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First published online July 20, 2006
Journal of Experimental Biology 209, 2952-2960 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02350
Sound production mechanism in carapid fish: first example with a slow sonic muscle
1 Laboratoire de Morphologie Fonctionnelle et Evolutive, Institut de chimie,
Université de Liège, B-4000 Liège, Belgium
2 CREMA-L'Houmeau (CNRS-Ifremer), BP 5, 17137 L'Houmeau, France
3 Laboratoire d'Ecophysiologie et Physiologie Animale, Université de
Liège, B-4000 Liège, Belgium
4 Department of Biology, Virginia Commonwealth University, Richmond, VA
23284-2012, USA
* Author for correspondence (e-mail: E.Parmentier{at}ulg.ac.be)
Accepted 26 May 2006
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Summary |
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Key words: Carapidae, sound production, sonic muscle, sonic mechanism, swimbladder
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Parmentier et al.,
2006). Sounds are most frequently produced by the action of
specialized fastcontracting striated muscles. Intrinsic sonic muscles
completely attach to the wall of the swimbladder, as in the Batrachoididae
Opsanus sp. (Demski et al.,
1973; Fine et al.,
1990) and Porichthys notatus
(Greene, 1924;
Bass and Marchaterre, 1989),
the Triglidae Prionotus sp., Bellator sp.
(Evans, 1973),
Eutrigla sp. (Hawkins and
Myrberg, 1983; Connaughton,
2004). Extrinsic sonic muscles have various origins and insertions
(Jones and Marshall, 1953;
Alexander, 1966,
Demski et al., 1973).
Generally speaking, these paired muscles insert on the swimbladder or a
neighbouring structure, which attaches to the swimbladder via
ligaments. Extrinisc muscles are found in different taxa including the
Ophidiiformes (Howes, 1992),
Holocentridae (Carlson and Bass,
2000) and Sciaenidae (Ono and
Poss, 1982; Connaughton et
al., 1997; Sprague,
2000).
Swimbladder sounds have a fundamental frequency ranging from 75 to 300 Hz,
which corresponds to the muscular contraction rate, placing sonic muscles
among the fastest in vertebrates (Rome et
al., 1996; Loesser et al.,
1997; Connaughton et al.,
2000; Fine et al.,
2001). The sonic muscles of the swimbladder in Opsanus
tau can generate power at 10 times the maximum frequency of white epaxial
muscles (Young and Rome,
2001). Additional studies on sonic muscles in Cynoscion
regalis (Sciaenidae), Prionotus scitulus (Triglidae), Arius
felis (Ariidae), Bagre marinus (Ariidae) and Terapon
jarbua (Terapontidae) place them among the `champions' of contraction
speed (Schneider, 1967;
Tavolga, 1967;
Sprague, 2000). This enormous
speed of the swimbladder muscles is due in part to their extremely fast
relaxation rate (Rome and Lindstedt,
1998). This characteristic results from numerous morphological and
biochemical adaptations, including specialization of protein isoforms
(Hamoir and Focant, 1981) and
the high concentration of intracellular components
(Pennypacker et al., 1985;
Rome et al., 1999). The fibres
and myofibrils of sonic muscles are also thinner
(Evans, 1973;
Fine et al., 1993), and
possess a more developed sarcoplasmic reticulum
(Hamoir and Focant, 1981;
Appelt et al., 1991;
Feher et al., 1998) than fast
white fibres (Eichelberg,
1976). This set of characteristics could facilitate rapid flows of
metabolites and calcium (Eichelberg,
1976; Fine et al.,
1990; Rome et al.,
1996; Feher et al.,
1998).
The sonic apparatus displays common characteristics in all known carapids
(Fig. 1)
(Parmentier et al., 2003a).
The first two vertebrae display epineural ribs that are movable in all
directions, and attach to the swimbladder by a distal ligament. The third
vertebra bears a broad, ossified swimbladder plate, which attaches to the
swimbladder and is fixed to the fourth epineural rib. The almost cylindrical
swimbladder may be divided into three regions
(Fig. 1B). The sonic muscles
insert on the anterior region; the wall of the second region, the `swimbladder
fenestra', is situated just under the swim bladder plate and is thinner due to
the lack of submucosa (Parmentier et al.,
2003a); the posterior region is long and narrow and firmly
attached to the abdominal vertebrae. The swimbladder fenestra is
teardrop-shaped on each side, and both parts are connected dorsally by a
segment of regular bladder tissue. Paired sonic muscles run from the upper
wall of the orbit to the anterior face of the swimbladder forward of the
swimbladder fenestra. These muscles present an unique helicoidal organization
(Parmentier et al., 2003b)
(Fig. 1C): central myofibrils
are straight whereas peripheral ones are more and more twisted. Sounds in
C. boraborensis, C. homei, C. acus and C. mourlani
and E. gracilis are species-specific
(Parmentier et al., 2003a;
Parmentier et al., 2006;
Lagardère et al., 2005)
although all species have a similar sonic bauplan
(Parmentier and Vandewalle,
2003).
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Biochemical, histochemical and morphological methods have been used to
examine sonic muscles and to compare them with epaxial muscles in Carapus
acus (Parmentier et al.,
2003b). Sonic muscles have features of both red (numerous
mitochondria, high glycogen content) and white (alkali-stable ATPase) fibres.
They differ also from the white epaxial muscle in the isoforms of the light
chain and heavy chain, in the position of the T tubules and in a unique
parvalbumin isoform that may aid relaxation.
In this study, the mechanism of sound production in carapids was examined by measuring twitch parameters of the sonic muscle, comparing sounds induced by slowly pulling on the sonic muscle to voluntary sounds, and finally by examining the motion of these artificially induced sounds on the swimbladder fenestra.
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Materials and methods |
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Carapus boraborensis
Twenty Carapus boraborensis (Kaup 1856) (total length
TL=18-25 cm) were collected by scuba diving in Opunohu Bay (Moorea,
French Polynesia) in March 2005. They were found inside specimens of sea
cucumber Bohadschia argus. They were stocked in tanks (15
m3) filled with running seawater. Sounds were recorded in a smaller
glass aquarium (0.9 mx0.5 mx0.4 m). Only females were used for the
experiments because they are easier to obtain. Carapus boraborensis
longer than 21 cm are females, and the sex ratio of this species is 3
females:1 male (Parmentier and Vandewalle,
2005). Males and females produce different sounds
(Lagardère et al.,
2005), and exclusive use of females allowed us to compare the same
type of sound. Two experiments were performed.
Following published protocol
(Lagardère et al.,
2005), a specimen of the host was placed in the centre of the
tank, and several individual Carapus boraborensis were introduced
successively into the aquarium. Sounds were recorded using an Orca hydrophone
(sensitivity: -186 dB re 1V/µPa) connected via an Orca-made
amplifier (ORCA Instrumentation, Brest, France) connected to a Sony TCD-D8
digital audio tape-recorder (recording band width: 20-22000 Hz ±1.0
dB). This system has a flat frequency response range (±3 dB) between 10
Hz and 23.8 kHz. The hydrophone was placed above the sea cucumber.
Seven females were deeply anesthetised with MS 222 and then rapidly dissected in order to expose the sonic mechanism. Manually generated sounds were obtained by pulling the sonic muscles forward with forceps. They were recorded in a small vessel (38 cmx28 cmx5 cm) full of seawater as described above. After recordings, head, body and swimbladder length were measured to the nearest millimetre with a vernier calliper.
There are potential hazards recording in small tanks because of reflections
and tank resonance (Akamatsu et al.,
2002). Akamatsu et al. provide formulae to calculate the resonant
frequency (Akamatsu et al.,
2002) and empirically determined that sound spectrum shape can be
measured without artefacts for a frequency range lower than the minimum
resonant frequency of the tank if a hydrophone is placed within an attenuation
length of the fish. The resonant frequencies of the tanks were 2560 Hz (0.9
mx0.5 mx0.4 m) and 3327 Hz (0.38x0.28x0.05 m),
respectively, and the hydrophone was placed within 23 cm of the fish.
After the sound recordings, the swimbladder plate was removed to expose the swimbladder fenestra and the insertions of the sonic muscle. The movement of the swimbladder was then filmed (Wild M10 binocular microscope, Heerbrugge, Switzerland, equipped with a Canon PowerShot S45 camera, Tokyo, Japan) while the sonic muscles were pulled with forceps. The microscope was coupled with a camera lucida that allowed measurement of the thickness of the swimbladder plate. The plate was progressively measured and then carved away from its posterior edge allowing a series of thickness measurements. Relative movements of the fenestra were determined by marking it with ink dots and taking a picture. A second photograph was then taken of the stretched fenestra. By superimposing the two pictures, it was possible to quantify relative movements of different parts of the fenestra.
The swimbladders of 14 females were removed, and their diameters and
lengths were measured with the Wild M10 binocular microscope and camera
lucida. Their calculated volume was used to obtain the equivalent radius of a
sphere. This radius was used to calculate the resonant frequency of the
swimbladder according to the formula for an underwater bubble
(Weston, 1967):
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where F is resonant frequency calculated for an underwater bubble;
R, radius (cm); 
, ratio of specific heats (=1.4); P,
pressure (atmospheric pressure + hydrostatic pressure); 
, water density.
To compare with the manually generated sounds, the resonant frequency was
calculated for a depth of 5 cm. Note that elongation of the bladder causes
only minor increases in resonant frequency
(Weston, 1967).
Carapus acus
Five Carapus acus Ratinesque (Brünnich 1768)
(TL=8-12 cm) were found in specimens of Holothuria tubulosa
obtained in front of the STA.RE.SO station (Calvi Bay, Corsica) in April 2004.
Fish were stored in a community tank (0.6 mx0.6 mx0.4 m) with
running seawater at 19°C. Recordings were made in a smaller tank (0.4
mx0.4 mx0.31 m). These fish were transported to the Aquarium
Dubuisson (Liège, Belgium) where their sonic muscles were stimulated
electrically.
The five fish were deeply anesthetised with MS 222 (500 mg l-1) and rapidly dissected to expose the sonic mechanism. The right and left ventral sonic muscles were ligatured together at their anterior and posterior ends, and the posterior ends were tied to a force transducer (P K30 type 351, Hugo Sach Elektronik-Harvard apparatus GmbH, Hugstretten, Germany). The opposite extremity was fixed, respecting the original in vivo length of muscles. Both muscles were stimulated simultaneously (0.1 ms pulses of 4 V and frequencies of 2, 5, 6, 8, 10, 13 and 20 Hz) with metal electrodes connected to an electrical stimulator (Stimulator P type 201, Hugo Sach Elektronik-Harvard apparatus GmbH).
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The sonic muscle terminates in a complex tendon, which includes a `hook' that fits over a tubercle on the dorsoanterior wall of the swimbladder (Fig. 4). Tendons of the right and left sonic muscles are connected by connective tissue within the anterior wall of the swimbladder. At rest, the hook is anchored over the bladder tubercle (Fig. 5). Muscle contraction pulls the anterior part of the swimbladder forward stretching the swimbladder fenestra, particularly at its forward end (Fig. 5). The caudal part of the bladder does not appear to move because it is decoupled from the anterior wall by the fenestra. Additionally, it is attached to the posterior margin of the third epineural rib, and its dorsal surface is firmly attached to the ventral face of the vertebrae. Contraction continues until the hook releases the tubercle allowing the anterior swimbladder and fenestra to snap back to their resting positions. Apparently guided by attached connective tissue, the hook returns to its locked position on the tubercle during muscle relaxation.
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Calculation of the resonant frequency of the bladder
Peak frequency of voluntary sounds was between 80 and 203 Hz. Voluntary
sounds were not compared against fish size since they are made by at least two
unseen fish within the body cavity of a sea cucumber. Peak frequency of
manually generated sounds in a 50 mm deep vessel of seawater decreased over an
octave (r2=0.28, P<0.001) from almost 500 Hz
in a 19.7 mm TL female with a 25.3 mm long bladder to about 170 Hz in
a 25.2 mm female with a 38 mm bladder (Fig.
8). These values were compared with the resonant frequency
calculated for the radius of swimbladders of an equivalent volume
(Weston, 1967). The calculated
resonant frequency values were about twice the measured values. This finding
strongly suggests that sound frequency is not determined by the natural
frequency of the swimbladder. Since the swimbladder is more likely to radiate
sounds with its lateral than its antero-posterior surfaces; a calculated
frequency from swimbladder radius, instead of equivalent radius, would make
this discrepancy even greater. Voluntary Carapus boraborensis sounds
were more sharply tuned (Q3dB=15, N=25;
Q3dB=quotient of the dominant frequency divided by the bandwidth 3
dB down from the peak frequency) than manually generated sounds
(4.3±0.3; P<0.001), but it is likely that opening the fish
could have changed its vibratory properties.
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; Sand and Hawkins,
1973; Bradbury and Vehrenkamp,
1998). An alternative explanation is that swimbladders are
inefficient low Q sources with minimal dependence on resonance because of
rapid damping by the swimbladder wall
(Fine et al., 2001;
Connaughton et al., 2002). In
this view, rapid speed in fish sonic muscles is necessary because sound
frequency is determined as a forced response to muscle contraction. As a
result, the rate of sonic muscle contraction determines fundamental frequency
in long duration calls (Fine et al.,
2001; Connaughton,
2004). In the oyster toadfish, for instance, a 250 Hz contraction
rate generates a sound with a 250 Hz fundamental frequency, and slow bladder
movements do not generate sound (Barimo and
Fine, 1998; Fine et al.,
2001). Sonic muscles of Bagre marinus, Galeichthys felis,
Prionotus scitiulus, Prionotus carolinus, Epinephalus guttatus and
Holocentrus sp. have been observed to tetanize between 150 and 400 Hz
(Tavolga, 1962;
Tavolga, 1964;
Gainer et al., 1965;
Connaughton, 2004). In
weakfish, which produce each sound pulse with a single muscle twitch, sound
frequency similarly appears to relate to the timing of bladder movement forced
by the sonic muscle contraction-relaxation cycle
(Connaughton et al., 1997;
Connaughton et al., 2002).
The carapid mechanism uniquely does not utilize fastcontracting muscles,
depending instead on a mechanical decoupling. Carapid fishes drive the bladder
with a slow muscle that puts the anterior bladder under tension and then trips
a release system that excites sound production. The muscle contraction rate is
dramatically slower than in other drumming muscles. The average dominant
frequency of the sounds in five different carapid species varies between 40
and 340 Hz (Parmentier et al.,
2003a; Parmentier et al.,
2006; Lagardère et al.,
2005). In C. acus, the dominant frequency of 340 Hz in
each isolated pulse (Parmentier et al.,
2006) does not correspond to the contraction rate of its sonic
muscle, which tetanizes in the vicinity of 10 Hz. Moreover, the manually
generated sound clearly demonstrates that the sound does not depend on the
contraction-relaxation cycle speed. On the other hand, the pulse period was
between 4.5 and 6.9 Hz in C. boraborensis
(Parmentier et al., 2003a;
Lagardère et al.,
2005), which likely corresponds to the muscle contraction rate. In
this case, the contraction rate of the muscle does not determine the main
frequency of the pulse but the pulse period. In the Ophidiiforme Ophidion
marginatum, sounds are composed of 1-27 pulses with a peak frequency of
1200 Hz (Mann et al., 1997;
Sprague and Luczkovich, 2001),
and a contraction-relaxation cycle at this rate would be physiologically
impossible. However, the pulse period is about 23 Hz, reinforcing the
assumption that, in this group, there is not a correspondence between sonic
muscle contraction and main sound frequency, but with the pulse period.
In carapids, calculations of the resonant frequency of the swimbladder
indicate that swimbladder resonance does not explain the recorded frequencies
(Fig. 7). The peak frequency is
lower than the calculated swimbladder resonant frequency, but it is higher
than dictated by the timing of a muscle twitch. Therefore, some other factor
must be driving the swimbladder. Cicada insects produce sound by rapid
buckling of a pair of domed tymbals situated on the sides of the first
abdominal segment (Pringle,
1954). This sound-producing system acts as a frequency multiplier
that converts the 117 Hz contraction frequency of each of the paired tymbal
muscles into the 4.3 kHz frequency of the insect's song
(Bennet-Clark, 1997;
Bennet-Clark and Daws, 1999).
In these insects, transduction of muscle energy into sound energy is a
two-stage process. Stage one uses muscle power to drive a small mechanical
resonator (=the primary resonator), which acts as the frequency-multiplier
that determines the song frequency
(Bennet-Clark, 1999). This
motion may then drive a second, larger acoustic resonator, from which the
sound is radiated. This second resonator was modelled in insects as a
Helmholtz resonator (Young,
1990; Bennet-Clark and Young,
1992), which consists of a cavity open to the outside via
a hole that has a real or notional neck
(Bennet-Clark and Young,
1994). Carapid sound production presents analogies with the insect
process.
The mechanical (=primary) resonator can correspond to the mechanical
decoupling, allowing the release of strain energy built up in the fenestra by
slow muscle contraction to be converted into acoustic energy. Movements of the
anterior edge and fenestra of the swimbladder appear to be decoupled from the
remainder of the bladder, which is rigidly attached to the vertebral column.
Carapus boraborensis sounds are sharply tuned; a Q3dB of
15 is considerably higher than values recorded for typical bladder sounds: it
is 1.9 in the searobin (Prionotus carolinus), 1.45 in the toadfish
(Opsanus tau), 0.89 in Galeichthys felis and 0.33 in
Bagre marinus, and 3 in the croaker (Micropogonius
undulates) (Connaughton,
2004; Fine et al.,
2004). Therefore, given the sharp tuning of carapid calls and
their slow muscles, we hypothesize that carapid sounds are generated by a
rapid release of the fenestra, which sets the swimbladder plate into motion;
energy from plate motion would then be transferred through the fenestra and
excite the bladder to produce sound. This forced vibration is possible due to
the modifications in the thickness of the swimbladder plate. The plate is
thicker at the anterior part with around 800 µm near its point of
articulation on the third vertebra, and it becomes progressively thinner
toward the posterior part; the posterior region of the swimbladder plate is
only about 20 µm at its connection with the swimbladder fenestra.
Despite numerous similarities between voluntary and manually generated
sounds, differences exist mainly in pulse duration and in Q3dB.
These differences could be due to tanks that can be subject to various
artifacts (Akamatsu et al.,
2002; Parvulescu,
1964), to differences in acoustic loading that would occur with
depth (Fine et al., 2004) or
to experimental manipulations: opening the fish could change the vibratory
coupling of the fenestra and swimbladder plate. Additionally, a second pair of
sonic muscles, the secondary sonic muscles
(Courtenay and McKittrick,
1970), could also influence sound production. These muscles
originate on the posterior part of the skull and insert on the two first
epipleural ribs (Fig. 1A),
which are connected to the anterior part of the swim bladder by ligaments.
According to Parmentier et al., the contraction of these muscles causes
forward and outward displacement of the posterior tips of the epipleural ribs,
stretching the swimbladder and making it more rigid
(Parmentier et al., 2003a).
The increased stiffness of the swimbladder should help to sustain the sound.
These muscles were not tensed in the manually generated sounds.
This study demonstrates for the first time that rapid muscle speed is not
required to generate sounds in a teleost fish. However, carapid sonic muscles
have characters of both red and white fibres
(Parmentier et al., 2003b) as
is the case in fast sonic muscles (Ladich
and Fine, 2006; Parmentier and
Diogo, 2006). It appears that these sets of characters should be
carefully interpreted.
Superfast muscles generate low forces
(Rome et al., 1999). The
production of high forces by `superslow' muscles is not yet shown. An
important feature lies in the unique myofibrillar helical organisation
providing the muscle with spring-like mechanical properties
(Parmentier et al., 2003b).
The uncoiling of the helix during relaxation should help in the lengthening of
the muscle during relaxation and may aid in the recoupling between the hook of
the muscle tendon and the tubercle of the swimbladder.
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Acknowledgments |
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References |
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