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The mechanical power output of the pectoralis muscle of blue-breasted quail (Coturnix chinensis): the in vivo length cycle and its implications for muscle performance

Graham N. Askew^1,* and Richard L. Marsh²

¹ Department of Zoology, Downing Street, University of Cambridge, Cambridge CB2 3EJ, UK and
² Department of Biology, Northeastern University, 360 Huntington Avenue, Boston, MA 02115, USA

View larger version (11K): [in a new window]   Fig. 1. Illustration of the sonomicrometry crystal holders used to implant the crystals into the pectoralis. The holders are sutured to the muscle fascia to secure the crystals in place. It is the movement of the holders that represents muscle strain, and an offset must therefore be calculated to allow the inter-crystal distance to be converted into strain: offset=inter-connector distance minus sonomicrometry distance.

View larger version (28K): [in a new window]   Fig. 2. (A) Representative sonomicrometry (top) and corresponding EMG (bottom) recordings from a quail during a vertical take-off. The resting length of the muscle (LR) is indicated before the flight. Variability in both recordings towards the end of the flight coincides with the bird flying into the mist net at the top of the flight chamber. (B). Expanded detail of three wing strokes, revealing the temporally asymmetrical strain trajectory (70.3 % of the time spent shortening and 29.7 % of the time spent lengthening for these three strokes). Note that, in this individual, the strain distribution is asymmetrical, with lengthening of +6 % and shortening of –14 % relative to LR. However, for all the birds for which measurements were obtained, the strain was distributed symmetrically relative to LR (lengthening of +11 % and shortening of –12 %, relative to LR; see Table 1).

View larger version (22K): [in a new window]   Fig. 3. Representative strain recordings from different quail during take-off and horizontal flights. Comparison of smoothing routines: (A) interpolation and (B) Fourier smoothing. In B, the standard error is indicated by the green line. (C) Comparison of the strain trajectory for one individual quail during take-off and horizontal flights. Strain recordings from three quails during (D) vertical take-off flights and (E) horizontal flights.

View larger version (15K): [in a new window]   Fig. 4. Variation in muscle shortening velocity over the course of three wingstrokes. (A) Pectoralis strain for typical wingstrokes; (B) the first derivative of strain and (C) details of the velocity during shortening for the cycle marked in B. L, muscle length.

View larger version (28K): [in a new window]   Fig. 5. Examples of data obtained from the in vitro work loop experiments. A bundle of muscle fibres was isolated from the quail pectoralis and subjected to a series of cyclical length changes. Two types of strain trajectory were studied: a wave that simulated the strain measured in vivo using sonomicrometry (A) and an asymmetrical sawtooth cycle (B). The muscle was activated 7 ms before peak length for 14 ms (indicated by the bold lines in A and B). Force was measured, and this has been used to calculate muscle stress (C,D). The instantaneous power output was calculated by multiplying force by the velocity of shortening (E,F). Work loops were generated by plotting stress against strain. Work loops from two consecutive cycles are shown in G and H. The arrows indicate the direction of the loop.

View larger version (8K): [in a new window]   Fig. 6. Peak force during lengthening plotted against the maximum lengthening velocity. Values are means ± S.E.M. (for at least five muscles). The force during lengthening increased with velocity of stretch, but the relationship was non-linear. The line is a third-order polynomial fitted using least-squares regression. L, muscle length.

View larger version (13K): [in a new window]   Fig. 7. Relationship between shortening duration and twitch rise time for a variety of muscles: (1) cicada singing muscle (Josephson, 1984), (2) rattlesnake shaker muscle (Rome et al., 1996), (3) toadfish swimbladder muscle (Rome et al., 1996), (4) hummingbird pectoralis muscle (Hagiwara et al., 1968), (5) Hyla chrysoscelis external oblique muscle (Girgenrath and Marsh, 1999), (6) zebra finch pectoralis muscle (Hagiwara et al., 1968), (7) blue-breasted quail pectoralis muscle (this study), (8) locust flight muscle (Josephson and Stevenson, 1991), (9) Hyla versicolor external oblique muscle (Girgenrath and Marsh, 1999), (10) starling pectoralis muscle (Goslow and Dial, 1990), (11) saithe white muscle at 0.35 body lengths from the anterior tip (Altringham et al., 1993), (12) scup pink muscle at 20°C (Coughlin et al., 1996), (13) scup red muscle (Swank et al., 1997), (14) toadfish white muscle (Rome et al., 1996), (15) rainbow trout slow muscle at 0.35 body lengths from the rostral tip (Hammond et al., 1998), (16) Argopecten irradians adductor muscle (Olson and Marsh, 1993), (17) toadfish red muscle (Rome et al., 1996). The lines represent data from several different temperatures: (A) Dipsosaurus dorsalis iliofibularis muscle (Marsh, 1988), (B) Dipsosaurus dorsalis iliofibularis muscle (Swoap et al., 1993), (C) Hyla chrysoscelis tensor chordarum muscle (McLister et al., 1995), (D) Hyla versicolor tensor chordarum muscle (McLister et al., 1995). The solid, bold line represents the linear regression for all the data (r2=0.935, P<0.01). For most of the muscles, the twitch rise time was the time from zero to maximum force; however, for the scup pink muscle, it was the time taken from 10 % to 90 % of the peak force.

View larger version (14K): [in a new window]   Fig. 8. Comparison of the strain (A) and shortening velocity (B) during shortening for the simulation and sawtooth cycles and the stress (C) and instantaneous power output (D) that is developed. The stress was higher during the simulation cycle than during the sawtooth cycle throughout most of shortening, but the instantaneous power output was only greater during the later part of shortening. L, muscle length.

View larger version (7K): [in a new window]   Fig. 9. Variation in the mean power during shortening averaged over the entire cycle period with total strain for the simulation length-change cycles. For comparison, data for the sawtooth cycle have also been included (open square); however for these cycles, strain was not varied. Values are means ± S.E.M., N=5–8.