SUMMARY The pectoralis muscles are the main source of mechanical power for avian flight. The power output of these muscles must be modulated to meet the changing power requirements of flight across a range of speeds. This can be achieved at the muscle level by manipulation of strain trajectory and recruitment patterns, and/or by intermittent flight strategies. We have measured the in vitro power outputs of pectoralis muscle fascicles from budgerigars Melopsittacus undulatus and zebra finches Taeniopygia guttata under conditions replicating those previously measured in vivo during flight. This has allowed us to quantify the extent to which different power modulation mechanisms control flight muscle power output. Intermittent flight behaviour is a more important determinant of flight power in zebra finches than budgerigars. This behaviour accounts for 25–62% of power modulation relative to the maximum available mechanical power output in zebra finch, compared to 0–38% in budgerigars. Muscle level changes in fascicle strain trajectory and motor unit recruitment, rather than intermittent flight behaviours, are the main determinants of pectoralis muscle power output in budgerigars at all speeds, and in zebra finch at speeds below 14 m s–1.

SUMMARY Flight power varies in a U-shaped relationship with flight speed, requiring the modulation of flight muscle power in order to meet these changing power demands. The power output of the pectoralis muscle can potentially be modulated by changing strain trajectory and the relative timing and intensity of muscle activity. Pectoralis muscle length change and activity patterns were recorded in budgerigars Melopsitaccus undulatus and zebra finches Taeniopygia guttata at a range of flight speeds using sonomicrometry and electromyography (EMG). The pectoralis muscles in these species contain a single muscle fibre type. Therefore, the power output is entirely determined by muscle activity and strain trajectory, rather than recruitment of motor units with different contractile properties as in many other vertebrate muscle systems. Relative EMG intensity, wingbeat frequency and muscle strain varied in an approximately U-shaped relationship with flight speed. The shape of the length trajectory varied with flight speed in budgerigars, with the proportion of the cycle spent shortening being lowest at intermediate flight speeds. In zebra finch pectoralis muscle the shape of the length trajectory did not vary significantly with flight speed. In both species the observed changes in muscle recruitment and length trajectory are consistent with meeting flight power requirements that vary in a U-shaped pattern with speed. Both species utilised intermittent flight, tending to spend relatively less time flapping at intermediate flight speeds. This supports the idea that intermittent flight is used as a simple power modulation strategy. However, the idea that intermittent flight serves to maintain a `fixed gear' is over-simplistic and fails to recognise the plasticity in performance at the level of the muscle. Intermittent flight is only one component of a complex power modulation strategy.

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.

The effects of 10 mM (high) and 70 microM (physiologically relevant) caffeine on force, work output, and power output of isolated mouse extensor digitorum longus (EDL) and soleus muscles were investigated in vitro during recovery from fatigue at 35 degrees C. To monitor muscle performance during recovery from fatigue, we regularly subjected the muscle to a series of cyclical work loops. Force, work, and power output during shortening were significantly higher after treatment with 10 mM caffeine, probably as a result of increased Ca2+ release from the sarcoplasmic reticulum. However, the work required to relengthen the muscle also increased in the presence of 10 mM caffeine. This was due to a slowing of relaxation and an increase in muscle stiffness. The combination of increased work output during shortening and increased work input during lengthening had different effects on the two muscles. Net power output of mouse soleus muscle decreased as a result of 10 mM caffeine exposure, whereas net power output of the EDL muscle showed a transient, significant increase. Treatment with 70 microM caffeine had no significant effect on force, work, or power output of EDL or soleus muscles, suggesting that the plasma concentrations found when caffeine is used to enhance performance in human athletes might not directly affect the contractile performance of fatigued skeletal muscle.

The distal muscle-tendon units of cursorial species are commonly composed of short muscle fibres and long, compliant tendons. It is assumed that the ability of these tendons to store and return mechanical energy over the course of a stride, thus avoiding the cyclic absorption and regeneration of mechanical energy by active muscle, offers some metabolic energy savings during running. However, this assumption has not been tested directly. We used muscle ergometry and myothermic measurements to determine the cost of force production in muscles acting isometrically, as they could if mechanical energy was stored and returned by tendon, and undergoing active stretch-shorten cycles, as they would if mechanical energy was absorbed and regenerated by muscle. We found no detectable difference in the cost of force production in isometric cycles compared with stretch-shorten cycles. This result suggests that replacing muscle stretch-shorten work with tendon elastic energy storage and recovery does not reduce the cost of force production. This calls into question the assumption that reduction of muscle work drove the evolution of long distal tendons. We propose that the energetic benefits of tendons are derived primarily from their effect on muscle and limb architecture rather than their ability to reduce the cyclic work of muscle.