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First published online May 2, 2008
Journal of Experimental Biology 211, 1603-1611 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.013250
Thunniform swimming: muscle dynamics and mechanical power production of aerobic fibres in yellowfin tuna (Thunnus albacares)
1 Department of Zoology, University of British Columbia, Vancouver, BC, V6T 2A9,
Canada
2 Department of Biological Sciences, University of Calgary, Calgary, AB, T2N
1N4, Canada
* Author for correspondence (e-mail: shadwick{at}zoology.ubc.ca)
Accepted 20 March 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: muscle strain, muscle power, red muscle, work loop, swimming, yellowfin tuna
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Donley et al., 2004;
Shadwick, 2005). These
features include a highly streamlined body, elevated core temperatures,
concentration of aerobic red muscle to anterior and medial positions, and high
sustained swimming speeds powered primarily by lateral motion of the
hydrofoil-like tail rather than body undulations
(Bernal et al., 2001;
Graham and Dickson, 2000;
Graham and Dickson, 2004).
Despite their innate appeal to comparative physiologists, studies on muscle
function in tunas during swimming are sparse, undoubtedly because laboratory
access for research on live specimens is very limited. In work carried out at
the Kewalo Research Facility in Hawaii we discovered an anomalous relation
between actual muscle shortening and that predicted based on midline curvature
in skipjack tuna (Katsuwonis pelamis), which appears to underpin the
thunniform mode of swimming (Shadwick et
al., 1999). We also found that red muscle shortening in yellowfin
tuna (Thunnus albacares) is greater than expected based on the degree
of body bending (Katz et al.,
2001), suggesting that the location of red muscle close to the
backbone does not limit shortening nor impose a mechanical disadvantage as
previously anticipated (Shadwick,
2005). Indeed, by having red muscle positioned close to the
backbone and away from direct linkage to the skin these fibres can produce
greater, rather than less, contractile work and power for swimming because of
greater shortening and long-reaching tendon linkages.
There is further evidence that thunniform swimmers use their red muscles
for propulsion under near-optimal conditions for power production. The impact
of regional endothermy on muscle performance in yellowfin tuna was
investigated using cyclic contractions on isolated segments of red muscle
(work loop technique) with optimized activation parameters
(Altringham and Block, 1997).
Their study showed that power output was highly temperature dependent, and
that an elevation of core temperature by 10°C would typically double the
maximum muscle power output and the frequency at which it occurs, providing a
basis for fast, sustained swimming due to their ability to retain muscle heat.
Additional evidence for muscle power enhancement in yellowfin tuna was
presented in a preliminary report of a work loop study using strain and
activation timing derived from measurements in swimming fish
(Katz et al., 2001).
Subsequently, we investigated muscle contractile properties in skipjack tuna
(K. pelamis) by the work loop technique and concluded that red muscle
fibres along the entire body are used in a similar fashion to produce
near-maximal mechanical power for propulsion during normal cruise swimming
(Syme and Shadwick, 2002).
In the present study we examine muscle dynamics in yellowfin tuna by the use of sonomicrometry and electromyography in swimming fish, and by the work loop technique on isolated bundles of muscle fibres in vitro. We present an analysis of the performance of aerobic muscle in swimming, and draw comparisons to previous data for skipjack tuna. We note that both species display a phase shift between red muscle strain and midline curvature, a hallmark of thunniform swimming, that both yellowfin and skipjack tuna appear to use their red muscles in a manner that is nearly optimal for power output while swimming, and that the red muscles of yellowfin tuna are slower than those of skipjack, corresponding to the slower tail beat frequencies in yellowfin and the larger pectoral fins that provide lift.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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In vivo muscle dynamics
Sonomicrometry was used to measure muscle length changes in the deep red
muscle of yellowfin tuna while they swam in a calibrated water tunnel
treadmill. The details of the techniques are described elsewhere
(Shadwick et al., 1999). In
brief, fish were anesthetized quickly by submergence in well-oxygenated
seawater containing 1 g l–1 tricaine methanesulphonate
(Argent Chemical, Redmond, WA, USA) buffered to pH 7.8 with Tris base (Sigma)
for 2–3 min, then transferred to a lower maintenance dose of 0.057 g
l–1 and ventilated while surgery was performed. Piezoelectric
sonomicrometry crystal pairs were implanted in deep red muscle at axial
locations between 0.45 L and 0.65 L via an entry point near
the dorsal midline (see Fig.
1). This approach was necessary to avoid damage to the vascular
rete, which is situated lateral to the red muscle loin. Each pair was
separated by 8–15 mm along the body axis and correct crystal alignment
was ensured by monitoring the RF signal with an oscilloscope. In six fish,
34-gauge insulated copper wire electrodes with 1 mm bare tips were also
implanted in the red muscle next to the crystals to monitor muscle activity.
Placement of electrodes and location of the crystals were determined by
post-mortem examination. In four fish muscle force was measured with a buckle
force transducer fixed on the caudal tendons (see
Fig. 1). Details of this
procedure, including calibration, are given elsewhere
(Knower et al., 1999). After
surgery the fish were revived by ventilation with clean seawater in the water
tunnel, and swimming trials were conducted over the range of speeds at which
the fish were willing to swim (0.7–3.5 L s–1).
Sonometric signals were processed by a Triton system-6 sonomicrometry unit.
EMG signals were conditioned with a Grass P15 amplifier using a bandwidth of
30–300 Hz. Both signals were recorded digitally on a microcomputer at
1000 Hz using a TL-2 interface and Axotape software (Axon Instruments, Foster
City, CA, USA). Simultaneous video images of the dorsal silhouette of the
swimming fish against a reflective background were collected at 60 Hz and
0.001 s shutter speed with a CCD camera. The excitation voltage of a flashing
red diode visible in the video image was recorded and used for data
synchronization.
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;
Donley and Shadwick,
2003).
Kinematic analyses of body bending were performed for eight swimming bouts
of at least eight consecutive tail beats from four fish, according to the
bending beam model we used previously
(Katz et al., 1999;
Shadwick et al., 1999;
Donley and Shadwick, 2003).
This consisted of fitting polynomial curves to the dorsal midline of each
video field in a bout, and then calculating curvature as a function of time at
the axial position where sonomicrometry crystals were placed. Multiplication
of curvature by the horizontal distance between the crystals and the backbone
yielded a prediction of axial strain, based on the equation for a bending beam
(van Leeuwen et al., 1990).
This result was then compared in phase to the muscle strain waveform from
sonomicrometry by using a Fourier transformation technique (see
Katz and Shadwick, 1998).
In six fish we successfully recorded muscle strain at two or three axial
locations simultaneously. In these cases, the phase shift (and hence
t) between adjacent strain waveforms was determined by Fourier
transformation of 10–20 successive tail beats per swimming bout, and
then the axial speed of the strain wave on the body was computed.
In vitro muscle contractile properties
Muscle fibre bundles were prepared for use in work-loop experiments as in
previous studies (Katz et al.,
2001; Syme and Shadwick,
2002). Fish were captured with a dip net and immediately killed
with a blow to the head followed by severing of the spinal cord. A slab of
muscle was cut from the side of the fish, extending laterally through the deep
loin of red muscle, and from this blocks of 2–5 myomeres were dissected
at 0.5 L (N=5) and 0.65 L (N=3). In two
cases bundles of white muscle were also successfully prepared. Samples were
pared to a single myomere with a fibre bundle approximately 0.5 mm in diameter
and strips of myosepta at each end. Dissections were done at 5–10°C.
The muscle was rinsed frequently with chilled saline during dissections
(composition, in mmol l–1: NaCl, 175.5; KCl, 2.6;
CaCl2, 2.7; MgCl2, 1.1; sodium pyruvate, 10; Hepes, 10;
pH 7.8 at 25°C, saturated with pure oxygen). Fibre bundles were
transferred to an acrylic chamber filled with circulating saline at 25°C
and bubbled with oxygen. The myoseptum at one end was tied to a stainless
steel pin on a servomotor arm (Cambridge Technology, model 350, Lexington, MA,
USA) and the other end was tied to a pin extending from a force transducer
(AE801, SensoNor, Horten, Norway). The sample was stretched to remove visible
slack. A platinum-tipped stimulating electrode was used to provide a stimulus,
and voltage was increased until a maximal isometric twitch was elicited (4 ms
pulse duration), and this was then increased by 50% to ensure maximal
activation of the preparation. The in vivo muscle mean length
l0 was approximated by a combination of isometric force
and work recordings; sample length was adjusted so that developed twitch force
and work were near maximal and passive tension during work recordings was not
excessive. A stimulus frequency of 40 Hz gave maximal, isometric, tetanic
force and was used during all subsequent measurements of force and work.
Work and power recordings
Mechanical work and power were determined using the work-loop method
(Josephson, 1985) as described
previously for skipjack tuna (Syme and
Shadwick, 2002). The servomotor imposed a small sinusoidal length
change centered about l0. The peak-to-peak amplitude of
the length change, expressed as a percent of l0, is the
strain amplitude. During each cycle the muscle was stimulated phasically so
that force was developed primarily during shortening and the muscle was
relaxed during lengthening. Stimulus phase is the time during the strain cycle
that the stimulus began, and is expressed in degrees of a cycle, with 0°
representing lengthening through l0, 90° the maximum
length and 270° the minimum length. Work and power were measured over a
range of cycle frequencies that encompassed the tail beat frequencies observed
in swimming yellowfin tuna of similar size. Strain amplitude used was
±5.5%, based on in vivo measurements
(Shadwick et al., 1999) (and
see below) and ±2.75%, based on midline curvature (see
Table 1). A strain of
±8% was also tested at 3 Hz to further assess the effects of strain
amplitude on work and power. For each frequency and strain combination,
stimulus duration and phase were systematically altered until the net work
produced by the muscle was maximal. Stimulus phase and duration measured
in vivo, based on EMG recordings in swimming fish, were compared to
optimal.
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Samples were subjected to three cycles of strain and stimulation at each
combination of parameters studied; measurements were taken from the second or
third cycle, whichever was greater. Work was calculated as the integral of
force with respect to muscle length over the complete sinusoidal strain cycle.
Power is the rate of doing work and equals work per cycle times the cycling
frequency. Isometric tetanic force was monitored regularly during the
experiments, and used to adjust work values for fatigue or gradual
deterioration of the preparation, assuming a linear relationship between any
change in force and work between recordings (e.g.
Coughlin, 2000;
Altringham and Young, 1991;
James et al., 1995;
Altringham and Block, 1997;
Ellerby et al., 2001). We
found that the isometric force declined over the course of the experiments by
21.6±13.9% (mean ± s.d.) of the initial value. For comparative
purposes we expressed work and power in mass-specific units, following the
method used previously (Katz et al.,
2001; Syme and Shadwick,
2002). Briefly, since determining the samples' mass or volume is
confounded by their very small size, irregular dimensions, and uncertainties
about the proportion of viable cells, we calculated active cross-sectional
area based on the assumption that live fibres could generate 140 kN
m–2 maximal, isometric, tetanic stress. This area, in
conjunction with the length of the fibre bundle, was used to calculate muscle
mass, assuming a muscle tissue density of 1050 kg m–3. These
assumptions mean that comparisons of mass-specific power with other
preparations should be made with caution, but relative changes in work and
power are independent of this calculation.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Stride length increased non-linearly with speed, as
expected, reaching values of 0.6–0.7 at cruising speeds of 2–3
L s–1 (Fig.
2B). These values are similar to those from other studies of
swimming fish including tunas (Altringham
and Shadwick, 2001; Shadwick
and Gemballa, 2006).
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).
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).
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In vitro red muscle work and power
Red muscle samples taken from 0.5 and 0.65 L generated large work
loops with positive net work output at cycle frequencies of 1–4 Hz at
25°C when stimulus phase and duration were optimized for maximum work
(Figs 8,
9). Net work per cycle peaked
at 2 Hz and decreased substantially with increasing frequency thereafter,
approaching zero after 10 Hz (Fig.
10A). For strain amplitude of ±5.5% contractile power
(=workxfrequency) had its peak at about 4 Hz, and fell to near zero by
12 Hz (Fig. 10B). Power at 8
Hz and 1 Hz were about equal, but only 30% of the maximum. Very similar
results were obtained from muscle sampled at 0.65 L (data not shown).
Across the frequency range that corresponds to observed tail beat frequencies
for steady swimming (
1.8 to 4.0 Hz), power is >70% of maximum
(Fig. 10B).
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In tests done from 2–6 Hz, net work increased with strain amplitude, approximately doubling when strain was doubled from ±2.75% to ±5.5% (Fig. 9, Fig. 10A). Note that the lower strain used corresponds to that predicted from midline curvature, while the higher strain corresponds to that measured by sonomicrometry. With a further increase in strain to ±8% (a 45% increase over ±5.5% strain) net work was only about 15% higher (data at 3 Hz only; Fig. 9, Fig. 10A). Fig. 11 shows that power output at 3 Hz increased significantly with strain above ±2.75% (t-test; P<0.01), but power at ±8% was not significantly higher than at ±5.5% (t-test; P>0.05).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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), such that red muscle shortening in the mid body was
coincident with curvature and lateral motion of sites about 0.2 L
more posterior. We note a similar phase shift in the red muscle of yellowfin
tuna (Fig. 5 and
Table 1). We suggested this
posterior phase shift in muscle action was facilitated by highly elongated
myomeres and long tendinous connections, not so extreme in other fishes, that
allowed the red muscle mass to adopt a more anterior and medial position in
the body while powering swimming primarily by lateral motions of the caudal
fin. This anatomical novelty provides a mechanism for uncoupling the red
muscle contractions from local bending so that the lateral motions can be
restricted to the caudal region, the essence of `thunniform' swimming. Recent
work on the architecture of the myoseptal tendon system in tunas and other
species supports this notion (Gemballa and
Konstantinidis, 2005; Shadwick
and Gemballa, 2006). Interestingly, lamnid sharks show a
remarkable convergence with tunas in their morphology and thunniform swimming
mode, as documented by kinematic and anatomical studies
(Donley et al., 2004;
Donley et al., 2005). It is
now clear from structural analysis (S. Gemballa, personal communication) that
the positioning of red fibres within the medial tips of the highly elongated
myomeres in lamnids and in tunas results in their location appearing to be
much more anterior than the rest of the myomere and tendons with which they
are associated (Shadwick and Gemballa,
2006; Shadwick,
2005), thus providing the basis for the apparent uncoupling of
muscle shortening from local curvature.
As noted in skipjack tuna, the uncoupling of red muscle shortening from
local bending (Fig. 5) allows
the waves of muscle strain in yellowfin to travel posteriorly along the body
at a high velocity relative to swim speed
(Shadwick et al., 1999) (Figs
3,
4); consequently muscle
shortening is nearly simultaneous along one side of the fish. For example, at
a swim speed of 2 L s–1 the tail beat frequency is
about 3 Hz (Fig. 2); the strain
wave velocity is about 5.2 L s–1
(Fig. 4) or 1.7 L
T–1, where T is the tail beat period. Thus, it
takes only about 66 ms for the muscle strain wave to propagate along the
entire loin of red muscle (i.e. from about 0.35 to 0.7 L). This is
slightly slower than what we observed for skipjack (2.5 L
T–1), but similar to strain wave velocities measured in
mako sharks [1.4–1.8 L T–1
(Donley et al., 2005)]. This
feature, combined with the elongated myotendinous system, facilitates the
characteristic thunniform locomotion, with midbody muscle contractions
producing posterior lateral motions. In contrast, muscle strain is coupled to
local bending in non-thunniform swimmers so the strain wave velocity is no
greater than the propagated wave of bending; for example approximately 0.7
L T–1 in a trout
(Wardle et al., 1995) and 0.85
L T–1 in a leopard shark
(Donley and Shadwick,
2003).
The effect of the special situation in the tuna is demonstrated by in
vivo muscle `work loops' (Fig.
7). Tunas are the only fish with large discrete tendons that have
been instrumented for direct muscle force measurements during swimming
(Knower et al., 1993;
Shadwick et al., 2002a). The
close synchrony between muscle shortening in the mid-body and force
development in the caudal tendons is evident; the resulting work loop is large
and positive net work is produced, like the optimized work loops of isolated
muscle fibres (Figs 8,
9).
The functional uncoupling of tuna red muscle contractions from local
curvature results in an additional novelty; shortening strains are greater
than predicted from body curvature in yellowfin
(Fig. 5 and
Table 1)
(Katz et al., 2001) and in
skipjack (Shadwick et al.,
1999). In the current study deep red muscle strain at 0.5
L was twice that predicted based on body curvature. In fact, strain
in the deep location was even greater than the strain predicted from curvature
if the fibres occupied a superficial position, as in other fish
(Shadwick et al., 2002b;
Katz, 2002). Thus, the
internalization of the red fibres does not reduce active shortening work per
cycle, or power output, as would be expected under the anatomical regime found
in other fish. To quantify this prediction we compared work and power
production from isolated red fibres in work-loop experiments at strains
representing the average measured in vivo using sonomicrometry
(±5.5%) and that predicted based on local body curvature assuming
muscle strain as in a homogenous material (±2.7%). The results show the
benefit of the unique muscle anatomy in the tuna; work and power output are
twice as high as they would be if the red muscle occupied its medial position,
but did not have the connective tissue framework that allows its contractions
to be directed to the caudal region (Figs
9,
10,
11) rather than cause local
bending. Further increases in strain amplitude above that measured in
vivo result in only a modest increase in work and power output (Figs
9,
10,
11). These observations are
particularly intriguing in the context of the evolution of this body form,
particularly the acquisition of regional endothermy. It has been hypothesized
that the shift in red muscle position from superficial to medial and anterior
preceded the development of the vascular counter-current heat exchanger that
now elevates core body temperature in tunas and lamnid sharks
(Graham and Dickson, 2000;
Bernal et al., 2001). Our
results suggest that a specific biomechanical advantage was realized by the
anterior and medial shift of the red fibres, supporting the notion that
selection for improved swimming performance could have occurred independent of
any advantage conferred by regional endothermy.
Performance of red muscle in vitro
Our estimate of maximum power produced by red muscle of yellowfin tuna from
work loops at a strain of ±5.5% is approximately 66 W
kg–1 at 0.5 L and 63 W kg–1 at 0.65
L. This is comparable to results from a similar study on skipjack red
muscle in which maximum power output ranged from 44 to 75 W
kg–1 between axial positions of 0.44 and 0.7 L
(Syme and Shadwick, 2002).
However, these values are substantially higher than those reported
(Altringham and Block, 1997) in
a work loop study of yellowfin red muscle (12 W kg–1 at
±5% strain and 25°C). While there are undoubtedly some differences
arising from experimental procedure, we believe the most likely explanation
for this discrepancy is in the determination of muscle mass. Altringham and
Block measured wet muscle mass directly
(Altringham and Block, 1997)
and, if there are substantial amounts of non-viable tissue in the
preparations, then active muscle mass would have been overestimated. With our
technique of estimating functional cross-sectional area (and mass) from
isometric stress this potential problem is avoided [for a detailed discussion,
see Syme and Shadwick (Syme and Shadwick,
2002)]; however assumptions about area-specific force may not
apply universally across different species and muscles, reducing the rigor of
such comparisons.
Muscle function in yellowfin vs skipjack tunas
The current study demonstrates differences in muscle mechanics of yellowfin
and skipjack tuna that support previous observations on differences in their
swimming behaviour, specifically their aerobic speed range. Firstly, the
minimum speed needed to maintain hydrodynamic equilibrium is based on the lift
generated by pectoral fins, which are significantly larger in yellowfin than
in skipjack; thus yellowfin minimum cruising speed is lower
(Magnuson, 1978). In captivity
the undisturbed routine cruising speed is also typically lower in yellowfin,
at about 1 L s–1 (this study)
(Altringham and Block, 1997)
vs 1.8 L s–1 for skipjack
(Gooding et al., 1981;
Syme and Shadwick, 2002). In
laboratory tests of 40–50 cm fish, yellowfin have a lower maximum
aerobic swim speed, at about 2.5 L s–1, than do
skipjack at about 3.7 L s–1
(Dewar and Graham, 1994;
Knower et al., 1999). These
speed ranges correspond to a range of tail beat frequencies and their
associated cycle frequencies in the work-loop experiments. A comparison of the
range of aerobic cycle (tail beat) frequencies for the two species and the
respective muscle power output at these frequencies
(Fig. 14) demonstrates that
power output is maximized at higher frequencies in skipjack than in yellowfin
and that both species employ tail beat frequencies during cruise swimming that
result in near-maximal or maximal power output from the red muscle.
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Our findings also suggest that specific differences in muscle contractile
properties contribute to the observed differences in sustained swimming
speeds. For example, support for this premise is seen by comparing the
optimized timing of activation for work output between the species
(Fig. 12); yellowfin muscle
must be activated earlier in the strain cycle and for a shorter duration than
skipjack muscle, a characteristic of slower force development
(Fig. 13) and most likely
slower relaxation times. Interestingly, the average phase delay between muscle
strain and midline curvature during swimming was less in the yellowfin
(31°; Table 1) than it was
in skipjack [48° (Shadwick et al.,
1999)], possibly reflecting more elongate myomeres and/or
connective tissue linkages in the latter which may also enhance the capacity
for faster swimming.
Manoeuvrability
While the specializations described above equip tunas to swim fast, they
also reduce manoeuvrability. The bulky cross section and relatively stiff
vertebral column of tunas compromise turning and sudden accelerations
(Blake, 2004). Furthermore, the
medial red muscles in tunas are designed to transmit power to the tail by the
elongated tendons, making them less effective in steering because they do not
cause local bending. As noted in earlier studies, sudden accelerations and
turns are powered solely by the caudal fin
(Fierstine and Walters, 1968),
so turning while cruising requires a large radius, nearly 0.5 L
(Blake et al., 1995), or
2–3 times greater than for carangiform or sub-carangiform species
(Webb and Keyes, 1981).
Consequently, tuna red muscles are primarily used for forward propulsion,
apparently permitting them to operate at or near maximal power, unlike other
fishes in which red myotomal muscles also aid in steering, which may preclude
them from operating near maximal power. Indeed, all the evidence points to
non-thunniform swimmers producing far less than maximal power with their red
muscles (Syme et al., 2008)
(reviewed by Altringham and Ellerby,
1999; Coughlin,
2002; Syme, 2006).
Thus, tunas appear to have opted for speed over manoeuvrability, a strategy
well suited to their niche as open water predators.
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Acknowledgments |
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References |
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