Patterns of red muscle strain/activation and body kinematics during steady swimming in a lamnid shark, the shortfin mako (Isurus oxyrinchus)
1 Marine Biology Research Division, Scripps Institution of Oceanography,
University of California, San Diego, La Jolla, CA 92093-0202, USA
2 Pfleger Institute of Environmental Research, Oceanside, CA 92054,
USA
3 Department of Zoology, University of Tübingen, Auf der Morgenstelle
28, 72076 Tübingen, Germany
* Author for correspondence (e-mail: jdonley{at}ucsd.edu)
Accepted 29 March 2005
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Summary |
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Key words: muscle activation, strain, swimming, lamnid, Isurus
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Introduction |
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Considering the amount of interest in the swimming mechanics of fishes, it
is surprising that few studies have examined dynamic muscle function in
elasmobranchs. In a previous study, we found that the leopard shark
(Triakis semifasciata), a common temperate subcarangiform swimmer,
lacks longitudinal variation in the timing of RM activation with respect to
muscle strain (Donley and Shadwick,
2003). These findings are in contrast with values reported for
most bony fishes and have fueled hypotheses regarding the evolution of muscle
mechanical design in these two distantly related groups of fishes.
As in bony fishes, sharks also display a broad spectrum of swimming modes,
ranging from species with a high degree of lateral undulation (such as the
leopard shark) to more tuna-like species such as the lamnid sharks (Family
Lamnidae) (Donley et al.,
2004). The present study examines steady-swimming kinematics and
muscle dynamics in a lamnid shark, the shortfin mako (Isurus
oxyrinchus). Furthermore, it considers specific aspects of the
morphological relationship between the RM and intermuscular tendons. Specific
objectives are to (1) examine longitudinal patterns of RM activation and
strain in the mako during steady swimming and clarify modes of transmission of
muscular forces along intermuscular tendons, (2) quantify patterns of body
curvature and lateral displacement derived from analysis of the swimming
kinematics and (3) compare these results with kinematic and muscle dynamic
characteristics investigated previously in the leopard shark to test the
hypothesis that the lack of longitudinal variation in the EMG/strain phase
relationship is a characteristic consistent among sharks that utilize
different modes of body/caudal fin propulsion.
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Materials and methods |
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Sonomicrometry and electromyography
Surgery was performed on anesthetized individuals (0.0028 g
l1 ethyl p-aminobenzoate) partially submerged in a seawater
bath to implant precalibrated piezoelectric crystals and EMG electrodes for
in vivo detection of instantaneous muscle segment length changes
(strain) and activation patterns (as described in
Shadwick et al., 1999;
Donley and Shadwick, 2003
)
(Fig. 1). The two axial
positions (0.4±0.02L, anterior; 0.6±0.04L,
posterior) chosen for this study encompass much of the longitudinal
distribution of RM in the mako (Bernal et
al., 2003
). Anterior to 0.35L and posterior to
0.65L, the mass of red muscle (RM) is relatively small and therefore
the accuracy in crystal placement declined when attempting to implant crystals
more rostral or caudal to these positions. To implant the crystals, a 2-mm
incision was made in the skin directly dorsal to the desired region of the
muscle and a puncture was made in the underlying tissue using a 15-gauge
hypodermic needle precalibrated to the required depth. Crystals were implanted
in a longitudinal orientation approximately 15 mm apart such that the degree
of shortening and lengthening of myotomes could be measured. This orientation
prevented the bending movements of the shark from causing slippage of the
crystals within the muscle and avoided damaging the lateral vascular rete.
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Crystal pairs and EMG electrodes were implanted into the deep RM at
anterior and posterior axial positions (N=6). Furthermore, six
additional experiments were performed in which a third set of sonomicrometric
crystals was implanted in the white muscle (WM) adjacent to and at the same
depth as a pair of crystals in the RM (N=3 for anterior; N=3
for posterior) to assess the degree of shearing between the RM and surrounding
WM. To identify any differences in the amount of strain within the RM mass at
a given body position, we also implanted two pairs of sonomicrometric crystals
at the same posterior axial position within the RM, one pair located more
medially and the other more peripherally within the RM mass. At the same axial
position, a third pair was implanted into the WM. During the recovery period
following surgery, we recorded muscle length changes during passive simulated
swimming movements induced by gentle side-to-side motion of the center of mass
that generated body undulation. After the sharks had completely recovered from
the anesthesia, muscle dynamics were recorded during active steady swimming
while sharks swam at speeds of 0.51.0 L
s1.
For each individual, muscle strain was calculated for 2550 tailbeat
cycles. Amplitudes represent the difference between peak and mean muscle
segment length divided by mean segment length. The muscle strain waveform was
periodic and therefore the phase of the strain cycle was designated in degrees
(from 0 to 360) as described in Altringham and Johnston
(1990). In AcqKnowledge, a
voltage threshold was set to determine the timing of onset and offset of
activation of the EMG bursts with precision over multiple tailbeat cycles (see
Knower et al., 1999
). The
temporal relationships between the onset and offset of activation and muscle
strain were expressed in degrees of the tailbeat cycle (0° is mean muscle
length during lengthening, 90° is peak length). Duty cycle (expressed in
both degrees and as a percentage of the strain cycle period) was calculated as
the duration of EMG activity relative to the total duration of the strain
cycle. EMG/strain phase and duty cycles are presented as an average of
2550 tailbeat cycles for each fish. A sample data set from one
individual, illustrating the sonomicrometric and EMG data common to all fish,
is provided in Fig. 1. RM
strain amplitudes are presented for eight individuals for the anterior
position and for seven individuals for the posterior position. EMG data for
both axial positions are presented for seven individuals.
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Propulsive wave velocity (C), the speed of the wave of lateral
motion that travels along the body from snout to tail, was calculated by
dividing the distance between the anterior and posterior positions by the time
it took for the wave of lateral displacement to travel between these two
points on the body. Propulsive wavelength () was calculated by
dividing C by mean tailbeat frequency.
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Morphology
Microdissections of a cleared and stained specimen and standard
histological techniques (20 µm; Azan-Domagk staining;
Gemballa et al., 2003) were
employed to characterize the position and trajectory of the hypaxial lateral
tendon within the red and white musculature. Details of the techniques were
described previously (Donley et al.,
2004
; Gemballa et al.,
2003
).
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Results |
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Muscle and body kinematics
Curvature (K) and lateral displacement (D) were
calculated for several axial positions along the dorsal midline from video
images of steady-swimming bouts. Predicted muscle strain was calculated from
curvature for sites corresponding to those where muscle segment length
recordings were made. In all individuals, the peaks in predicted strain (and
curvature) preceded (in time) the peaks in measured RM strain (N=5).
Amplitudes of predicted and measured RM strain were similar, with predicted
strain values of approximately ±7% in the anterior and ±9% in
the posterior. Phase shifts of curvature relative to measured RM strain ranged
from 58 to 64 ms, with a mean of 60.5 ms, corresponding to 8% of the
tailbeat cycle period. RM is therefore uncoupled from local body curvature and
shortens in phase with curvature at more posterior locations, as illustrated
in Fig. 3, where RM strain at
0.42L occurred in synchrony with midline curvature at 0.6L.
As a direct measure of the degree of uncoupling that can occur between active
RM and inactive WM, we compared timing of RM and WM strain waveforms at
0.4L during simulated and active swimming. During passive simulated
swimming movements induced under anesthesia, in which all muscle was inactive,
length changes in RM and adjacent WM were closely matched in phase
(Fig. 4A), as one would expect.
However, during steady swimming using only RM, the waveforms were no longer
synchronized; WM strain preceded (in time) the peak in RM strain
(Fig. 4B). By cross-correlation
analysis, we determined that the mean phase shift between simultaneous
recordings of RM and WM strain was 90 ms [or
10% of the tailbeat cycle,
with one individual as high as 174 ms (
17%)]. r2
values for these correlations ranged from 0.892 to 0.977.
The phase relationship between local shortening in RM and WM during passive
and active swimming was also examined in the posterior body position.
Fig. 5 illustrates an
experiment where crystals were placed in the RM and adjacent WM on the right
side of the body directly opposite a pair of crystals implanted in the RM on
the left side (Fig. 5A). During
passive simulated swimming, shortening in the posterior WM and RM (1 and 2,
respectively, in Fig. 5) were
in phase on the right side of the body and 180° out of phase with
shortening of the RM on the left side of the body, as expected
(Fig. 5B), but during active
swimming (Fig. 5C), shortening
in the WM preceded that in RM by a mean of 248 ms (48% of the tailbeat
cycle), a substantially greater phase shift than in the anterior position.
Comparison of curvature calculated for several positions along the dorsal midline between 0.4 and 0.8L indicates that both the amplitude of curvature as well as the speed of progression of the wave of curvature increases posteriorly (Figs 6, 7). Between 0.4 and 0.6L, the speed of propagation of the wave of midline curvature ranged from 240 to 1332 L s1 among five makos (Table 2). Amplitudes of lateral displacement also increased posteriorly, ranging from 1.33±0.10% at 0.38L to 12.94±0.86% at 1.0L. The speed of progression of the wave of lateral displacement (propulsive wave velocity) remained constant from snout to tail and ranged between 138 and 170 cm s1 (1.61.8 L s1) (Fig. 6; Table 2). Because of the lack of a phase shift in timing of muscle activation from anterior to posterior, the speed of the wave of muscle contraction from anterior to posterior is the same as the propulsive wave velocity (Table 2). Propulsive wavelengths were between 152 and 175 cm in makos of lengths 80 to 92.3 cm, or 1.8 to 2.1L (Table 2).
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To test whether the amplitude of strain varies within the RM mass at one axial position, an additional experiment was performed in which two pairs of sonomicrometric crystals were placed at the same posterior axial position within the RM, one pair located more medially and the other more peripherally within the RM mass, and a third pair in the adjacent WM (Fig. 8A). Strain amplitudes and phases varied within the RM mass. Strain was greater near the lateral surface of the RM mass. Furthermore, peaks in WM strain (1 in Fig. 8B) preceded peaks in medial RM strain (3 in Fig. 8B) by nearly 50% of the strain cycle in this posterior position but were in phase with shortening in the peripheral RM (2 in Fig. 8B).
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Discussion |
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Amplitudes and phases of strain varied significantly within the RM mass at
a given body position (Fig. 8).
We found significantly lower strain amplitudes near the medial surface of the
RM mass where the surrounding lubricative sheath, the layer of smooth
connective tissue that surrounds the RM mass, thought to facilitate shearing
between the adjacent RM and WM, is more prominent
(Fig. 9). Furthermore, peaks in
WM strain preceded peaks in medial RM strain by nearly 50% of the strain cycle
in this posterior position but were in phase with shortening in the peripheral
RM (Fig. 8B). Thus, although
strains in the WM and the most peripheral RM were in phase, their amplitudes
differed, reflecting the general increase in strain that occurs away from the
neutral axis of bending if the body deforms as a simple beam
(Katz et al., 1999). This
result suggests that moving from the medial edge to the periphery of the RM
mass, strains vary in both magnitude and phase and that closest to the medial
surface of the RM mass, where the lubricative sheath is most well-developed,
RM strain is the most uncoupled from shortening of the surrounding
musculature.
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In a previous study, we found that, in contrast to teleosts, in the leopard
shark both muscle activation phase and duty cycle remain constant along the
body (Donley and Shadwick,
2003), and we hypothesized that regional variation in muscle
function is not necessary for undulatory aquatic locomotion and may not occur
in cartilaginous fishes. The muscle activation data presented here for the
mako further support this hypothesis. In the mako, as in most fishes studied
previously (Gillis, 1998
;
Altringham and Ellerby, 1999
),
onset of RM activation occurred during muscle lengthening and offset occurred
during shortening (Fig. 2).
However, both the phase and duration of activation remained constant along the
body in the mako.
The present study identified one key difference in RM dynamics between mako
and leopard sharks: mean onset and offset of activation occur approximately
30° later in the strain cycle in the mako, producing only a very short
period in which the muscle is active while lengthening at both axial positions
(Fig. 2). This significantly
later activation phase suggests that RM in the mako may be faster to develop
force and faster to relax than RM in the leopard shark. If so, then these
fibers may perform proportionally less negative work and more net positive
work in each contraction cycle. Since shorter activation and relaxation times
allow muscle fibers to produce power at higher cycle frequencies, the mako may
have a greater range of aerobic swimming speeds than its ectothermic
relatives, as do tuna (Syme and Shadwick,
2002).
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Because RM activation is so late in the mako, the period in which the
muscle is active while lengthening is brief and there is no opportunity for
posterior muscle fibers to act as force transmitters. Instead, we expect
muscle function to be uniform along the body, with contractions optimized for
positive power production, as has been shown to occur in tunas
(Shadwick et al., 1999).
Furthermore, strain amplitudes approximately double while RM cross-sectional
area decreases by
50% between 0.4 and 0.6L
(Bernal et al., 2003
), so we
predict that overall work per cycle is similar at the two axial positions.
Most fishes generally bear a set of six intermuscular tendons within a
single myoseptum (Gemballa et al.,
2003). In the mako, one tendon out of this set of six, the
hypaxial lateral tendon, shows striking differences to its homologue in bony
fishes. This tendon is remarkably thick and elongated, up to 0.19L in
the posterior (Donley et al.,
2004
; Fig. 10),
whereas the length of the homologous tendon in bony fishes at 0.6L
does not exceed 0.075L (Gemballa
and Treiber, 2003
; Gemballa
and Röder, 2004
). Observed differences in tendon
ultrastructure add further support to the idea that intermuscular tendons, not
the muscle itself, are used for force transmission along the body in the
mako.
Kinematics
In a previous study on the evolutionary convergence between lamnid sharks
and tunas, we reported that lamnids swim more like tunas than like other
sharks or subcarangiform teleosts (Donley
et al., 2004). Lamnids share the same thunniform swimming mode,
exemplified by a combination of minimal lateral motion in the mid-body region,
where the bulk of the muscle resides, and reduced body mass in the caudal
region, where lateral amplitudes are high
(Donley et al., 2004
). The
present study provides additional kinematic data to show the strong similarity
between lamnids and tunas. Specifically, we examined the degree of lateral
displacement and curvature along the body and the relationship between the
timing of waves of midline curvature, predicted strain and measured RM strain.
Lateral displacement and midline curvature increase rostrocaudally
(Fig. 6), but both have
significantly lower amplitudes in the mako than in the leopard shark, between
0.4 and 0.8L (Fig. 7),
indicating that the lamnid has a less undulatory mode of locomotion.
A defining characteristic of thunniform locomotion is the physical
uncoupling of RM shortening from local body bending during steady swimming.
This relationship between the timing of shortening in the deep RM and
deformation of the surrounding tissue and skin was quantified in a number of
ways in the mako. First, we found in all individuals that the timing of waves
of predicted strain and curvature preceded measured RM strain. This phase
relationship indicates that RM shortening is not linked to local bending but
is, in fact, in phase with and thus influencing bending at more posterior body
locations. This is illustrated in Fig.
3, which shows RM strain at 0.42L in phase with curvature
calculated simultaneously at 0.6L. Second, we found that shortening
in the RM and local WM at both axial positions was in phase when we imposed
whole body undulations on inactive fish (i.e. `passive swimming'; Figs
4,
5). However, during steady
swimming, shortening in the active RM was delayed relative to the adjacent
white muscle by 1017% of the tailbeat cycle in the anterior
(Fig. 4), and this phase delay
increased to nearly half of the tailbeat cycle in the posterior
(Fig. 5). Thus, the RM
shortening projects posteriorly along the mako, and the increase in the phase
shift between shortening in the RM and local WM accords well with the
rostrocaudal increase in myotomal lengths as well as the increase in hypaxial
lateral tendon lengths recorded previously in the mako
(Fig.
10;Donley et al.,
2004).
In the leopard shark, as in most fishes with superficial RM, it has been
shown that shortening in muscle occurs in phase with local body bending
(Coughlin et al., 1996;
Shadwick et al., 1998
;
Katz et al., 1999
;
Katz, 2002
;
Donley and Shadwick, 2003
).
The results presented here for the mako thus differ from the leopard shark and
accord well with patterns observed in skipjack tuna, where Shadwick et al.
(1999
) reported that
shortening in the deep RM occurred 17% later in the strain cycle than that
predicted by midline curvature.
How do patterns of RM shortening along the body relate to whole-body
kinematics in the mako? Fig.
11 illustrates the connection between the position of the dorsal
midline and amplitudes of lateral displacement, body curvature and anterior
and posterior RM strain as a function of time through one complete tailbeat
cycle in an 87 cm L mako. During the course of a typical tailbeat
cycle in a steady swimming mako, contractions of the body musculature produce
a wave of lateral displacement that travels down the body rostrocaudally such
that peaks in lateral displacement occur later in time at more posterior body
positions. Fig. 11B compares
the amplitudes of lateral displacement measured simultaneously at
0.6L and 1.0L (tail tip). As in most fish, the amplitude of
lateral displacement in the mako increases towards the tail. In the mako,
peaks in lateral displacement at 0.6L occur almost in synchrony with
peaks in displacement at the tail tip but in the opposite direction. That is,
when the tail tip is at its maximum in one direction, lateral displacement at
0.6L is at its maximum in the opposing direction. Curvature waves
also propagate down the body from snout to tail but, unlike lateral
displacement, the speed of the wave of K is much greater and
increases rostrocaudally (Fig.
6). RM strain at 0.4L is in phase with K at
0.6L, as well as with peaks in displacement at the tail tip (Figs
3,
11B,C). Following the progress
of muscle shortening at 0.4L
(Fig. 11D), muscle on the left
side of the body is lengthening at 0.4L when K is increasing
and lateral displacement of the tail tip is increasing to the right. The RM at
0.4L therefore transmits its force down the body, causing bending at
0.6L, pulling the body at 0.6L and beyond to the left. This
demonstrates that the RM in the mid-body region operates in near synchrony
with the movements of the tail and is therefore uncoupled from local body
curvature. Thus, by this uncoupling of RM shortening and local body bending,
made possible by the development of thick and elongated hypaxial lateral
tendons, the mako is able to achieve a tuna-like thunniform swimming mode
(Donley et al., 2004).
Conclusion
Examination of the longitudinal patterns of RM strain and activation,
together with dorsal midline kinematics, in a lamnid shark species, the
shortfin mako (Isurus oxyrinchus), has demonstrated some key features
of the locomotor system in makos that are in common with tunas as well as
other sharks. One specific goal of this project was to test the hypothesis
that the lack of longitudinal variation in the EMG/strain phase relationship
is a characteristic consistent among sharks regardless of their mode of
body/caudal fin propulsion. In support of this hypothesis, we found no
variation in the timing of RM activation along the body in the mako and infer
that functional properties of the RM remain constant from anterior to
posterior, a characteristic consistent with the leopard shark but unlike that
observed in many bony fish species. As in tunas, the elongated tendons in the
mako help transfer force along the body such that shortening in the RM is
synchronous with bending at more posterior regions, a characteristic of
thunniform locomotion.
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Acknowledgments |
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