Muscle designed for maximum short-term power output: quail flight muscle
1 School of Biology, University of Leeds, Leeds LS2 9JT, UK
2 Department of Biology, Northeastern University, 360 Huntington Avenue,
Boston, MA 02115, USA
* e-mail g.n.askew{at}leeds.ac.uk
Accepted 13 May 2002
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Summary |
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Key words: blue-breasted quail, Coturnix chinensis, muscle, mechanics, power output, take-off, flight
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Introduction |
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In this paper, we review the power produced during the explosive take-off flight of blue-breasted quail (Coturnix chinensis) and examine some of the physiological properties of the pectoralis muscle that enable these remarkable performances to be achieved.
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Power output of the pectoralis muscle during take-off |
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In arriving at this estimate of muscle-mass-specific power output, we
assumed that all the aerodynamic power was provided by the pectoralis muscle.
In fact, this must be the case unless (i) significant aerodynamic power is
provided during the upstroke, or (i) the kinetic energy of the wing during the
upstroke is stored elastically in the pectoralis tendon and recovered during
the downstroke. With regard to the first possibility, we saw no evidence of a
wing-tip reversal during the upstroke that would allow aerodynamic power to be
produced. We consider it unlikely that the second possibility significantly
reduces the power produced by the pectoralis muscles for the following
reasons. First, the detailed kinematics of the wings reported by Askew et al.
(2001) shows that the decrease
in kinetic energy of the wing during the upstroke approximately coincides with
the start of shortening of the pectoralis muscle. Second, the pectoralis has
an internal aponeurosis, but no free tendon, and thus appears to have limited
ability for elastic energy storage. Third, during the upstroke, the work
required to provide the kinetic energy to the wing would require the major
upstroke muscle, the supracoracoideus, to produce more than 300 W
kg-1, and additional power is required for profile power during the
upstroke. This level of power output from a muscle that shortens for only 30 %
of the cycle period is extraordinarily high
(Askew et al., 2001
). Thus, it
seems more likely that transfer of energy is required at the end of the
downstroke to provide energy to accelerate the wing during the upstroke. The
very long tendon of the supracoracoideus provides a ready structure that could
store this energy, and the decrease in kinetic energy of the wing at the end
of the downstroke begins before the proximal wing reverses direction. Any
transfer of energy at the end of the downstroke would require even higher
power output from the pectoralis than we have estimated.
Work loop measurements using in vivo strain and activity
patterns
Askew and Marsh (2001) used
sonomicrometry and electromyography to determine the in vivo strain
and activity patterns (Fig.
3A,B). Bundles of fibres dissected from the pectoralis were
subjected in vitro to these in vivo operating conditions,
using the work loop technique (Josephson,
1985a
). The mean power output of the pectoralis muscle during
shortening (equivalent to the downstroke) averaged over the whole
wingbeat cycle was approximately 350 W kg-1, with a maximum
recorded value of 433 W kg-1.
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These two independent methods yield pectoralis muscle power outputs of
approximately 400 W kg-1. This power output far exceeds that
measured in other cyclically contracting non-avian fast vertebrate muscles in
which a high power output has been of selective advantage. For example, the
adductor muscle of swimming scallops generates approximately 30 W
kg-1 (Marsh and Olson,
1994), the external oblique muscles of hylid tree frogs generate
50-60 W kg-1 (Girgenrath and
Marsh, 1999
) and the white muscle of fish during fast-starts
produces 143 W kg-1 (Wakeling
and Johnston, 1998
). In the following sections, we consider the
physiological adaptations that enable the pectoralis muscle of the quail to
generate these high powers during take-off.
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Adaptations that facilitate the generation of a high power output |
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The mean muscle stress during a cyclical contraction can be calculated as
follows (illustrated for blue-breasted quail pectoralis muscle):
![]() | (1) |
Note that the mean muscle stress calculated in this way is the difference between the mean shortening stress and the mean lengthening stress.
The mean muscle stress developed by quail pectoralis muscle is similar to that generated by many other powergenerating muscles, including examples from several vertebrates and invertebrates (Table 1) whose muscles operate over a wide range of cycle frequencies. Thus, the high shortening strain rates in blue-breasted quail pectoralis muscle are not at the expense of the muscle's ability to develop high stresses during cycling. This enables quail pectoralis muscle to generate much higher power outputs compared with other muscles. The physiological properties that allow these stresses to be developed at such high strain rates include the density of myofibrils in the muscle, the force/velocity characteristics and the kinetics. In addition, a number of properties of the strain cycle contribute to the high performance, including the point on the length/force relationship at which the muscle operates, the asymmetry of the strain cycle and changes in velocity during shortening. Each of these properties will be reviewed in the subsequent sections.
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Physiological properties |
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The effect of myofibrillar density can be seen in muscles that produce
power continuously as opposed to the burst power required in the quail. The
sound-producing muscles of hylid frogs have a reduced mean stress
(Table 1) at least in part
because of a low myofibrillar volume, although other effects are evident in
these high-frequency muscles (Marsh,
1999a; Girgenrath and Marsh,
1999
). Also, hummingbirds, which have high sustained power
capacities (Chai and Dudley,
1995
), have lower muscle-mass-specific burst power capacities than
quail (Chai and Millard, 1997
;
Chai et al., 1997
).
The high myofibrillar volumes in the pectoralis muscle of blue-breasted quail give these muscles the potential for generating large forces. Whether this potential translates into high power outputs depends on the performance of the muscle during dynamic contractions. The generation of large forces at high cycling rates requires that the muscle can activate and deactivate rapidly and requires the muscle to have force/velocity characteristics that allow large forces to be developed at rapid shortening velocities.
Twitch characteristics
To allow operation at high wingbeat frequencies, the pectoralis muscle must
have rapid rates of activation and deactivation. Although twitch kinetics is
affected by the rate at which the muscle lengthens or shortens (Askew and
Marsh, 1997,
1998
), isometric twitch times
can be used as a comparative measure of deactivation rates. The twitch times
measured for cyclic power-producing muscles are proportional to the operating
frequency of the muscle (Askew and Marsh,
2001
). Blue-breasted quail pectoralis muscle has rapid twitch
kinetics with a twitch rise-time of 10.8 ms and a half-twitch relaxation time
of 8.8 ms (Askew and Marsh,
2001
). These twitch parameters are similar to those of muscles
that operate at similar cycle frequencies, such as the calling muscles of
hylid tree frogs (McLister et al.,
1995
; Girgenrath and Marsh,
1999
), zebra finch pectoralis muscle
(Hagiwara et al., 1968
) and a
locust flight muscle (Josephson and
Stevenson, 1991
).
Force/velocity relationship
The instantaneous isotonic power output is obtained by multiplying force by
velocity during contractions against a constant load and depends on the
maximum velocity of shortening at zero load and the shape of the
force/velocity curve. Although muscles do not operate isotonically in
vivo, the isotonic speed clearly limits power output, and maximising
power output requires a high maximum intrinsic shortening velocity.
Preliminary measurements during afterloaded isotonic contractions indicate a
high maximum shortening velocity for quail pectoralis muscle. Maximum power
output is also affected by the curvature of the force/velocity curve. The
force/velocity curve of the pectoralis in the blue-breasted quail has a low
curvature (G. N. Askew and R. L. Marsh, unpublished observations). Relatively
flat force/velocity curves have been measured for the external oblique muscles
of tree frogs (Girgenrath and Marsh,
1999; Marsh,
1999a
). Flattening of the force/velocity curve increases the
maximum instantaneous power output and the optimal relative shortening
velocity at which it is attained.
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Muscle length trajectory |
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Length/force relationship
The active force that can be developed by an isometrically contracting
muscle is a non-linear function of its length
(Fig. 4A) and is determined by
the amount of overlap between the thick and thin filaments
(Gordon et al., 1966) and,
hence, the number of crossbridges that can be formed. On the basis of the
length/force relationship, we have calculated the optimum relative length
(Lm/L0) about which a muscle should
oscillate to maximise work (Fig.
4B; Lm is the length at the midpoint of the
length cycle and L0 is the length at the midpoint of the
plateau of the length/force relationship). Optimum
Lm/L0 was calculated by maximising the
integral of force with respect to relative muscle length change (dL)
over a sinusoidal length change for a range of starting length (force/velocity
effects and time for activation and deactivation have not been included). For
strains equal to 0.06, the muscle should clearly operate on the plateau, and
for strains less than this there is a range of values of
Lm/L0 that allows the muscle to
operate entirely on the plateau (the diverging lines at relative lengths below
0.06 represents the extremes of the range of optimum lengths over which the
muscle can perform whilst still operating on the plateau of the length/force
relationship). Strains greater than 0.06 require that part of the length
excursion should occur at lengths not on the plateau. For these strains,
optimal Lm/L0 is less than 1 because,
for a given change in dL, the decline in relative force is greater on
the descending limb than on the first part of the ascending limb of the
length/force relationship.
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The strain in the pectoralis muscle in blue-breasted quail is 0.23
(Askew and Marsh, 2001). From
Fig. 4B, an optimum
Lm/L0 of 0.95 is predicted, giving a
maximum length excursion of 0.04L0 above the plateau and a
minimum length excursion of 0.13L0 below the plateau. For
strains of 0.36, as have been observed in mallards during take-off
(Williamson et al., 2001
), the
predicted optimum relative length is 9% below L0. The
length/force relationship has not been systematically measured for these bird
flight muscles in relation to the lengths about which the muscles oscillate
in vivo. However, Askew and Marsh
(2001
) noted that the peak
stress during work loops exceeded by 7% that measured under isometric
conditions at the mean in vivo resting length about which the muscle
was oscillated. They suggested that this indicated that the mean in
vivo resting length was shorter than the plateau of the length/force
relationship. It should be noted, however, that the length/force relationship
for whole muscle does not have the distinct regions illustrated in
Fig. 4A (see
Askew and Marsh, 1998
) because
of inhomogeneities among the sarcomeres and possibly as a result of
inhomogeneities in the lengths of the thick and thin filaments in individual
sarcomeres (Edman and Reggiani,
1987
; Josephson,
1999
).
Other reasons may also exist for operating predominantly on the ascending
limb of the length/force relationship. The effects of the strain trajectory on
activation and deactivation events may very with length. In addition, the
ascending limb is an inherently stable part of the length/force curve on which
to operate compared with the descending limb, where sarcomeres can become
unstable during lengthening (Morgan,
1990). At long muscle lengths, sarcomere inhomogeneity may result
in longer, weaker sarcomeres being `popped' by shorter, stronger ones.
However, such effects could presumably be avoided by having a muscle with a
high passive tension, which is determined by the content of the protein titin
(Rief et al., 1997
).
Cycle asymmetry
In vitro experiments have shown that the proportion of the cycle
time spent shortening is an important determinant of power output. In
experiments in which mouse limb muscles were subjected to sawtooth cycles in
which the proportion of the cycle spent shortening was varied, Askew and Marsh
(1997) showed that net power
output increased as the proportion of the cycle spent shortening increased.
Net power output during asymmetrical sawtooth cycles in which 75% of the cycle
was spent shortening was approximately 40% greater than during symmetrical
sawtooth cycles and was 50-60% of the maximum instantaneous power output that
can be generated during after-loaded isotonic contractions
(Askew and Marsh, 1997
). The
increase in power is attributable to more complete activation of the muscle as
a result of the longer stimulation duration, to a more rapid rise in force
resulting from increased stretch velocity and to an increase in the optimal
strain amplitude.
During flight, the downstroke (the main power-generating stroke) is often
longer in duration than the upstroke. For example, in osprey and Rüpell's
griffon vulture, the downstroke represents 63% and 70% of the wing stroke,
respectively (Scholey, 1983;
G. N. Askew, personal observation). The precise phase of the length changes in
the pectoralis muscles cannot be determined from these observations because of
the lack of synchrony between wing tip movements and the movements of the
humerus to which the pectoralis is attached
(Askew et al., 2001
).
Sonomicrometry recordings from the pectoralis muscle in various species of
bird during take-off reveal that the length trajectory of these muscles is
definitely asymmetrical. For example, during take-off, pectoralis muscle
shortening represents 63% of the total wing stroke duration in pigeons
(Biewener et al., 1998
), 68% in
mallards (Williamson et al.,
2001
) and 56-70% in some members of the Phasianidae
(Fig. 3A; Tobalske and Dial, 2000
;
Askew and Marsh, 2001
).
The strain measured in the avian pectoralis muscle during take-off is high
in comparison with optimal strains observed in many in vitro work
loop experiments using symmetrical cycles. The strain in blue-breasted quail
pectoralis muscle is 23 % of the muscle's resting length, which is comparable
with that measured in the ring-necked pheasant, although not as high as in the
pigeon and mallard (32 and 36 %, respectively;
Biewener et al., 1998;
Williamson et al., 2001
). The
optimum strain occurs at an optimal relative shortening velocity that is
dependent on the length/force relationship, the force/velocity relationship
and the state of activation of the muscle
(Askew and Marsh, 1998
).
However, for a given cycle frequency, as the proportion of the cycle spent
shortening increases, the optimal strain also increases to maintain an optimal
relative shortening velocity. This has the effect of increasing the work
generated and, hence, the power output of the muscle.
Velocity profile
In addition to enhancing power by prolonging the shortening phase of the
contraction, Askew and Marsh
(2001) have shown that during
take-off flights in quail there may be improvements in power output due to
subtle changes in the velocity profile. They compared the power output during
simulated natural length trajectories with that during sawtooth cycles that
had the same proportion of the cycle spent shortening as the natural cycles
(Fig. 5). The timing and
duration of stimulation and the total strain were identical in both sets of
cycles. The power output was 16 % higher during the natural cycles than during
the sawtooth cycles. The higher peak lengthening velocity during the natural
cycles appeared to result in greater activation and led to higher
instantaneous power outputs towards the end of shortening compared with the
sawtooth cycles (Askew and Marsh,
1998
,
2001
). The rate at which force
rises during activation increases with higher velocities of stretch during
cyclical length changes (Askew and Marsh,
1997
,
1998
) and when the stretch is
imposed during a tetanic contraction
(Edman et al., 1978
;
Lombardi and Piazzesi, 1990
;
Takarada et al., 1997
).
Reducing the time required to activate the muscle means that the muscle is
more completely activated during shortening.
|
Furthermore, during the second half of the downstroke, the rate of
shortening increases (see Fig.
3), which further enhances deactivation of the muscle
(Askew and Marsh, 1998;
Askew et al., 2001
). Shortening
of a partially activated muscle reduces its ability to develop force, with the
magnitude of the reduction being positively correlated with the shortening
velocity (Gordon and Ridgway,
1987
; Caputo et al.,
1994
; Askew and Marsh,
1997
,
1998
). Rapid deactivation at
the end of shortening ensures that there is little residual force during
re-lengthening of the pectoralis on the upstroke, which would increase the
power required from the supracoracoideus muscle. However, even during this
relaxation period, the instantaneous power output is greater during the in
vivo simulation than during the sawtooth trajectory because of the higher
stress and higher shortening velocity (Fig.
5).
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Concluding remarks |
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Acknowledgments |
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References |
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