scholarly journals Flight muscle power increases with strain amplitude and decreases with cycle frequency in zebra finches (Taeniopygia guttata)

2020 ◽  
Vol 223 (21) ◽  
pp. jeb225839 ◽  
Author(s):  
Joseph W. Bahlman ◽  
Vikram B. Baliga ◽  
Douglas L. Altshuler

ABSTRACTBirds that use high flapping frequencies can modulate aerodynamic force by varying wing velocity, which is primarily a function of stroke amplitude and wingbeat frequency. Previous measurements from zebra finches (Taeniopygia guttata) flying across a range of speeds in a wind tunnel demonstrate that although the birds modulated both wingbeat kinematic parameters, they exhibited greater changes in stroke amplitude. These two kinematic parameters contribute equally to aerodynamic force, so the preference for modulating amplitude over frequency may instead derive from limitations of muscle physiology at high frequency. We tested this hypothesis by developing a novel in situ work loop approach to measure muscle force and power output from the whole pectoralis major of zebra finches. This method allowed for multiple measurements over several hours without significant degradation in muscle power. We explored the parameter space of stimulus, strain amplitude and cycle frequencies measured previously from zebra finches, which revealed overall high net power output of the muscle, despite substantial levels of counter-productive power during muscle lengthening. We directly compared how changes to muscle shortening velocity via strain amplitude and cycle frequency affected muscle power. Increases in strain amplitude led to increased power output during shortening with little to no change in power output during lengthening. In contrast, increases in cycle frequency did not lead to increased power during shortening but instead increased counter-productive power during lengthening. These results demonstrate why at high wingbeat frequency, increasing wing stroke amplitude could be a more effective mechanism to cope with increased aerodynamic demands.

1993 ◽  
Vol 182 (1) ◽  
pp. 191-206 ◽  
Author(s):  
J. D. Altringham ◽  
C. S. Wardle ◽  
C. I. Smith

We describe experiments on isolated, live muscle fibres which simulate their in vivo activity in a swimming saithe (Pollachius virens). Superficial fast muscle fibres isolated from points 0.35, 0.5 and 0.65 body lengths (BL) from the anterior tip had different contractile properties. Twitch contraction time increased from rostral to caudal myotomes and power output (measured by the work loop technique) decreased. Power versus cycle frequency curves of rostral fibres were shifted to higher frequencies relative to those of caudal fibres. In the fish, phase differences between caudally travelling waves of muscle activation and fish bending suggest a change in muscle function along the body. In vitro experiments indicate that in vivo superficial fast fibres of rostral myotomes are operating under conditions that yield maximum power output. Caudal myotomes are active as they are lengthened in vivo and initially operate under conditions which maximise their stiffness, before entering a positive power-generating phase. A description is presented for the generation of thrust at the tail blade by the superficial, fast, lateral muscle. Power generated rostrally is transmitted to the tail by stiffened muscle placed more caudally. A transition zone between power generation and stiffening travels caudally, and all but the most caudal myotomes generate power at some phase of the tailbeat. Rostral power output, caudal force, bending moment and force at the tail blade are all maximal at essentially the same moment in the tailbeat cycle, as the tail blade crosses the swimming track.


1990 ◽  
Vol 148 (1) ◽  
pp. 395-402 ◽  
Author(s):  
JOHN D. ALTRINGHAM ◽  
IAN A. JOHNSTON

Intact, electrically excitable fibre bundles were isolated from the fast and slow myotomal muscle of the bullrout (Myoxocephalus scorpius L.). Power output was measured under conditions simulating their activity in a fish swimming at different speeds. Preparations were subjected to sinusoidal length changes of ±5% of resting length, and stimulated briefly during each cycle. The number and timing of stimuli were adjusted at each cycle frequency to maximise power output. Maximum power was produced at 5–7 Hz for fast fibres (25–35 W kg−1) and 2 Hz for slow fibres (5–8 Wkg−1). Under these conditions, pre-stretch of active muscle provides an important mechanism for storing potential energy for release during the shortening part of the cycle.


1996 ◽  
Vol 199 (12) ◽  
pp. 2745-2755 ◽  
Author(s):  
P Chai ◽  
R Harrykissoon ◽  
R Dudley

Owing to their small size and hovering locomotion, hummingbirds are the most aerobically active vertebrate endotherms. Can hyperoxia enhance the flight performance of this highly oxygen-dependent group? Hovering performance of ruby-throated hummingbirds (Archilochus colubris) was manipulated non-invasively using hyperoxic but hypodense gas mixtures of sea-level air combined with heliox containing 35% O2. This manipulation sheds light on the interplay among metabolic power input, mechanical power output and aerodynamic force production in limiting flight performance. No significant differences in flight mechanics and oxygen consumption were identified between hyperoxic and normoxic conditions. Thus, at least in the present experimental context, hyperoxia did not change the major metabolic and mechanical parameters; O2 diffusive capacities of the respiratory system were probably not limiting to a significant extent. Compared with hummingbirds in our previous studies, the present experimental birds were heavier, had resultant shorter hover-feeding durations and experienced aerodynamic failure at higher air densities. Because hummingbirds have relatively stable wingbeat frequencies, modulation of power output was attained primarily through variation in stroke amplitude up to near 180 degrees. This result indicates that maximum hovering performance was constrained geometrically and that heavier birds with greater fat loads had less margin for enhancement of power production. Sexual dimorphism in flight adaptation also played a role, with males showing more limited hovering capacities, presumably as a trade-off for increased maneuverability.


1997 ◽  
Vol 200 (24) ◽  
pp. 3119-3131 ◽  
Author(s):  
G N Askew ◽  
R L Marsh

The effects of length trajectory on the mechanical power output of mouse soleus and extensor digitorum longus (EDL) muscles were investigated using the work loop technique in vitro at 37 degrees C. Muscles were subjected to sinusoidal and sawtooth cycles of lengthening and shortening; for the sawtooth cycles, the proportion of the cycle spent shortening was varied. For each cycle frequency examined, the timing and duration of stimulation and the strain amplitude were optimized to yield the maximum power output. During sawtooth length trajectories, power increased as the proportion of the cycle spent shortening increased. The increase in power was attributable to more complete activation of the muscle due to 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. The power produced during symmetrical sawtooth cycles was 5-10 % higher than during sinusoidal work loops. Maximum power outputs of 92 W kg-1 (soleus) and 247 W kg-1 (EDL) were obtained by manipulating the length trajectory. For each muscle, this was approximately 70 % of the maximum power output estimated from the isotonic force-velocity relationship. We have found a number of examples suggesting that animals exploit prolonging the shortening phase during activities requiring a high power output, such as flying, jet-propulsion swimming and vocalization. In an evolutionary context, increasing the relative shortening duration provides an alternative to increasing the maximum shortening velocity (Vmax) as a way to increase power output.


1994 ◽  
Vol 267 (2) ◽  
pp. R481-R488 ◽  
Author(s):  
T. P. Johnson ◽  
D. A. Syme ◽  
B. C. Jayne ◽  
G. V. Lauder ◽  
A. F. Bennett

We recorded electromyograms of slow-twitch (red) muscle fibers and videotaped swimming in the largemouth bass (Micropterus salmoides) during cruise, burst-and-glide, and C-start maneuvers. By use of in vivo patterns of stimulation and estimates of strain, in vitro power output was measured at 20 degrees C with the oscillatory work loop technique on slow-twitch fiber bundles from the midbody area near the soft dorsal fin. Power output increased slightly with cycle frequency to a plateau of approximately 10 W/kg at 3-5 Hz, encompassing the normal range of tail-beat frequencies for steady swimming (approximately 2-4 Hz). Power output declined at cycle frequencies simulating unsteady swimming (burst-and-glide, 10 Hz; C-start, 15 Hz). However, activating the muscle at 10 Hz did significantly increase the net work done compared with the work produced by the inactive muscle (work done by the viscous and elastic components). Thus this study provides further insight into the apparently paradoxical observation that red muscle can contribute little or no power and yet continues to show some recruitment during unsteady swimming. Comparison with published values of power requirements from oxygen consumption measurements indicates a limit to steady swimming speed imposed by the maximum power available from red muscle.


1991 ◽  
Vol 157 (1) ◽  
pp. 409-423 ◽  
Author(s):  
TIMOTHY P. JOHNSON ◽  
IAN A. JOHNSTON

Fast muscle fibres were isolated from the abdominal myotomes of the shorthorned sculpin Myoxocephalus scorpius L. Sinusoidal length changes were imposed about resting muscle length and fibres were stimulated at a selected phase during the strain cycle. The work output per cycle was calculated from the area of the resulting force-position loops. The strain amplitude required for maximum work per cycle had a distinct optimum at ±5 % of resting length, which was independent of temperature. Maximum positive work loops were obtained by retarding the stimulus relative to the start of the length-change cycle by 30° (full cycle=360°). The maximum negative work output was obtained with a 210° stimulus phase shift. At intermediate stimulus phase shifts, work loops became complex with both positive (anticlockwise) and negative (clockwise) components. The number and timing of stimuli were adjusted, at constant strain amplitude (±5% of resting muscle length), to optimize net positive work output over a range of cycle frequencies. The cycle frequency required for maximum power output (work per cycle times cycle frequency) increased from around 5–7 Hz at 4°C to 9–13 Hz at 15°C. The maximum tension generated per cycle at 15°C was around two times higher at all cycle frequencies in summer-relative to winter-acclimatized fish. Fast muscle fibres from summer fish produced consistently higher tensions at 4°C, but the differences were only significant at 15 Hz. Acclimatization also modified the relationship between peak length and peak force at 4°C and 15°C. The maximum power output of muscle fibres showed little seasonal variation at 4°C and was in the range 20–25 W kg−1. In contrast, at 15°C, maximum muscle power output increased from 9 W kg−1 in the winter- to 30 W kg−1 in the summeracclimatized fish


1995 ◽  
Vol 198 (4) ◽  
pp. 1035-1043 ◽  
Author(s):  
J Layland ◽  
I S Young ◽  
J D Altringham

Papillary muscles were isolated from the right ventricles of rats and the length for maximum active force generation (Lmax) was determined isometrically. The work loop technique was used to derive the length for maximum work production (Lopt) at the cycle frequency, strain amplitude and stimulation phase shift found to be optimal for power output. Lopt was typically 7% shorter than Lmax and within the physiological length range (87.5% Lmax to Lmax). Net work and power output were measured during sinusoidal strain cycles around Lopt, over the cycle frequency range 1-9 Hz, strain amplitude and phase shift being optimised for work and power at each frequency. Experiments were performed at 37 degrees C. Distinct optima were found in both the work-frequency and the power-frequency relationships. The optimum cycle frequency for net work production was lower than the frequency for maximum power output. The mean maximum power output at 37 degrees C was 8.62 +/- 0.50 W kg-1 (mean +/- S.E.M., N = 9) and was achieved at a cycle frequency of approximately 6 Hz, close to the estimated resting heart rate of 5.8 Hz for the rats used (mean mass 223 +/- 25 g). The cycle frequency, strain amplitude and stimulation phase shift found to be optimal for power output produced an in vitro contraction closely simulating the basal in vivo contraction.


1988 ◽  
Vol 140 (1) ◽  
pp. 287-299 ◽  
Author(s):  
DARRELL R. STOKES ◽  
ROBERT K. JOSEPHSON

The mechanical power output was measured from scaphognathite (SG = gill bailer) muscle L2B of the crab Carcinus maenas (L.). The work was determined from the area of the loop formed by plotting muscle length against force when the muscle was subjected to sinusoidal length change (strain) and phasic stimulation in the length cycle. The stimulation pattern (10 stimuli per burst, burst length = 20% of cycle length) mimicked that which has been recorded from muscle L2B in intact animals. Work output was measured at cycle frequencies ranging from 0.5 to 5 Hz. The work output at optimum strain and stimulus phase increased with increasing cycle frequency to a maximum at 2–3 Hz and declined thereafter. The maximum work per cycle was 2.7 J kg−1 (15 °C). The power output reached a maximum (8.8 W kg−1) at 4 Hz. Both optimum strain and optimum stimulus phase were relatively constant over the range of burst frequencies examined. Based on the fraction of the total SG musculature represented by muscle L2B (18%) and literature values for the oxygen consumption associated with ventilation in C. maenas and for the hydraulic power output from an SG, we estimate that at a beat frequency of 2 Hz the SG muscle is about 10% efficient in converting metabolic energy to muscle power, and about 19% efficient in converting muscle power to hydraulic power.


1997 ◽  
Vol 200 (20) ◽  
pp. 2617-2627 ◽  
Author(s):  
J D Altringham ◽  
B A Block

It has been hypothesised that regional endothermy has evolved in the muscle of some tunas to enhance the locomotory performance of the fish by increasing muscle power output. Using the work loop technique, we have determined the relationship between cycle frequency and power output, over a range of temperatures, in isolated bundles of slow muscle fibres from the endothermic yellowfin tuna (Thunnus albacares) and its ectothermic relative the bonito (Sarda chiliensis). Power output in all preparations was highly temperature-dependent. A counter-current heat exchanger which could maintain a 10 degrees C temperature differential would typically double maximum muscle power output and the frequency at which maximum power is generated (fopt). The deep slow muscle of the tuna was able to operate at higher temperatures than slow muscle from the bonito, but was more sensitive to temperature change than more superficially located slow fibres from both tuna and bonito. This suggests that it has undergone some evolutionary specialisation for operation at higher, but relatively stable, temperatures. fopt of slow muscle was higher than the tailbeat frequency of undisturbed cruising tuna and, together with the high intrinsic power output of the slow muscle mass, suggests that cruising fish have a substantial slow muscle power reserve. This reserve should be sufficient to power significantly higher sustainable swimming speeds, presumably at lower energetic cost than if intrinsically less efficient fast fibres were recruited.


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