The mechanical power requirements of avian flight.

A major goal of flight research has been to establish the relationship between the mechanical power requirements of flight and flight speed. This relationship is central to our understanding of the ecology and evolution of bird flight behaviour. Current approaches to determining flight power have relied on a variety of indirect measurements and led to a controversy over the shape of the power-speed relationship and a lack of quantitative agreement between the different techniques. We have used a new approach to determine flight power at a range of speeds based on the performance of the pectoralis muscles. As such, our measurements provide a unique dataset for comparison with other methods. Here we show that in budgerigars (Melopsittacus undulatus) and zebra finches (Taenopygia guttata) power is modulated with flight speed, resulting in U-shaped power-speed relationship. Our measured muscle powers agreed well with a range of powers predicted using an aerodynamic model. Assessing the accuracy of mechanical power calculated using such models is essential as they are the basis for determining flight efficiency when compared to measurements of flight metabolic rate and for predicting minimum power and maximum range speeds, key determinants of optimal flight behaviour in the field.

Tribute to R. G. Boutilier: the role for skeletal muscle in the hypoxia-induced hypometabolic responses of submerged frogs.

Much of Bob Boutilier's research characterised the subcellular, organ-level and in vivo behavioural responses of frogs to environmental hypoxia. His entirely integrative approach helped to reveal the diversity of tissue-level responses to O(2) lack and to advance our understanding of the ecological relevance of hypoxia tolerance in frogs. Work from Bob's lab mainly focused on the role for skeletal muscle in the hypoxic energetics of overwintering frogs. Muscle energy demand affects whole-body metabolism, not only because of its capacity for rapid increases in ATP usage, but also because hypometabolism of the large skeletal muscle mass in inactive animals impacts so greatly on in vivo energetics. The oxyconformance and typical hypoxia-tolerance characteristics (e.g. suppressed heat flux and preserved membrane ion gradients during O(2) lack) of skeletal muscle in vitro suggest that muscle hypoperfusion in vivo is possibly a key mechanism for (i) downregulating muscle and whole-body metabolic rates and (ii) redistributing O(2) supply to hypoxia-sensitive tissues. The gradual onset of a low-level aerobic metabolic state in the muscle of hypoxic, cold-submerged frogs is indeed important for slowing depletion of on-board fuels and extending overwintering survival time. However, it has long been known that overwintering frogs cannot survive anoxia or even severe hypoxia. Recent work shows that they remain sensitive to ambient O(2) and that they emerge rapidly from quiescence in order to actively avoid environmental hypoxia. Hence, overwintering frogs experience periods of hypometabolic quiescence interspersed with episodes of costly hypoxia avoidance behaviour and exercise recovery. In keeping with this flexible physiology and behaviour, muscle mechanical properties in frogs do not deteriorate during periods of overwintering quiescence. On-going studies inspired by Bob Boutilier's integrative mindset continue to illuminate the cost-benefit(s) of intermittent locomotion in overwintering frogs, the constraints on muscle function during hypoxia, the mechanisms of tissue-level hypometabolism, and the details of possible muscle atrophy resistance in quiescent frogs.

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.

Sonomicrometry and electromyographic (EMG) recordings were made for the pectoralis muscle of blue-breasted quail (Coturnix chinensis) during take-off and horizontal flight. In both modes of flight, the pectoralis strain trajectory was asymmetrical, with 70 % of the total cycle time spent shortening. EMG activity was found to start just before mid-upstroke and continued into the downstroke. The wingbeat frequency was 23 Hz, and the total strain was 23 % of the mean resting length. Bundles of fibres were dissected from the pectoralis and subjected in vitro to the in vivo length and activity patterns, whilst measuring force. The net power output was only 80 W kg(-1) because of a large artefact in the force record during lengthening. For more realistic estimates of the pectoralis power output, we ignored the power absorbed by the muscle bundles during lengthening. The net power output during shortening averaged over the entire cycle was approximately 350 W kg(-1), and in several preparations over 400 W kg(-1). Sawtooth cycles were also examined for comparison with the simulation cycles, which were identical in all respects apart from the velocity profile. The power output during these cycles was found to be 14 % lower than during the in vivo strain trajectory. This difference was due to a higher velocity of stretch, which resulted in greater activation and higher power output throughout the later part of shortening, and the increase in shortening velocity towards the end of shortening, which facilitated deactivation. The muscle was found to operate at a mean length shorter than the plateau of the length/force relationship, which resulted in the isometric stress measured at the mean resting length being lower than is typically reported for striated muscle.

The mechanical power output of the flight muscles of blue-breasted quail (Coturnix chinensis) during take-off.

Blue-breasted quail (Coturnix chinensis) were filmed during take-off flights. By tracking the position of the centre of mass of the bird in three dimensions, we were able to calculate the power required to increase the potential and kinetic energy. In addition, high-speed video recordings of the position of the wings over the course of the wing stroke, and morphological measurements, allowed us to calculate the aerodynamic and inertial power requirements. The total power output required from the pectoralis muscle was, on average, 390 W kg(-1), which was similar to the highest measurements made on bundles of muscle fibres in vitro (433 W kg(-1)), although for one individual a power output of 530 W kg(-1) was calculated. The majority of the power was required to increase the potential energy of the body. The power output of these muscles is the highest yet found for any muscle in repetitive contractions. We also calculated the power requirements during take-off flights in four other species in the family Phasianidae. Power output was found to be independent of body mass in this family. However, the precise scaling of burst power output within this group must await a better assessment of whether similar levels of performance were measured across the group. We extended our analysis to one species of hawk, several species of hummingbird and two species of bee. Remarkably, we concluded that, over a broad range of body size (0.0002-5 kg) and contractile frequency (5-186 Hz), the myofibrillar power output of flight muscles during short maximal bursts is very high (360-460 W kg(-1)) and shows very little scaling with body mass. The approximate constancy of power output means that the work output varies inversely with wingbeat frequency and reaches values of approximately 30-60 J kg(-1) in the largest species.

Optimal shortening velocity (V/Vmax) of skeletal muscle during cyclical contractions: length-force effects and velocity-dependent activation and deactivation.

The force-velocity relationship has frequently been used to predict the shortening velocity that muscles should use to generate maximal net power output. Such predictions ignore other well-characterized intrinsic properties of the muscle, such as the length-force relationship and the kinetics of activation and deactivation (relaxation). We examined the effects of relative shortening velocity on the maximum net power output (over the entire cycle) of mouse soleus muscle, using sawtooth strain trajectories over a range of cycle frequencies. The strain trajectory was varied such that the proportion of the cycle spent shortening was 25, 50 or 75 % of the total cycle duration. A peak isotonic power output of 167 W kg-1 was obtained at a relative shortening velocity (V/Vmax) of 0.22. Over the range of cyclical contractions studied, the optimal V/Vmax for power production ranged almost fourfold from 0.075 to 0.30, with a maximum net power output of 94 W kg-1. The net power output increased as the proportion of the cycle spent shortening increased. Under conditions where the strain amplitude was high (i.e. low cycle frequencies and strain trajectories where the proportion of time spent shortening was greater than that spent lengthening), the effects of the length-force relationship reduced the optimal V/Vmax below that predicted from the force-velocity curve. At high cycle frequencies and also for strain trajectories with brief shortening periods, higher rates of activation and deactivation with increased strain rate shifted the optimal V/Vmax above that predicted from the force-velocity relationship. Thus, the force-velocity relationship alone does not accurately predict the optimal V/Vmax for maximum power production in muscles that operate over a wide range of conditions (e.g. red muscle of fish). The change in the rates of activation and deactivation with increasing velocity of stretch and shortening, respectively, made it difficult to model force accurately on the basis of the force-velocity and length-force relationships and isometric activation and deactivation kinetics. The discrepancies between the modelled and measured forces were largest at high cycle frequencies.

Fatigue of mouse soleus muscle, using the work loop technique.

The function of many muscles requires that they perform work. Fatigue of mouse soleus muscle was studied in vitro by subjecting it to repeated work loop cycles. Fatigue resulted in a reduction in force, a slowing of relaxation and in changes in the force-velocity properties of the muscle (indicated by changes in work loop shape). These effects interacted to reduce the positive work and to increase the negative work performed by the muscle, producing a decline in net work. Power output was sustained for longer and more cumulative work was performed with decreasing cycle frequency. However, absolute power output was highest at 5 Hz (the cycle frequency for maximum power output) until power fell below 20% of peak power. As cycle frequency increased, slowing of relaxation had greater effects in reducing the positive work and increasing the negative work performed by the muscle, compared with lower cycle frequencies.

The effects of length trajectory on the mechanical power output of mouse skeletal muscles.

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.