Steady swimming muscle dynamics in the leopard shark Triakis semifasciata
Marine Biology Research Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093-0202, USA
* Author for correspondence (e-mail: jdonley{at}ucsd.edu)
Accepted 23 December 2002
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Summary |
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Key words: muscle activation, muscle strain, electromyography, sonomicrometry, shark, Triakis semifasciata
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Introduction |
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In addition to examining the roles of the two major muscle fiber types as a
function of swimming speed, numerous studies have investigated the timing of
red muscle activation at different positions along the body during steady
swimming. When superficial red muscle is active it contracts to produce local
bending of the body, and the wave of lateral motion that generates thrust is
the summation of the sequential muscle contractions along the body. Common
features of activation patterns during steady swimming among several teleost
species are that the wave of red muscle activation travels (1) down the body
in a rostrocaudal direction (Grillner and
Kashin, 1976; Williams et al.,
1989
; He et al.,
1990
; van Leeuwen et al.,
1990
; Jayne and Lauder,
1993
,
1995b
;
Gillis, 1998
;
Knower et al., 1999
;
Shadwick et al., 1999
) and (2)
faster than the propulsive wave of lateral displacement
(Grillner and Kashin, 1976
;
Wardle et al., 1995
;
Katz and Shadwick, 1998
).
Because the wave of muscle activation travels down the body faster than the
wave of lateral displacement, the phase of the muscle length change (strain)
cycle in which red muscle is active also varies along the body. This
observation led to research that focused on quantifying red muscle activity
and shortening at different axial positions; specifically, studies examined
the EMG/strain phase relationship. A common trend that has emerged among
teleosts is that red muscle activation typically occurs during muscle
lengthening (from 0 to 90° of the strain cycle) and offset occurs during
muscle shortening (typically 100250°)
(Altringham and Ellerby, 1999).
This pattern enhances positive power production in cyclic contractions of fish
muscle (Altringham and Johnston,
1990
). In addition, in many teleosts there is a decrease in the
duration of muscle activation towards the tail, a shift in the EMG/strain
phase at more posterior locations such that onset occurs relatively earlier in
the strain cycle (Williams et al.,
1989
; van Leeuwen et al.,
1990
; Rome et al.,
1993
; Wardle and Videler,
1993
; Jayne and Lauder,
1995b
; Hammond et al.,
1998
; Shadwick et al.,
1998
; Ellerby and Altringham,
2001
; Knower et al.,
1999
), and a rostrocaudal increase in strain amplitude.
The importance of the longitudinal variation in the EMG/strain phase
relationship is that the timing of activation of a muscle relative to its
lengthening and shortening cycle, and the duration of muscle activation,
affect the net work produced and thus its mechanical contribution to swimming,
as has been shown in recent in vitro work loop studies. In some fish
species, the anterior musculature is hypothesized to produce the majority of
the power for thrust (van Leeuwen et al.,
1990; Altringham et al.,
1993
; Wardle and Videler,
1993
), whereas in other species the posterior musculature is
mainly responsible for thrust production
(Coughlin and Rome, 1996
;
Rome et al., 1993
;
Johnson et al., 1994
;
Jayne and Lauder, 1995b
). Some
fish species display a relatively constant pattern of power production along
the body (Shadwick et al.,
1998
; Ellerby et al.,
2000
; Syme and Shadwick,
2002
; D'Aout et al.,
2001
).
The main conclusions to be drawn from recent studies are that dynamic
muscle function varies longitudinally in many bony fishes and that different
species exhibit various patterns of muscle activation and strain in order to
optimize muscle function for their particular swimming behavior. Optimization
of muscle function along the body may be correlated with differences in
swimming mode (Wardle et al.,
1995). Since the earliest research on muscle function in fish
swimming, attention has been focused on bony fishes representing a wide range
of swimming modes. However, sharks also display a broad spectrum of swimming
modes, ranging from highly undulatory species (large lateral displacement over
much of the body) such as the leopard shark, to more stiff-bodied, tuna-like
species (lateral displacement restricted primarily to caudal region) such as
the lamnid sharks, yet virtually nothing is known about dynamic muscle
function in any shark species. To build a more complete picture of the
evolution of muscle function in fish swimming it is important to address the
following questions with respect to sharks: (1) which features of the muscle
dynamics found in teleosts also occur in sharks, (2) are there any regional
variations in patterns of muscle strain and activation in sharks as seen in
teleosts, and (3) are there differences in the muscle dynamics of sharks that
have different swimming modes? The present study addresses the first two
questions by examining the in vivo muscle dynamics of the leopard
shark Triakis semifasciata and comparing muscle function in this
coastal shark species with data that exist on bony fishes. Specific objectives
are to (1) characterize the patterns of muscle strain at different axial
positions, (2) compare the timing of red muscle activation relative to the
phase of the strain cycle at different axial positions, (3) determine if
longitudinal differences in EMG duration occur and (4) compare measured strain
to strain predicted from midline curvature derived from analysis of the
kinematics during steady swimming.
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Materials and methods |
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Surgical procedures
Surgery was performed to implant piezoelectric crystals and EMG electrodes
into the red muscle of each leopard shark for in vivo detection of
muscle strain and activation patterns. Prior to surgery, the fish were
submerged in seawater containing anesthetic (0.0139 g l1
ethyl p-aminobenzoate) and remained anesthetized typically for 30
min, but for no more than 60 min, throughout the procedure by recirculation of
the anesthetic across the gill surfaces. Following surgery, the fish were
allowed to recover in fresh seawater and placed into the swim tunnel to become
acclimated to the test chamber prior to data collection.
Sonomicrometry
Pairs of 2 mm barrel piezoelectric ceramic crystals (Sonometrics Corp.,
Ontario, Canada), one acting as an acoustic transmitter and the other as a
receiver, were first calibrated in seawater and then implanted using a
13-gauge hypodermic needle at three axial positions (0.42±0.024
L, 0.61±0.02 L and 0.72±0.023 L)
(Fig. 1). Pairs of crystals
were implanted into the subcutaneous red muscle parallel to each other just
ventral to the lateral line on the left side of the body. The crystals were
implanted perpendicular to the longitudinal axis of the body, so the bending
movements of the shark would not cause slippage of the crystals within the
muscle or prevent restriction of movement of the crystal head. They were
implanted at the same depth within the muscle (2.0 mm) to avoid miscalculation
of changes in muscle length. The proper position and orientation of the
crystals was maintained by anchoring the crystal wires to the skin in several
locations along the left side of the body and along the dorsal surface with
sutures and Vetbond tissue adhesive. The wires were then bundled together to
prevent tangling. Sonometric data were collected digitally at a frequency of
500 Hz during periods of steady swimming when the shark was positioned in the
center of the flow chamber. At the end of each experiment, crystal depth and
body width at implantation sites was recorded. Sonometric data were filtered
in AcqKnowledge 3.5 (Biopac Systems Inc.) using a Blackman-92db FIR 60 Hz band
stop filter. This filter removed from the sonometric data the electrical noise
produced by the swim tunnel motor.
|
Electromyography
During the surgery for sonomicrometry, EMG electrodes were implanted into
the red muscle approximately 12 mm apart at the same depth and axial
position as the sonometric crystals. The electrode wires were anchored to the
skin with sutures and tissue adhesive and bundled together with the crystal
wires. EMG signals were amplified using a.c. preamplifiers (Grass Instrument
Co., West Warwick, USA), band-pass filtered (31000 Hz), and recorded
simultaneously with the sonometric data at 500 Hz. With a sample frequency of
500 Hz and a typical tailbeat period of 1 Hz, the error in EMG timing did not
exceed 2 ms or an error of 0.2% of one cycle.
Analysis of sonometric and EMG data
Selection criteria
In order to select a series of tailbeat cycles for analysis, the following
criteria were established: (1) the data must correspond to periods when the
shark swam for 10 or more consecutive complete tailbeat cycles in the center
of the chamber, and (2) the EMG traces must display a signal in which the
onset and offset of EMG activity were discernible. Because of difficulty in
eliminating all sources of electrical noise during data collection, some of
the sonometric and EMG data traces were not adequate for analysis. Therefore,
EMG data for the anterior position (0.42 L) are presented for eight
individuals, for the mid body position (0.61 L) for nine individuals,
and for the posterior position (0.72 L) for four individuals.
Sonometric data for the anterior and mid body positions are presented for nine
individuals, and for the most posterior location for four individuals.
Muscle strain
Muscle strain was calculated from the muscle length traces recorded during
steady swimming. Muscle strain amplitude was calculated by subtracting the
mean muscle length from the peak of the waveform and dividing this difference
by mean length.
EMG/strain phase and EMG duration
The muscle strain waveform was periodic and therefore the phase of the
strain cycle was designated in degrees (from 0 to 360), the start of each
strain cycle (0°) being the point at which mean muscle length was achieved
during lengthening (see Altringham and
Johnston, 1990). Using AcqKnowledge 3.5 (Biopac Systems Inc.), EMG
traces were filtered with a Blackman-92 db FIR high-pass filter with a cut-off
frequency of 3 Hz (to remove low-frequency movement artefact) and a 60 Hz band
stop filter to remove the electrical noise created by the swim tunnel motor.
Timing of onset and offset of activation were determined using a voltage
threshold method described in Knower et al.
(1999
). The temporal
relationships between onset and offset of activation and the muscle strain
cycle were expressed in degrees. The duration of muscle activation was
calculated from the onset and offset times for each tailbeat cycle. EMG/strain
phase and EMG duration data presented in this paper represent an average of
multiple tailbeat cycles for each fish.
Fig. 2 illustrates one complete
strain cycle with the corresponding EMG trace; the vertical lines in
Fig. 2B indicate the positions
at which onset and offset of activation occurred.
|
Kinematic analysis
Concurrent with measurements of instantaneous muscle length changes and EMG
activity, each individual was videotaped at 60 Hz with a Canon Inc. digital
camera (model XL1) while swimming against a current of known velocity in a
swim tunnel. The variable-speed swim tunnel used in these experiments has been
described in Graham et al.
(1990). When the fish
maintained its position in the flow chamber, its swimming speed was determined
from the speed of the current inside the chamber. To synchronize the
collection of sonometric, EMG and video recordings, a flashing red diode was
recorded in the video sequences and its excitation voltage was recorded with
the sonometric and EMG data.
The camera was positioned approximately 1 m directly above the working section of the swim tunnel to obtain a dorsal view of the fish (Fig. 3). Video recordings were made over a 1045 min period at a speed of approximately 1.0 L s1 (total body lengths s1). Video segments in which the fish completed four or more symmetrical tailbeats near the center of the chamber and that corresponded to acceptable strain and EMG data for all axial locations were selected for kinematic analysis.
|
The purpose of the kinematic analyses was to correlate patterns of body bending captured on videotape with measurements of local muscle activation and strain. 32 equally spaced points along the dorsal outline were digitized in sequential video fields using Scion Image (Scion Corporation, www.scioncorp.com). Dorsal outlines were confined to the mid and posterior regions of each fish, beginning anteriorly at the trailing edge of the pectorals (approx. 0.3 L) and ending at the tip of the caudal fin. A scaling factor was calculated for each video sequence using a 10 cm grid on the bottom of the chamber.
A cubic spline function was used to convert the point coordinate data of
each digitized outline into complete curves (see
Jayne and Lauder, 1995a). A
dorsal midline for each field was then calculated using a computer algorithm
and this midline was divided into 50 equally spaced segments. The progression
of these points in the y-direction (perpendicular to axis of
progression of the fish) was used to calculate lateral amplitude along the
body through a series of consecutive tailbeat cycles. Lateral displacement was
defined as the peak-to-peak lateral amplitude divided by two. A mean value was
calculated from four consecutive tailbeat cycles in nine fish. To allow for
comparison of individuals of different sizes, lateral displacements were
expressed in units relative to body length (% L).
Propulsive wave velocity C, defined as the speed of the wave of
lateral motion that travels along the body rostrocaudally, was calculated from
the lateral displacement data by dividing the distance between two designated
points on the body, the anteriormost position observed in consecutive video
frames (0.3 L) and the tip of the caudal fin, by the time between
peaks of lateral motion at these two axial positions. Propulsive wavelength
() was then calculated as C divided by mean tailbeat
frequency (tbf).
Curvature
Using the point coordinate data of the dorsal midline, curvature was
calculated as described in van Leeuwen et al.
(1990), Rome et al.
(1992
), Coughlin et al.
(1996
) and Katz and Shadwick
(1998
). The fish body was
treated as a dynamic bending beam in which the bending of segments along the
body was correlated with the local shortening of the red muscle. Midline
coordinate data were normalized in the x-direction (defined by the
direction of travel) and a fourth order polynomial equation was fitted to each
midline (see Katz and Shadwick,
1998
). r2 values ranged from 0.98000 to
0.99999. Curvature K, defined as the inverse of the radius of
curvature, was calculated from the polynomial equations for several positions
along the dorsal midline (0.4 L, 0.5 L, 0.6 L, 0.7
L, 0.8 L and 0.9 L) in nine individuals using the
following equation:
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Statistics
Muscle dynamics
We investigated whether or not there was a significant difference among the
different body positions examined in terms of the degree of muscle strain, the
timing of onset and offset of activation, and duty cycle. Because these
parameters may vary both with position and among the individuals, a
multivariate analysis of variance (MANOVA) was performed in order to assess
the effects of position, individual and a position/individual interaction. In
addition, when individual effects were significant, an analysis of variance
(ANOVA) was performed on each individual in order to determine whether the
position effects were significant. A TukeyKramer pairwise comparisons
analysis was performed to identify specific differences in mean strain, the
timing of onset and offset of activation, and duty cycle between the three
different body positions.
Kinematics
The lateral displacement data were examined using a MANOVA to determine
whether there were any significant effects of body position, individual or
position/individual interactions. To examine the relationship between strain
values predicted from calculations of midline curvature and those values
measured using sonomicrometry, these data were also subjected to analysis of
variance with position and individual effects incorporated into the
statistical model. All statistical analyses were performed in Minitab (version
13) using a significance level of P=0.05.
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Results |
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Patterns in muscle activation
The timing of muscle activation was expressed in degrees relative to the
phase of the strain cycle, and duty cycle, defined as the time in which the
muscle was activated relative to the total time of the strain cycle, was
expressed as a percentage. At all three axial positions onset of activation
occurred during muscle lengthening and offset occurred during muscle
shortening (Fig. 5). Mean onset
of activation occurred at 54.2° in the anterior, 51.4° in mid and
61.8° in the posterior positions. Mean offset of activation occurred at
165.2° in the anterior, 163.1° in mid and 159.7° in the posterior
positions (Table 1). Duty
cycles were 30.9% in the anterior, 31.0% in mid and 25.8% in the posterior
positions.
|
In order to identify longitudinal variation in the timing of muscle activation, as with the analysis of the strain data, these data were subjected to a MANOVA using position, individual and position/individual interaction as the parameters in the statistical model. Statistical analysis indicated that there was no significant effect of body position (P>0.050) in both the onset and offset of activation as well as the duty cycle. There was a significant variation among individuals, however, so an additional analysis was performed. In order to remove the effect of individual variation from the statistical model and simply determine whether the timing of muscle activation was similar along the body in all sharks, an ANOVA was performed on the EMG/strain phase and duty cycle data for each individual. After removing the confounding effects of individual variation from the statistical model, there remained no significant longitudinal variation in the onset and offset of activation (P>0.050). Mean duty cycles were also statistically similar at all three body positions (P>0.050).
Lateral displacement
Kinematic analysis was performed on nine leopard sharks in which mean
lateral displacement of the dorsal midline was calculated for each fish over a
series of approximately five tailbeat cycles. Lateral displacement D
was expressed as a percentage of total body length (% L). Position
along the body was represented as a fraction of total length L.
Displacement data were collected for positions along the body between 0.3
L and 1.0 L. Lateral displacement varied significantly
(P<0.001) with axial position and ranged from 1.43±0.22 at
0.3 L to 9.95±0.87 at 1.0 L. D increased rapidly over
the posterior half of the body, reaching a maximum at the tip of the caudal
fin (Fig. 6).
|
Propulsive wave velocity and wave length
Average propulsive wave velocity C was lower than the speed of the
wave of muscle strain (Table
2). Propulsive wavelength was shorter than body length in
all individuals, indicating that more than one propulsive wave was traveling
along the body at any point in time, a result similar to those shown for
Triakis in previous studies (Webb
and Keyes, 1982
).
|
Muscle shortening in relation to body curvature and predicted
strain
Curvature as a function of time was calculated at several positions along
the dorsal midline, including those corresponding to the locations of
implanted crystals and electrodes. A comparison between the midline curvature
and muscle strain at a given point in time revealed that red muscle shortening
at all three body positions (0.42 L, 0.61 L and 0.72
L) closely matched the phase of local midline curvature
(Fig. 7).
|
Predicted strain values were calculated from curvature by multiplying the curvature by the distance between the crystals and the backbone. There was no significant difference between strain measured by sonomicrometry and strain predicted from midline curvature (P>0.050) at all three body positions (N=3).
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Discussion |
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Lateral displacement
Comparison of the lateral displacement as a function of body position
between the leopard shark and various bony fishes indicates that the leopard
shark is not an anguilliform swimmer (e.g.
Lindsay, 1978), but rather
swims with a subcarangiform mode of locomotion that is intermediate between
anguilliform (e.g. eel) and carangiform (e.g. mackerel), and characterized by
displacement amplitudes that increase rapidly over the posterior half of the
body (Webb, 1975
). For
example, lateral displacement increases from 2.8% at 0.5 L to 9.95%
at 1.0 L (Fig. 6).
Furthermore, the displacement at 0.5 L in the leopard shark is
approximately half that in the eel and double that observed in a mackerel (see
fig. 2 in Altringham and Shadwick,
2001
). A similar conclusion was reached by Webb and Keyes
(1982
), who examined the
kinematics of six species of free-swimming sharks, including Triakis,
and showed that patterns of undulation and the approximate number of
propulsive waves on the body at a given time were consistent with a
subcarangiform mode of locomotion.
Muscle shortening in relation to body curvature and predicted
strain
Dorsal midline curvature has been shown to provide an accurate
approximation of strain in teleosts with superficial red muscle
(Coughlin et al., 1996;
Shadwick et al., 1998
; Katz et
al., 1999). A comparison between the midline curvature and muscle length as a
function of time revealed that red muscle shortening is in-phase with local
curvature in the leopard shark (Fig.
7). Synchronization between muscle length changes and curvature
indicates that red muscle contractions are responsible for local bending of
the body, a result consistent with observations in teleosts with red muscle
closely associated with the skin. In addition, strain amplitude calculated
from a bending beam model closely matched strain measured at three body
positions (Fig. 7).
Muscle strain
Red muscle strain amplitudes observed in the leopard shark were similar in
magnitude to those observed in previous studies of teleosts. Strain varied
from ±3.9% in the anterior to ±6.6% in mid and ±4.8% in
the posterior position (Fig. 4;
Table 1). Hammond et al.
(1998) described strains of
3.3% at 0.35 L and 6.0% at 0.65 L in rainbow trout. These
values are similar to those observed in saithe
(Hess and Videler, 1984
), carp
(van Leeuwen et al., 1990
),
scup (Rome and Swank, 1992
;
Rome et al., 1993
), mackerel
(Shadwick et al., 1998
) and
bonito (Ellerby et al.,
2000
).
A trend commonly observed in teleosts is an increase in red muscle strain
from anterior to posterior, generally corresponding to an increase in lateral
displacement along the body (Hess and
Videler, 1984; Rome et al.,
1990
,
1993
;
Coughlin et al., 1996
; Knower
et al., 1998; Shadwick et al.,
1999
). Similar to teleosts, the leopard shark also displays an
increase in strain from the anterior to mid body region; however, unlike many
fishes, the tapering of the body leads to a decline in strain amplitude at 0.7
L. From 0.6 L to 0.7 L, body thickness decreases,
but curvature is similar at both positions, leading to a small decrease in
predicted and measured strain at 0.7 L (see Figs
7 and
8). This decrease in strain
near 0.7 L may simply be a consequence of the high degree of tapering
along much of the body that is seen in elongated fishes (e.g. European eel;
D'Aout and Aerts, 1999
) as
opposed to fishes with tapering confined largely to the peduncular region.
|
Patterns of red muscle activation
There is a high degree of similarity in red muscle activation patterns
along the body between the leopard shark and many fish species, in that the
onset of activation typically occurs late in the lengthening phase, while
offset occurs during muscle shortening. This activation pattern ensures that
muscle develops high force near peak length and actively shortens to produce
positive contractile work, and it is a requirement for optimizing power
production during steady swimming
(Altringham and Johnston,
1990).
In vitro work-loop studies have verified the difference in net
work produced by muscles operating under different patterns of strain and
activation. Recent in vitro work-loop studies approximating in
vivo patterns of strain and activation have revealed different trends in
muscle function among fishes. In some species there is little longitudinal
variation in muscle power output (Syme and
Shadwick, 2002). Conversely, other fish species have been shown to
produce net positive work at both anterior and posterior body positions
(Coughlin and Rome, 1996
;
Rome et al., 1993
;
Johnson et al., 1994
). Because
the amplitude of strain is greater in the posterior region, it was suggested
in these studies that power production originates mainly from the posterior
musculature. A third trend is that the anterior musculature has a greater net
positive work (muscles activated predominantly during shortening) than the
posterior musculature and thus produces the majority of power for thrust
production (van Leeuwen et al.,
1990
; Altringham et al.,
1993
; Wardle and Videler,
1993
; Hammond et al.,
1998
). Regardless of the pattern of power production, the
situation where posterior muscles are being lengthened while active during a
portion of the time in which the anterior muscle is actively shortening
probably occurs because of the time delay that accompanies the wave of
contraction traveling along the body. For example, in saithe peak power in the
anterior portion of the body occurred while the rear muscles were lengthening
and developing peak force (Altringham et
al., 1993
). In the leopard shark, a portion of the EMG/strain
cycle producing positive work in the anterior region occurred simultaneously
with active lengthening in the mid and posterior musculature
(Fig. 9). Stiffening of the
posterior musculature (due to active lengthening) concurrent with positive
power production by the anterior musculature may affect the transmission of
the wave of bending that travels from snout to tail during swimming, but the
functional significance of this is unknown.
|
Interestingly, the phase of muscle activation, as well as the duty cycle,
were similar along the body in the leopard shark. By contrast, all teleost
species that have been examined display some degree of longitudinal variation
in the phase of red muscle activation. This typically consists of (1) red
muscle activation occurring relatively earlier in the strain cycle in more
posterior locations (Williams et al.,
1989; van Leeuwen et al.,
1990
; Rome et al.,
1993
; Wardle and Videler,
1993
; Jayne and Lauder,
1995b
; Gillis,
1998
; Hammond et al.,
1998
; Shadwick et al.,
1998
; Ellerby and Altringham,
2001
; Knower et al.,
1999
) and (2) a decrease in the duration of muscle activation in
more posterior locations (van Leeuwen et
al., 1990
; Rome et al.,
1993
; Wardle and Videler,
1993
; Jayne and Lauder,
1995b
; Gillis,
1998
; Hammond et al.,
1998
; Shadwick et al.,
1998
; Ellerby and Altringham,
2001
; Knower et al.,
1999
). Because this negative phase shift in the timing of muscle
activation is a common feature in most teleosts and is also seen in aquatic
locomotion in eels (Gillis,
1998
) and snakes (Jayne,
1988
), Gillis
(1998
) proposed that this
phase shift may simply be a characteristic feature of axial-based undulatory
swimming. However, our study shows that this is not the case in sharks like
Triakis and therefore it does not appear to be a requirement for
locomotion in cartilaginous fishes that swim by body-caudal fin
propulsion.
Apparent differences between the pattern of red muscle activation in the
leopard shark and most teleosts may reflect differences in the evolution of
swimming in these two groups. Specifically, differential muscle function along
the body, which occurs in many teleosts, may have evolved after the divergence
of cartilaginous and bony fishes. In addition, many teleosts exhibit
longitudinal differences in red muscle twitch kinetics that accompany
differences in strain and activation patterns
(Altringham and Ellerby, 1999).
Given that there is no longitudinal variation in the EMG/strain phase
relationship in the leopard shark, we hypothesize that the power-producing
characteristics of the red muscle are also constant along the body in sharks
that share a similar red muscle distribution. We are currently testing this
hypothesis by performing in vitro work-loop studies. This will allow
us to better understand differences in the mechanics of swimming and its
evolution in bony and cartilaginous fishes.
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Acknowledgments |
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References |
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