Sound generation in the searobin (Prionotus carolinus), a fish with alternate sonic muscle contraction
Washington College, Department of Biology, 300 Washington Ave, Chestertown, MD 21620, USA
e-mail: mconnaughton2{at}washcoll.edu
Accepted 6 February 2004
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Summary |
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Key words: sound production, sonic muscle, alternate contraction, swimbladder, fundamental frequency, constructive interference, sound amplitude, Prionotus carolinus
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Introduction |
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The sonic muscle of the toadfish, which has been called the fastest
vertebrate striated muscle (Rome and
Lindstedt, 1998; Rome et al.,
1996
; Tavolga,
1964
), can be stimulated to contract in situ at rates of
500 Hz without reaching tetany (Fine et
al., 2001
). In order to contract at these speeds, sonic muscles
express a variety of morphological and biochemical adaptations for speed.
These adaptations include, but are not limited to, small diameter, radial
morphology (Bass and Marchaterre,
1989
; Eichelberg,
1976
; Fawcett and Revel,
1961
; Fine et al.,
1993
), multiple innervation of muscle fibres
(Gainer and Klancher, 1965
;
Hirsch et al., 1998
;
Ono and Poss, 1982
), abundant
sarcoplasmic reticulum (Eichelberg,
1977
; Franzini-Armstrong and
Nunzi, 1983
) and parvalbumin
(Appelt et al., 1991
;
Hamoir et al., 1980
) content,
a large calcium capacity (Feher et al.,
1998
), the fastest calcium transient in a vertebrate muscle, and a
rapid cross-bridge detachment rate (Rome et al.,
1996
,
1999
). A result of rapid
cross-bridge detachment rates is the sacrifice of much of the twitch force.
The sonic muscles of toadfish produce approximately 10% of the force per
cross-sectional area of white muscle myofibrils
(Rome et al., 1999
). However,
these muscles still manage to displace the highly damped swimbladder and
produce a clearly audible sound at high contraction rates
(Fine et al., 2001
).
The Northern searobin, Prionotus carolinus, bears both intrinsic
and extrinsic sonic muscles (Evans,
1973), and the intrinsic muscles are known to play a role in sound
production (Evans, 1973
;
Tower, 1908
). The function of
the smaller, extrinsic sonic muscles is not clear and they will not be
considered in this paper. Little information is available regarding the
acoustic behavior of searobins. Captive
(Fish, 1954
) and field
(Fish and Mowbray, 1970
)
recordings suggest that sound is used in fright and perhaps antagonistic
interactions. The intrinsic muscles of the searobin are innervated
ipsilaterally by fibres from the occipital nerve
(Fig. 1; Bass and Baker, 1991
;
Evans, 1973
;
Finger and Kalil, 1985
). Bass
and Baker (1991
) recorded
discharges from the sonic nerve (a branch of the occipital nerve) indicating
that the bilateral sonic muscles contract alternately in this species rather
than synchronously, the norm among sonic fishes
(Cohen and Winn, 1967
;
Connaughton et al., 2000
;
Skoglund, 1961
;
Tower, 1908
).
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The purpose of the present study was to describe sound generation in the
searobin Prionotus carolinus using voluntary and electrically
stimulated sounds. The objectives of this study were several-fold: to describe
the disturbance sounds of searobins, to confirm that the sonic muscles
contract alternately, to determine the optimal and maximal rates of muscle
contraction producing audible sound and to determine if unilateral contraction
of the sonic muscles sacrifices sound amplitude. Voluntary and evoked calls
and muscle action potentials were recorded in air to avoid difficulties
associated with recording in an enclosed aquatic space
(Akamatsu et al., 2002;
Parvulescu, 1964
;
Tavolga, 1962
) and to allow
for the determination of absolute sound pressure level at a standard distance.
Carrying out the experiments in air also simplified the recording of action
potentials and stimulation of the sonic nerve.
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Materials and methods |
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Simultaneous EMG and acoustic recordings were made from voluntarily calling
searobins in air. In-air and in-water recordings of weakfish (Cynoscion
regalis; Connaughton et al.,
2000) and Atlantic croaker (Micropogonias undulatus; J.
Drummond and M. A. Connaughton, unpublished data) indicate that sounds
produced under these conditions are identical except for a greater number of
pulses in calls recorded in air. In-air recording trials were kept to less
than 1 min in duration, after which the fish was anaesthetized for electrical
stimulation of the SN (see below). EMGs were recorded differentially (World
Precision Instruments, DAM 50 amplifier, Sarasota, FL, USA) using
Teflon-coated wire electrodes placed no more than 2 mm apart in either the
left or right sonic muscle through a 1 cm incision in the lateral body wall.
In four experiments, recordings were made simultaneously from the left and
right sonic muscles using a single amplifier, with only one electrode placed
in each of the muscles. Acoustic recordings were made with a pressure zone
microphone (Realistic, Tandy Corp., Fort Worth, TX, USA; frequency response
flat from 20 Hz to 18 kHz) held 10 cm from the fish. The signal was amplified
(Radio Shack Karaoke Mate), digitized (MacLab; AD Instruments, Castle Hill,
NSW, Australia) and recorded at 11.1 kHz on a Macintosh computer. A 500 Hz, 70
dB (re: 20 µPa) calibration tone, measured with a sound level meter
(Realistic) adjacent to the microphone, was recorded to permit measurement of
absolute sound pressure level (SPL). Recordings were analyzed with Scope
oscilloscope software (v. 3.3; AD Instruments) and Canary bioacoustic
workstation software (v. 1.2; Cornell Laboratory of Ornithology, Ithaca, NY,
USA). For comparison with action potential repetition rate, acoustic
repetition rate (= fundamental frequency) was calculated from the period of
the waveform.
Specimens were anaesthetized with 100 mg l1 MS-222 (tricaine methanesulfonate; Sigma Chemical Co., St Louis, MO, USA) buffered to a neutral pH. Fish were placed in a recording chamber with water and anaesthetic recirculating over the gills. The SN was exposed by dissection of a 1 cmx2 cm window in the hypaxial musculature and stimulated (MacLab) via hook electrodes with 0.5 ms, 1 V, square wave pulses in 90 ms sweeps (the approximate duration of a disturbance call) at frequencies ranging from 50 Hz to 500 Hz. Simultaneous unilateral EMG and acoustic recordings were made with the microphone at 6 cm from the fish during SN stimulation. In four stimulation experiments, one, then both SNs were stimulated at frequencies between 100 Hz and 150 Hz for comparison of unilateral and bilateral SPL within a fish. SPL was determined as the average sound intensity across a 90 ms stimulation sweep. Fish were then sacrificed via an overdose of anaesthetic at low temperatures. Total length, total mass, total sonic muscle mass and average sonic muscle thickness were measured for each fish (13 male and 12 female). All experimental protocols were approved by the Mount Desert Island Biological Laboratory Institutional Animal Care and Use Committee.
A pooled t-test, or Wilcoxon signed rank test in the case of
non-parametric data, was used to compare male and female data. Acoustic
parameters were regressed across total length and holding tank temperature. A
pooled t-test was used to compare the duration of acoustic waveforms
from evoked and voluntary single twitches. Bonferroni multiple comparison
tests (summed =0.05) were used to compare among various parts of single
twitch acoustic waveforms and among peak-to-peak negative pressure intervals.
A paired t-test was used to compare unilateral and bilateral SPL for
each fish at each stimulus rate.
The sharpness of tuning (Q) of the swimbladder was calculated as:
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Results |
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Disturbance calls
Prior to electrode implantation, duration, SPL and peak frequencies were
collected for six disturbance calls from each fish (10 male, 7 female) and
none of these call characters varied significantly with sex. Calls had a mean
duration of 62.8±16.1 ms, a SPL of 75.4±2.0 dB (re: 20 µPa at
10 cm), a fundamental frequency of approximately 200 Hz (204.1±15.5 Hz)
with harmonics at approximately 400 Hz and 600 Hz
(Fig. 2). However, some
compound calls (ranging in duration from 100.6 ms to 132.2 ms) were recorded
from one fish, and some longer sounds (240.4933 ms) were recorded from
two other fish. These compound and longer calls are not included in the mean
data.
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Call duration did not vary significantly with total length or temperature. SPL increased significantly with total length (y=0.50x+63.1, r2=0.238, P=0.047) but did not vary over a temperature range of 2.5°C.
The power spectra of voluntary calls exhibited three or more clear frequency peaks. The frequency with the greatest amplitude often varied among these peaks even within the calls of a single individual. For example, a typical fish would produce a fundamental frequency of 217 Hz and two harmonic peaks at 435 Hz and 652 Hz. The range of fundamental frequencies observed was 174217 Hz. The ranges for the two harmonic peaks were more variable, 348481 Hz and 522674 Hz, respectively. Peak frequencies did not vary significantly with total length. Fundamental frequency increased significantly with temperature, rising 43 Hz over a modest 2.5°C change in temperature (Fig. 3A).
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Alternate muscle contraction during disturbance calls
Trains of EMGs in unilateral recordings of disturbance calls
(N=12) expressed a mean duration of 89.5±15.6 ms and consisted
of 48 action potentials (mean action potential duration= 6.2±1.0
ms) followed by an extended return to baseline (30.4±10.8 ms;
Fig. 4A). The number of sound
pulses per call ranged from 6 to 15 (11.2±2.2). The interval between
action potentials for one muscle averaged 9.5±0.8 ms while the interval
between sound pulses was 4.8±0.4 ms. Action potential repetition rate
was half the sound repetition rate (fundamental frequency;
Fig. 5), a typical call
expressing values of 107 Hz and 213 Hz, respectively. Mean action potential
repetition rate (106.5±8.3) was close to half that of the sound
repetition rate (206.4±16.1). In unilateral recordings, either the
muscle with the electrode or the contralateral muscle might contract first.
Since the first action potential did not always generate an acoustic pulse, it
was not always possible to determine if the contralateral muscle contracted
first. When the ipsilateral muscle contracted first, the time between onset of
the action potential and the first sound pulse was 2.1±0.5 ms.
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|
An action potential was present prior to alternate sound pulses in unilateral recordings (Fig. 4A), whereas in bilateral EMG recordings, every sound was preceded by an action potential (Fig. 4B). Between the large amplitude sound pulses, smaller single, double or more complex waveforms were visible. These smaller waveforms varied between fish. At the onset of most traces, one or more action potentials failed to produce acoustic pulses, most commonly the first, second or third action potential. The number of action potentials without resultant sounds at the onset of a call decreased with increasing temperature (Fig. 3B). Amplitude of sound pulses in a call increased to a maximum at the 5th (= mode; mean=5.7±0.5) pulse. Two additional, attenuated sound pulses followed the final action potential (Fig. 4A,B). The durations of the negative pressure peaks of these attenuated pulses (2.9±0.5 ms and 3.3±0.6 ms, respectively) were significantly greater than those of sound pulses associated with action potentials (2.0±0.4 ms; P=0.0001 for both).
Single twitch mechanics
Simulating the SN at 50 Hz provided the opportunity to examine single
twitch mechanics, as the acoustic waveform of one twitch was complete before
the next stimulus in the series occurred. The acoustic waveform resulting from
a single twitch consisted of two distinct sound pulses (see
Table 1 fordurations)
putatively described as the contraction and relaxation components of the
sound, following Fine et al.
(2001). The first, or
contraction waveform, began with a negative half-cycle followed by a positive
half-cycle of acoustic pressure (B in Fig.
6A). A plateau containing little or no sound energy followed this
waveform (D). The second, or relaxation waveform, began with a positive
half-cycle followed by a negative half-cycle and another positive half-cycle
of acoustic pressure (C). Data from evoked single twitches (N=9 fish,
4 twitches each) were corroborated by voluntary single twitches recorded
during abortive calls (N=2 fish, a total of 9 twitches). The only
significant differences between the dual-waveform sounds of evoked and
voluntary single twitches were the duration of the relaxation waveform
(P=0.0039) and, consequently, the total duration (P=0.0048;
Table 1). The durations of the
contraction and relaxation waveforms differed significantly within evoked and
voluntary twitches, as did peak frequencies
(Table 1).
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Evoked trains
The sonic muscle followed the SN stimulus rate (produced sound of that
frequency) from 50 Hz to 360 Hz. At 400 Hz, the peak frequency in the power
spectra was half the stimulus rate, indicating that the muscle was contracting
in response to alternate stimuli. Greatest sound amplitudes were recorded
between 100 Hz and 140 Hz, with the maximal amplitude (98.8 dB re: 20 µPa)
at 120 Hz (Fig. 8). A
Q3dB of 1.98 was calculated from the response of the
swimbladder to this range of stimuli.
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Action potential amplitude began to decrease by the end of any stimulus series above 120 Hz (Fig. 9). At frequencies as high as 360 Hz (data not shown) the muscle responded to each stimuli, although action potential amplitude dropped sharply after the first few stimuli. At 400 Hz, the muscle was observed to respond to alternate stimuli, while at 500 Hz the muscle either did not respond after the first stimulus or did so irregularly (Fig. 9).
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Evoked trains of sound at 100150 Hz (see Fig. 9) were similar to voluntary calls. They began with a small initial sound followed by one or more action potentials without resultant sounds. Amplitude of the sound pulses increased to a maximum and then declined. As the stimulus rate increased, the highest amplitude sound pulse came later in the series, shifting from the second pulse at a 50 Hz stimulus rate to the fifth or sixth pulse at 160180 Hz (Table 3). In addition, as the stimulus rate increased, more initial action potentials failed to produce sounds and the muscle often failed to produce sounds through the end of the stimulus series. At stimulus rates for which sound was produced through the end of the series, the final sound pulse was not associated with any stimulus or action potential and was attenuated (see 100 Hz in Fig. 9). Note that there was only one attenuated sound pulse in evoked calls.
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Bilateral vs unilateral amplitude
In evoked calls, synchronous bilateral contraction of the sonic muscles
produced greater amplitude sound than unilateral contraction at all stimulus
rates (P=0.005, 0.0021, 0.005 and 0.001 for four fish; see a sample
distribution for one fish in Fig.
10A). The SPL difference between bilaterally and unilaterally
evoked sounds (3.3±0.6 dB) ranged from 2.6 dB at 100 Hz stimulation to
3.8 dB at 140 Hz (Fig. 10B).
Individual differences in unilateral and bilateral SPL ranged as high as 5.9
dB, an approximate doubling of acoustic pressure.
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Discussion |
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The voluntary disturbance sounds produced by the searobin in this study
were similar in duration and frequency to `barks' recorded in captivity
(Fish, 1954) and in the field
(Fish and Mowbray, 1970
).
Fundamental frequency increased with temperature as it does in other species
producing long, non-pulsatile sounds
(Brantley and Bass, 1994
;
Fine, 1978
;
Schneider, 1967
). The basis
for this change in frequency is an increase in discharge rate of the sonic
motor nucleus with temperature (Bass and
Baker, 1991
).
Searobin sonic muscles contract alternately, as suggested by the
observation of asynchronous sonic nerve discharges
(Bass and Baker, 1991). This is
a unique arrangement for a teleost sonic system, as all other sonic muscles
examined to date contract synchronously
(Cohen and Winn, 1967
;
Connaughton et al., 2000
;
Packard, 1960
;
Skoglund, 1961
;
Tower, 1908
). During voluntary
disturbance calls, the searobin sonic muscles contracted alternately at a mean
of 105 Hz, producing a fundamental acoustic frequency of approximately twice
this value. When driven by stimulation of the sonic nerve, the sonic muscle
produced maximal sound amplitudes at 120 Hz, somewhat higher than the muscle
operates during voluntary calling. Midshipman (Porichthys notatus)
produce a courtship buzz at fundamental frequencies between 98 Hz and 108 Hz
by synchronously contracting their sonic muscles
(Cohen and Winn, 1967
;
Ibara et al., 1983
). Therefore
muscles of the searobin and midshipman contract at approximately the same
rate, although a twofold difference in acoustic fundamental frequency results.
The sonic muscles of the toadfish and pigfish (Congiopodus
leucopaecilus) produce 200 Hz calls via synchronous muscle
contraction (Fine, 1978
;
Packard, 1960
;
Skoglund, 1961
) and thus
function at twice the contraction rate of the searobin. The extrinsic sonic
muscles of two catfish, Galeichthys felis and Bagre marinus,
produce 150 Hz fundamentals (Tavolga,
1962
), falling between the toadfish and the searobin.
The sonic muscles of the toadfish have been reported to tetanize at
250300 Hz (at 25°C) in isolated bundles
(Rome et al., 1996) but are
able to produce trains of sound in situ at 400 Hz and can respond to
alternate stimuli without tetany at 500 Hz
(Fine et al., 2001
). The sonic
muscles of Bagre also did not fully tetanize at 500 Hz, while those
of Galeichthys reached tetany at 300400 Hz
(Tavolga, 1962
). The sonic
muscles of another searobin, Prionotus scitiulus, have been observed
to tetanize in half a second at stimulus rates of 340380 Hz
(Tavolga, 1964
). Finally, the
slower sonic muscles of the squirrelfish (Holocentrus sp.) and the
red hind (Epinephalus guttatus) have been observed to tetanize
between 150 Hz and 200 Hz (Gainer et al.,
1965
; Tavolga,
1964
).
Determination of tetany requires a constant muscle force at a known
stimulation frequency. This study did not measure force, nor can it be
determined with any certainty that all of the muscle fibres in the stimulated
muscles were activated by each stimulus during evoked trains. Having said
this, sound production might be used to make some simple suggestions about the
capabilities of the searobin sonic muscle. Based on sound amplitude, it
appears that the searobin sonic muscle (more accurately the sonic
muscleswimbladder system) was operating optimally when stimulated
between 100 Hz and 140 Hz. The muscle was capable of producing sound of
matching frequencies at stimulus rates of up to 360 Hz but, at a stimulus rate
of 400 Hz, the searobin sonic muscle contracted during alternate stimuli and,
at 500 Hz, the muscle ceased to respond after the initial stimulus. Thus,
using sound production as a tentative indicator of muscle mechanics, the sonic
muscle of the searobin appears to be capable of contraction rates in the
mid-range for sonic muscles and at rates similar to those reported for P.
scitiulus (Tavolga,
1964).
A number of characteristic acoustic traits identified in voluntary calls are also present in evoked calls. The commonality of these traits in voluntary and evoked calls suggests that they may reflect important features of the mechanics of the sonic motor system in searobins. The first few sound pulses are of low amplitude or are even missing, i.e. an action potential is present but no obvious sound is recorded. Action potentials that failed to produce acoustic pulses were more common at lower temperatures in voluntary calls and at stimulation rates above 150 Hz in evoked calls. Also, a gradual increase in amplitude of the sound pulses within a call is evident in both voluntary and evoked calls. Action potentials without resultant sounds and delayed amplitude maxima are probably due to an interaction of calcium release and reuptake, sonic muscle twitch characteristics and swimbladder displacement resulting in constructive interference.
Low initial sound amplitude and a gradual increase to maximum amplitude can
be see in the traces of evoked calls in toadfish
(Fine et al., 2001) and
voluntary calls in midshipman (Cohen and
Winn, 1967
). When the toadfish sonic nerve is stimulated at 200
Hz, peak amplitude was reached at the sixth muscle twitch
(Fine et al., 2001
). In the
voluntary grunts (175200 Hz) produced by the midshipman, Porichthys
notatus, the fourth muscle twitch produced maximal sound amplitude
(Cohen and Winn, 1967
). Fine et
al. (2001
) used a laser
vibrometer to measure swimbladder displacement during sound production evoked
at 200 Hz. They observed that the swimbladder did not reach full oscillations
until the fifth or sixth action potential, coincident with peak sound
amplitude. Rome et al. (1996
)
observed a similar delay in the development of maximal force from bundles of
toadfish sonic fibres. Fine et al.
(2001
) have suggested that the
initial summation of bladder displacement and resultant low acoustic amplitude
may be the result of the initial timing of calcium release and reuptake by the
sarcoplasmic reticulum. This hypothesis may explain the low initial amplitude
and, in conjunction with the concept of constructive interference (see below),
the gradual build up to maximal amplitude in voluntary and evoked searobin
calls. It may also explain the action potentials lacking acoustic pulses
observed at call onset in this study. In voluntary calls, the number of action
potentials without resultant sounds decreased with increasing temperature, and
a warmer sarcoplasmic reticulum can cycle (release and reuptake) calcium more
rapidly (Feher et al., 1998
).
More rapid cycling of calcium would allow the muscle to relax and twitch
again, producing a sound that might otherwise have been missing due to sonic
muscle twitch and bladder displacement summation early in the call.
Recordings of evoked and voluntary single twitches revealed a sound
consisting of two distinct waveforms of acoustic energy separated by 56
ms of relative quiet. One possibility is that these two pulses might represent
twitches of the two sonic muscles; i.e. a twitch of the contralateral muscle
might be responsible for the second waveform in unilateral EMG recordings.
However, this two-part waveform was confirmed in bilateral recordings. In
addition, the same double sound was produced by unilateral twitches evoked by
stimulation of one SN. As the sonic motor nuclei of the searobin only branch
ipsilaterally (Bass and Baker,
1991; Finger and Kalil,
1985
), a feedback mechanism from the stimulated SN to the
contralateral nerve is unlikely. Furthermore, duration, dominant frequency
(Table 1) and waveform shape
(Fig. 7) of the two waveforms
were distinct, suggesting that these sounds were not the result of identical,
alternate twitches of the two sonic muscles.
The two acoustic waveforms produced by a single twitch were nearly
identical to the `contraction' and `relaxation' sounds that Fine et al.
(2001) recorded from the
toadfish sonic muscle. Based on simultaneous bladder displacement and sound
measurements, they have modelled the movement of the bladder relative to the
positive and negative pressure peaks of the resultant sounds. Their model
suggests quadrupole movement of the swimbladder, rather than the monopole
movement associated with an oscillating sphere
(Harris, 1964
). They found
that the initial negative peak of the contraction sound represents inward
displacement of the side of the swimbladder by shortening of the sonic muscle.
The following positive pressure peak represents the outward displacement of
the bottom of the bladder caused by increasing internal pressure. The
relaxation sound begins with a positive pressure peak as the muscle relaxes
and the sides of the bladder move back out. The bottom then falls, producing a
negative peak, and as the bottom stops moving the sides complete their outward
movement, producing the final positive peak.
While this model of bladder movement
(Fine et al., 2001) accurately
describes the two waveforms produced by a single searobin sonic muscle twitch,
it cannot explain the extended interval of relative quiet between these two
waveforms. This 56 ms plateau between the contraction and relaxation
sounds represents an interval of relative stillness of the swimbladder and
would result from sonic muscle mechanics and/or the morphology of the
swimbladder. The interval between the toadfish contraction and relaxation
sounds coincides with minimal velocity of the bladder surface, indicative of
complete muscle contraction (Fine et al.,
2001
). It is possible that a delayed relaxation of the muscle
might produce the longer interval between the contraction and relaxation
sounds in the searobin. Alternatively, this interval might be the result of
swimbladder morphology. The searobin swimbladder is bi-lobed and distinct from
that of the heart-shaped toadfish bladder
(Evans, 1973
;
Tower, 1908
). The tapered oval
lobes are separated by anterior and posterior clefts and are connected only by
a constricted passage towards the anterior end of the bladder. Perhaps inertia
resulting from the constriction between the bi-lobed halves of the bladder
might delay the displacement waveform long enough to produce the interval.
This interval is crucial in allowing constructive interference and a resultant amplification of sound to occur during the searobin call. The peak negative pressure of the relaxation sound produced by one twitch coincides with that of the contraction sound of the next twitch of that sonic muscle (not the contralateral muscle; see Fig. 7). This process can be observed in evoked trains of sound at 50, 100 and 120 Hz (Fig. 9). At 50 Hz, the entire dual sound waveform can be seen between action potentials. At 100 Hz, the small negative acoustic pressure peak that appears just prior to the next action potential (and resultant contraction sound) is the relaxation sound of the preceding twitch. At 120 Hz, these two negative peaks superimpose. Each muscle twitch reinforces the next twitch of that muscle by compounding the displacement of the bladder, resulting in increased sound amplitude. Note that the first two acoustic pulses will not be reinforced in this manner. In addition to the cycling of calcium, this may help explain why some action potentials at call onset fail to produce an audible sound.
The same phenomenon has been observed in sounds evoked from toadfish sonic
muscles, but the reinforcement takes place at higher muscle contraction
frequencies. In the toadfish, the interval of 5.3 ms between contraction
and relaxation sounds should produce reinforcement of the next sound at 188
Hz, and such reinforcement can be observed at 200 Hz
(Fine et al., 2001
).
Similarly, the 9.3 ms interval in evoked calls in the searobin produces
maximal reinforcement at 107.6 Hz for one muscle. The longer interval between
the contraction and relaxation sounds in voluntary single twitches, 10.8 ms,
would produce maximal reinforcement at 92.7 Hz. Both of these values are close
to the 105.6 Hz mean frequency of contraction in a voluntary call.
Constructive interference and sonic fibre characteristics are both likely
to play a role in determining the range of stimulation frequencies at which
the searobin can produce maximum sound amplitudes (100140 Hz; see
Fig. 10A).Constructive
interference of negative pressure peaks might also explain the dominance of
negative acoustic pressure in the waveforms of searobin and toadfish calls
when both positive and negative acoustic pressure is evident in the sounds
produced by single twitches in both species
(Fine et al., 2001).
This constructive interference may be an inherent part of the mechanism of
sound production in searobins, toadfish and other species producing sound
via trains of muscle contractions rather than single twitches.
Although the sonic motor systems of toadfish and searobins are considered
homologous, they differ in three of nine compared vocal control traits
(Bass and Baker, 1991), in
sonic muscle function (synchronous vs alternate contraction) and in
swimbladder morphology (Evans,
1973
; Tower,
1908
). The appearance of an essentially identical mode of
constructive interference in both species suggests the importance of this
mechanism in amplifying sounds produced by a highly damped and inefficient
sound source such as a swimbladder
(Connaughton et al., 2002
;
Fine et al., 2001
). The timing
of the contraction and relaxation sounds produced by a single twitch plays an
essential role in this constructive interference and should be studied
further.
A final characteristic of both voluntary calls and evoked trains is rapid
damping, expressed by the greater duration and lower amplitude of the final
two sound pulses. Bilateral EMG recordings confirm that these attenuated sound
pulses were not produced by twitches of the contralateral sonic muscle. These
attenuated sounds do not represent resonance of the swimbladder, rather they
represent the relaxation sound of the final twitch of each alternately
contracting muscle (see Fig. 7;
Table 2). In evoked calls there
is only one attenuated sound because only one muscle is being stimulated.
Similarly, single attenuated sound pulses are observed in trains of evoked
sounds in toadfish (Fine et al.,
2001) and in voluntary calls of midshipman
(Cohen and Winn, 1967
). In one
case, a single muscle is being stimulated and in the other the sonic muscles
are contracting synchronously.
The rapid damping of the searobin sonic system supports the proposal that
swimbladders are low Q, broadly tuned sound sources and are unlikely
to resonate (Connaughton et al.,
2002; Fine et al.,
2001
). The swimbladder of the searobin produced sound at any
frequency imparted upon it, from 50 Hz to 360 Hz, and a
Q3dB of 1.98 was calculated based on these data. A
Q3dB of 1.45 has been reported for the toadfish
swimbladder (Fine et al.,
2001
), and frequency response curves generated by sounds evoked
from Galeichthys and Bagre
(Tavolga, 1962
) produce very
low Q3dB values of 0.89 and 0.33, respectively. The
time-course of sound produced by single muscle twitches in the searobin is
brief, and both evoked (11.7 ms) and voluntarily (14.1 ms) produced sounds
ended abruptly after the cessation of the action potential. Similar
short-duration, highly damped waveforms have been observed in toadfish
(Fine et al., 2001
) and
weakfish (Connaughton et al.,
2002
), supporting the hypothesis that swimbladders are inefficient
sound sources and need to be driven rapidly in order to produce sound
(Fine et al., 2001
).
The searobin can produce a call with a fundamental frequency of 200 Hz
while each muscle twitches at 100 Hz. A trade-off that accompanies this mode
of function is that only half of the total sonic muscle mass is displacing the
swimbladder during any given contraction, resulting in an average 3.3 dB
decrease in SPL when comparing bilateral and unilateral sounds. Decreased SPL
has been noted in other species when comparing unilateral and bilateral sound
production (Tavolga, 1962;
Winn and Marshall, 1963
), but
these species do not naturally contract their sonic muscles alternately.
A possible adaptation to the decrease in sound amplitude resulting from
contraction of only one sonic muscle at a time is a bigger or thicker sonic
muscle. In the present study, the more massive sonic muscles of the males
expressed a mass of 2.0% of total mass and a thickness of 1.8% of total
length. By comparison, the seasonal sonic muscles of the male weakfish
Cynoscion regalis express a mass of 3.2% of total mass and a
thickness of 1.6% of total length at the peak of the spawning season
(Connaughton and Taylor, 1994).
The sonic muscle of male Atlantic croaker (Micropogonias undulatus),
also seasonal, peaks at a mass of 1.8% and a thickness of 0.8% (S. Modla, M.
L. Lunn and M. A. Connaughton, unpublished data). The sonic muscle of the
calling, nest-building, type I male midshipman peaks at 1.5% of body mass
(Brantley et al., 1993
) and
that of male toadfish at
1.3% (calculated from a regression of sonic
muscle mass vs total mass in Fine
et al., 1990
). Although these data are limited, it appears that
searobin sonic muscle expresses the greatest relative thickness and second
greatest relative mass of those species examined thus far, perhaps as an
adaptation to compensate for decreased amplitude due to alternate contraction
of the sonic muscles.
The central and peripheral components of the searobin sonic motor system
have evolved to produce sound via a novel mode of
swimbladder-generated sound production. Central components, including
ipsilateral branching and alternate firing of the SN
(Bass and Baker, 1991),
generate alternate contractions of the sonic muscles. Peripheral components
are likewise specialized. Alternate contraction of the sonic muscles fulfils
the need for rapid movement of the swimbladder without the need for super-fast
mechanics (by the standards of sonic muscles), and optimal sound output for
these muscles occurs at relatively low frequencies (100140 Hz). Muscle
mechanics and/or swimbladder morphology result in constructive interference of
sequential relaxation and contraction sounds, maximizing signal amplitude at
typical muscle contraction frequencies. It is hypothesized that this
reinforcement may partially compensate for the loss in amplitude inherent in
the use of only half the total sonic muscle mass to displace the swimbladder
during unilateral muscle contraction. The relatively great mass and thickness
of the searobin sonic muscle may also play a role in compensating for loss in
amplitude due to alternate contraction. Although the impact of muscle twitch
force on sound amplitude has never been directly examined, it seems that
searobin sonic muscle function is a novel solution to the trade-off between
speed and force characterized in sonic muscles by the extremely fast, low
force toadfish sonic muscle (Rome et al.,
1999
).
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