). Particle displacements in small tanks are complex, and for
an equal sound pressure level they may be greater in tanks than in an
unbounded body of water (Parvulescu,
1967; Rogers and Cox,
1988). General comparisons across studies may be complicated by
differences in the location of the sound source in air versus water,
the proximity of subjects to the sound source and air-water interfaces
(Fay and Edds-Walton, 1997).
Such concerns demonstrate the utility of routine particle motion assessment of
experimental sound stimuli. Submersible units capable of generating and
measuring particle motion are available
(Casper and Mann, 2007a;
Casper and Mann, 2007b). Future
fish audition experiments should attempt to measure and report both the
pressure and particle motion components of their experimental stimuli if
possible (Popper and Fay,
1993; Casper and Mann,
2006).
The frequency range detected by the six sciaenids we studied was similar to
those of other hearing generalist fishes (100 to <2000 Hz)
(Popper and Fay, 1993;
Kenyon et al., 1998;
Ramcharitar, 2003;
Ramcharitar and Popper, 2004;
Ramcharitar et al., 2006b).
Pressure detection thresholds of sciaenid fishes were significantly lower at
low frequencies from 100–300 Hz. Our mean pressure thresholds for spot,
weakfish and Atlantic croaker, obtained with a speaker in air, averaged about
6 dB higher than those obtained by others using a speaker in water
(Ramcharitar and Popper, 2004;
Ramcharitar et al., 2006b).
Whether the different results are a consequence of speaker location/type,
different levels of background noise, individual variation due to the use of
larger animals in our study, or a combination of these factors, is unclear.
Overall, our results generally support the conclusion of Ramcharitar et al.
(Ramcharitar et al., 2006b)
that enhanced swim bladder–otolith relationships within the Sciaenidae
can improve auditory sensitivity. Among sciaenids bearing swim bladders, those
possessing diverticulae (weakfish, spotted seatrout and Atlantic croaker) had
generally but not significantly lower pressure thresholds than species lacking
diverticulae (spot and red drum). Swim bladders lacking mechanical coupling to
the otic capsule may not enhance sound pressure detection
(Yan et al., 2000).
Surprisingly, however, we found the lowest sound pressure thresholds at higher
frequencies (800–1100 Hz) in northern kingfish, a species with low hair
cell densities and swim bladder atrophy in adults
(Chao, 1978;
Ramcharitar et al., 2001).
Since species lacking swim bladders are unlikely to detect sound pressure
(Casper and Mann, 2006;
Mann et al., 2007), lower
`pressure' thresholds of kingfish at higher frequencies are most likely a
response to particle motion during the simultaneous presentation of pressure
and particle motion stimuli.
Otoliths are biological accelerometers most sensitive to particle motion on
their longitudinal axis (Lu and Xu,
2002), and the larger otoliths of sciaenid fishes may confer
higher sensitivity to the particle motion components of low frequency sounds
(Lychakov and Rebane, 1993;
Ramcharitar et al., 2006b).
Our particle acceleration audiograms demonstrate significantly greater
sensitivity at low frequencies (Fig.
3C) and are comparable to results obtained with elasmobranchs
(Casper and Mann, 2006).
Sciaenid species with enhanced connections between the swim bladder and otic
capsule (Atlantic croaker, spotted seatrout, weakfish) may be able to obtain
different information from the acoustic particle motion and sound pressure
fields (van den Berg, 1985;
Ramcharitar et al., 2001). By
contrast, sciaenid fishes lacking connections between these organ systems
(spot, red drum) are more likely to be responsive solely to particle motion
fields (Ramcharitar, 2003).
Similar conclusions have been reached for elasmobranch and teleost fishes
lacking swim bladders (Mann et al.,
2007; Casper and Mann,
2006). Adult kingfish (lacking swim bladders) used in our study
probably detect acoustic particle motion rather than pressure. The situation
is less clear for juvenile kingfish, which do have swim bladders that are
distant from the otic capsule (Chao,
1978; Ramcharitar,
2003). Unfortunately, little is known about ontogenetic
differences in pressure and particle motion discrimination in most fishes,
including sciaenids.
A better understanding of particle motion thresholds in fishes is required,
particularly with respect to hearing relative to the direction of stimulus
(sensu Fay and Edds-Walton,
1997). In our study, maximum particle displacement occurred along
the vertical axis (Table 2).
But are sciaenids most sensitive to particle motion on this axis? Spawning
aggregations, which involve chorusing fish juxtaposed in close proximity
(Mok and Gilmore, 1983;
Ramcharitar et al., 2006a;
Gilmore, 2003), more likely
stimulate otoliths in a horizontal direction. Although density and orientation
of hair cell bundles in sciaenid fishes differ among species
(Ramcharitar, 2003),
behavioral sensitivity of oscars (Cichlidae: Astronotus ocellatus) to
particle motion did not differ among orthogonal axes
(Lu et al., 1996). The
individual presentation of particle motion stimuli in various orthogonal
Cartesian planes to sciaenids would shed light on this question
(Lovell et al., 2005;
Casper and Mann, 2007a;
Casper and Mann, 2007b).
Dominant frequencies of most sciaenid reproductive and disturbance
vocalizations [100–500 Hz
(Ramcharitar et al., 2006a)]
lie well within the frequency bandwidths of the six species we measured.
Therefore, if they are within range, sciaenids should be able to detect each
others' species-specific vocalizations, which differ in their dominant
frequency, pulse duration, repetition rate, number of pulses per call and
sound pressure level (Ramcharitar et al.,
2006a). The extent to which these sciaenids use auditory cues to
discriminate among species or between individuals in generally noisy estuarine
environments remains unknown. This ability has, however, been demonstrated in
other soniferous fishes (Ladich,
2000; Ripley et al.,
2002; Wysocki and Ladich,
2003).
Sound pressure and particle motion detection thresholds in sciaenids were
lowest at the lower frequencies at which they communicate, but whether these
species primarily detect conspecific and congeneric vocalizations via
their sound pressure, particle motion, or both components of these sounds
remains unknown. Communication in sound-producing fishes occurs over
relatively short distances and typically in fairly shallow water, where the
acoustic near field is dominated by particle motion
(Myrberg, 2001;
Bass and Clark, 2002;
Weeg et al., 2002). Although
the characteristics of sciaenid spawning aggregations differ among species,
most occur in waters from 3–50 m depth
(Saucier and Baltz, 1993).
Sciaenids and other soniferous fishes communicate in shallow coastal and
estuarine waters despite high levels of background noise and the theoretical
short-distance propagation of low frequency sounds in shallow water
(Lugli et al., 2003;
Ramcharitar et al., 2006a).
Under idealized conditions, we estimate that sciaenid calls may propagate
8–128 m from the source, based on their amplitudes, simple spherical
spreading (a loss of 6 dB for every distance doubled) and auditory thresholds
(Table 4). Further, our
calculations assumed that background noise was below the auditory thresholds,
which is unlikely. For example, background ambient noise levels measured in a
North Carolina estuary ranged from 110 to 125 dB re: 1 µPa
(Sprague and Luczkovich,
2004). There is evidence for frequency selectivity amidst
background masking within the Sciaenidae, suggesting that some species may
still detect certain sounds amidst the masking din of background noise in
coastal environments (Ramcharitar and
Popper, 2004). Therefore, the distances at which these
vocalizations can be heard depend on the source's sound pressure level, the
pressure sensitivity and masked hearing ability of the listener, and
environmental variables such as background noise, depth, bottom type and
habitat complexity (Mann,
2006). Unfortunately, masked auditory thresholds are known for
only two sciaenids [Atlantic croaker and black drum
(Ramcharitar and Popper,
2004)]. Additionally, the propagation of pressure and particle
motion fields and actual attraction distances of sound sources in shallow,
complex, high-scattering, high-background estuarine habitats, are not well
understood at present (Mann,
2006; Casper and Mann,
2006; Lugli and Fine,
2007).
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In this study, we presented the pressure and particle motion thresholds of
six sciaenid fishes, including the first reports of particle acceleration
thresholds in this teleost family and first reports of pressure thresholds for
three species. Together, emerging data on sciaenid auditory abilities and
sonifery support growing efforts to identify and manage their spawning
habitats in environments with ever-increasing anthropogenic noise
(Wahlberg and Westerberg,
2005; Ramcharitar et al.,
2006a; Vasconcelos et al.,
2007). Sciaenid bioacoustics therefore remains a fruitful research
avenue and critical link between sensory physiology and behavioral ecology
(Popper et al., 2005;
Ramcharitar et al., 2006a;
Roundtree et al., 2006). Such
research promotes multidisciplinary syntheses that can mechanistically link
processes from the cellular to the individual to the population level in
support of fisheries management.
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Acknowledgments |
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Footnotes |
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