Weakfish sonic muscle: influence of size, temperature and season
1 Washington College, Department of Biology, 300 Washington Avenue,
Chestertown, MD 21620, USA
2 Department of Biology, Virginia Commonwealth University, Richmond, VA
23284-2012, USA
3 College of Marine Studies and Department of Biological Sciences,
University of Delaware, Newark, DE 19716, USA
* e-mail: martin.connaughton{at}washcoll.edu
Accepted 13 May 2002
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Summary |
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Key words: sound production, reproductive behaviour, dominant frequency, sound pressure level, pulse duration, repetition rate, muscle hypertrophy, testosterone, swimbladder, acoustics, secondary sexual character, weakfish, Cynoscion regalis
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Introduction |
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Fish sonic muscles are adapted for speed and are considered to be the
fastest-contracting vertebrate skeletal muscles
(Rome and Lindstedt, 1998).
The sonic muscles of the squirrelfish (Holocentrus sp.) and
midshipman (Porichthyes notatus) can contract at over 100 Hz
(Gainer et al., 1965
;
Cohen and Winn, 1967
), and the
toadfish (Opsanus tau) sonic muscle can contract at over 400 Hz
without reaching tetany (Skoglund,
1961
; Rome et al.,
1996
; Fine et al.,
2001
). The fibers of toadfish sonic muscles express a number of
structural, biochemical and biophysical adaptations for speed, including an
unusual radial morphology (Fawcett and
Revel, 1961
; Fine et al.,
1993
; Loesser et al.,
1997
), multiple innervation
(Gainer and Klancher, 1965
;
Hirsch et al., 1998
), the
positioning of the triads over the A/I boundary
(Fawcett and Revel, 1961
), a
large volume of sarcoplasmic reticulum
(Franzini-Armstrong and Nunzi,
1983
; Appelt et al.,
1991
) with a huge Ca2+ capacity
(Feher et al., 1998
), the
fastest Ca2+ spike known in a vertebrate muscle and extremely rapid
cross-bridge detachment (Rome et al.,
1996
,
1999
). Weakfish sonic muscle
fibers share similar radial morphology and multiple innervation, as well as
expressing well-developed folding of the postsynaptic membrane, not reported
in other fishes (Ono and Poss,
1982
).
In this paper, we review our research on weakfish sonic muscles and their use in sound production. We have three goals. First, we will characterize the sounds produced by the weakfish, their periodicity (seasonality) and behavioral role. Second, we will describe seasonal hypertrophy and atrophy of the muscle, including its endocrine basis and the morphological changes occurring in the muscle. Finally, we will describe the influence of size, temperature and season (i.e. muscle mass) on the acoustic parameters of weakfish disturbance calls. We use these data to formulate a hypothesis for the mechanism of sound generation in weakfish.
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Sound production and spawning |
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Field and laboratory studies indicate a close link between male drumming
behavior and reproductive activity. In Delaware Bay, weakfish form spawning
aggregations in shallow, in-shore waters during May, June and July
(Taylor and Villoso, 1994;
Connaughton and Taylor, 1995a
).
Hydrophone recordings in Delaware Bay indicate that drumming activity is
always more intense in-shore than in deeper, offshore waters. Drumming is also
strongly seasonal, increasing abruptly to near peak levels in mid-May and
waning in late July (Connaughton and
Taylor, 1995a
). Reproductive data, including male and female gonad
condition, male plasma androgen levels, sperm motility and the percentage of
males running ripe (producing milt when handled), indicate that spawning
activity for this population peaks during the period of maximal drumming
activity (Connaughton and Taylor,
1995a
). Drumming activity also exhibits a diel periodicity,
peaking in the early evening (Connaughton
and Taylor, 1995a
) when weakfish spawning activity is at its
maximum, as indicated by the percentage of hydrated eggs in the ovaries and
back-calculation of time of fertilization from collected larvae
(Taylor and Villoso,
1994
).
Positive identification of the sounds recorded in the field and the role of
these sounds in courtship were examined in captive weakfish
(Connaughton and Taylor,
1996a). The calls of captive, spawning weakfish were identical to
the sounds recorded in the field. Audio and video recordings of captive
weakfish indicate that the rate of calling by the male does not increase as
the spawning event approaches. Drumming may begin before or after the first
spawning event and continues for several hours after the last one of the
evening, but it is maintained at a relatively constant rate until the behavior
ceases. In addition, drumming ceases prior to spawning and is apparently not
involved in the timing of gamete release in weakfish
(Connaughton and Taylor,
1996a
) or in two other sciaenids, red drum Sciaenops
ocellatus (Guest and Lasswell,
1978
) and Atlantic croaker Micropogonias undulatus (M. A.
Connaughton and M. L. Lunn, unpublished data). Male courtship drumming
therefore probably functions to attract a female, although this could not be
experimentally determined in the small tanks used for these studies. The high
turbidity of the inshore waters in which these fish reproduce
(Biggs et al., 1983
), the
evening spawning habit (Taylor and
Villoso, 1994
; Connaughton and
Taylor, 1995a
) and the absence of external sexual dimorphism that
might serve as visual cues support this hypothesis. Drumming may also act as a
rallying call for the formation of spawning aggregations, as has been
suggested for haddock Melanogrammus aeglefinus
(Templeman and Hodder, 1958
).
As pair spawning was observed in captivity, drumming may play a role in mate
selection. Variation in acoustic signals with fish size (Connaughton et al.,
1997
,
2000
) could also provide
females with a basis for choice among several calling males (see below).
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Seasonal cycles in the sonic muscle |
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Sonic muscle hypertrophy results from increases in fiber cross-sectional
area. Fiber diameter averages 40 µm during the spawning season and 23 µm
during the off-season (Connaughton et al.,
1997). Both the contractile cylinder (myofibrils and sarcoplasmic
reticulum) and the peripheral sarcoplasm increase in size. The late-summer
atrophy of the muscle reflects decreasing contractile cylinder size and the
virtual disappearance of the peripheral sarcoplasm in conjunction with a
significant decrease in muscle protein content. Ono and Poss
(1982
) observed a fiber
diameter of 29.6 µm in specimens collected in late August, after sonic
muscle atrophy had begun. Muscle glycogen and lipid content decrease
precipitously during early June as these energy stores are used, but muscle
mass, protein content and fiber cross-sectional area do not decrease until
later in the summer as androgen levels decrease (Connaughton and Taylor,
1994
,
1995a
;
Connaughton et al., 1997
).
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Variation in call characteristics: influence of temperature, size and season |
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The effects of temperature on acoustic characteristics were determined by
recording eight similarly sized fish (28-31 cm) at 18, 23 and 12 °C, and
again at 18 °C (Connaughton et al.,
2000). Temperature changes took place over 3-4 days, and fish were
then allowed to acclimate to each temperature for a minimum of 4 days.
Recordings were made twice at 18 °C to control for possible effects of
on-going muscle atrophy on acoustic characteristics. Repetition rate increases
with temperature as a result of its effect on the pulse pattern-generator
circuits in the central nervous system
(Demski et al., 1973
). Over
the temperature range 12-23 °C, mean repetition rate increased from 13.4
to 24.3 Hz. Similar changes in repetition rate with temperature have been
noted in a number of sound-producing teleost species
(Schneider, 1967
;
Fine, 1978
;
Bass and Baker, 1991
). SPL also
increases with temperature (from 69.6 to 79.5 dB), suggesting a faster twitch
time in warmer muscle.
The rate of Ca2+ uptake in toadfish sonic muscle sarcoplasmic
reticulum increases at higher temperatures, which would support more rapid
contraction (Feher et al.,
1998). As acoustic amplitude is proportional to volume velocity,
which is the product of surface area and the movement velocity of the
swimbladder surface (Bradbury and
Vehrenkamp, 1998
), SPL will increase with greater movement
velocity generated by faster muscle twitches. Similarly, dominant frequency
increases from 494 to 554 Hz across the 11 °C change in temperature. It is
unlikely that this temperature range would change the resonant frequency of
the swimbladder; the standard resonance equation for an oscillating bubble
does not contain a temperature variable
(Harris, 1964
). Therefore, we
argue that dominant frequency is determined by the forced response to muscle
contraction rather by than the natural frequency of the swimbladder. Finally,
pulse duration, which is inversely proportional to frequency, decreases with
increasing temperature (from 3.7 to 3.4 ms), supporting the notion of faster
twitches.
Eleven fish ranging in total length from 25 to 36 cm were recorded at 18
°C to examine the effect of fish size on acoustic parameters
(Connaughton et al., 2000).
Repetition rate does not change with fish size, indicating that the output of
central pattern generators is independent of fish size. SPL increased by 9.7
dB, from 65.6 to 75.3 dB, across an 11 cm increase in total length. Increasing
SPL with size may be attributed to increasing swimbladder size in larger fish
(Hill et al., 1987
). A larger
swimbladder has a greater surface area, resulting in an increase in the volume
velocity and, consequently, acoustic pressure. Dominant frequency decreases
(from 560 to 479 Hz) and pulse duration increases (from 3.3 to 3.9 ms) with
fish size. We argue against a resonance interpretation for the decrease in
frequency because of the inverse relationship between pulse duration and
dominant frequency (Fig. 3A,B);
pulse duration would not be affected by the natural frequency of the bladder.
A scaling argument suggests that a larger muscle with longer fibers would take
longer to complete a contraction, resulting in both a longer pulse duration
and a lower acoustic frequency in larger fish
(Hill, 1950
;
Wainwright and Barton,
1995
).
|
The influence of season on call characteristics reflects the seasonal
hypertrophy/atrophy cycle of the muscle. SPL increases by 6 dB (a doubling of
acoustic pressure) (Bradbury and
Vehrenkamp, 1998) from 59.8 to 65.7 dB with the seasonal tripling
in sonic muscle mass. Pulse duration also decreases slightly, although there
is no significant change in dominant frequency or repetition rate
(Connaughton et al., 1997
).
Acoustic pressure is proportional to volume velocity and, as there is no
indication that swimbladder size varies seasonally, it is likely that the
increased SPL with muscle mass is due to faster movement of the sonic muscle,
which is supported by the slight decrease in pulse duration with increasing
muscle mass. Although seasonal changes in muscle fiber morphology include
increases in both myofibrillar and sarcoplasmic area, the mechanism relating
the effect of increased muscle mass on SPL to pulse duration has not been
examined.
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Mechanisms of sound generation |
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The variation in dominant frequency with temperature also indicates that
sonic muscle twitch speed, and not the natural frequency of the bladder,
determines acoustic frequency because only the former will vary with
temperature (Harris, 1964).
Finally, there is a tight inverse relationship between pulse duration and
dominant frequency across a wide range of temperatures and fish sizes. Indeed,
the inverse of the second cycle of acoustic energy (with the greatest
amplitude) matches the dominant frequency almost perfectly
(Fig. 3C). These data support
the hypothesis that acoustic frequency is determined by the velocity of the
sonic muscle twitch rather than by the natural frequency of the swimbladder,
i.e. we are extending established results on fish sounds produced by trains of
muscle contractions to ones produced by a single twitch.
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Concluding remarks |
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Acknowledgments |
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