Graham N. Askew

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.

The metabolic power requirements of flight and estimations of flight muscle efficiency in the cockatiel (Nymphicus hollandicus)

SUMMARY Little is known about how in vivo muscle efficiency, that is the ratio of mechanical and metabolic power, is affected by changes in locomotory tasks. One of the main problems with determining in vivo muscle efficiency is the large number of muscles generally used to produce mechanical power. Animal flight provides a unique model for determining muscle efficiency because only one muscle, the pectoralis muscle, produces nearly all of the mechanical power required for flight. In order to estimate in vivo flight muscle efficiency, we measured the metabolic cost of flight across a range of flight speeds (6–13 m s−1) using masked respirometry in the cockatiel (Nymphicus hollandicus) and compared it with measurements of mechanical power determined in the same wind tunnel. Similar to measurements of the mechanical power–speed relationship, the metabolic power–speed relationship had a U-shape, with a minimum at 10 m s−1. Although the mechanical and metabolic power–speed relationships had similar minimum power speeds, the metabolic power requirements are not a simple multiple of the mechanical power requirements across a range of flight speeds. The pectoralis muscle efficiency (estimated from mechanical and metabolic power, basal metabolism and an assumed value for the ‘postural costs’ of flight) increased with flight speed and ranged from 6.9% to 11.2%. However, it is probable that previous estimates of the postural costs of flight have been too low and that the pectoralis muscle efficiency is higher.

ENU Mutagenesis Reveals a Novel Phenotype of Reduced Limb Strength in Mice Lacking Fibrillin 2

Background Fibrillins 1 (FBN1) and 2 (FBN2) are components of microfibrils, microfilaments that are present in many connective tissues, either alone or in association with elastin. Marfans syndrome and congenital contractural arachnodactyly (CCA) result from dominant mutations in the genes FBN1 and FBN2 respectively. Patients with both conditions often present with specific muscle atrophy or weakness, yet this has not been reported in the mouse models. In the case of Fbn1, this is due to perinatal lethality of the homozygous null mice making measurements of strength difficult. In the case of Fbn2, four different mutant alleles have been described in the mouse and in all cases syndactyly was reported as the defining phenotypic feature of homozygotes. Methodology/Principal Findings As part of a large-scale N-ethyl-N-nitrosourea (ENU) mutagenesis screen, we identified a mouse mutant, Mariusz, which exhibited muscle weakness along with hindlimb syndactyly. We identified an amber nonsense mutation in Fbn2 in this mouse mutant. Examination of a previously characterised Fbn2-null mutant, Fbn2fp, identified a similar muscle weakness phenotype. The two Fbn2 mutant alleles complement each other confirming that the weakness is the result of a lack of Fbn2 activity. Skeletal muscle from mutants proved to be abnormal with higher than average numbers of fibres with centrally placed nuclei, an indicator that there are some regenerating muscle fibres. Physiological tests indicated that the mutant muscle produces significantly less maximal force, possibly as a result of the muscles being relatively smaller in Mariusz mice. Conclusions These findings indicate that Fbn2 is involved in integrity of structures required for strength in limb movement. As human patients with mutations in the fibrillin genes FBN1 and FBN2 often present with muscle weakness and atrophy as a symptom, Fbn2-null mice will be a useful model for examining this aspect of the disease process further.

Modulation of flight muscle power output in budgerigars Melopsittacus undulatus and zebra finches Taeniopygia guttata: in vitro muscle performance.

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.

The energetic benefits of tendon springs in running: is the reduction of muscle work important?

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.

Locomotion on a slope in leaf-cutter ants: metabolic energy use, behavioural adaptations and the implications for route selection on hilly terrain

SUMMARY The metabolic cost of the negotiation of obstacles, and the influence that this has on route selection, are important determinants of an animals locomotor behaviour. We determined the gross metabolic cost of locomotion on slopes of different gradients, ranging from –90 to +90 deg, in leaf-cutter ants (Acromyrmex octospinosus) in a closed-circuit respirometry system. Ants were able to select their preferred speed for each gradient. The gross metabolic energy expenditure per unit distance travelled on the slope (Cpath) was calculated from the rate of CO2 production and the speed of locomotion. These data were used to predict the optimal slopes for minimising the vertical cost of locomotion and vertical journey time. The gross rate of CO2 production was approximately constant (1.7 ml g–1 h–1) and was not significantly affected by slope. Ants moderated their speed with slope (P<0.05), travelling the fastest during level locomotion (2.0±0.1 cm s–1, N=20) and increasingly slowly with increased gradient (both on an incline and a decline). Cpath varied significantly with slope, being lowest during level locomotion (646.0±51.2 J kg–1 m–1) and increasing with increasing gradient. These results suggest that ants adapt their locomotor behaviour to keep metabolic rate constant despite changing mechanical demands. It is predicted that when undertaking a journey involving vertical displacement that ants will select routes with a gradient of between 51 and 57 deg during ascent and with a gradient of between –45 and –51 deg during descent, in order to minimise both vertical journey time and vertical cost of locomotion.

The mechanical power output of the pectoralis muscle of cockatiel (Nymphicus hollandicus): the in vivo muscle length trajectory and activity patterns and their implications for power modulation.

SUMMARY In order to meet the varying demands of flight, pectoralis muscle power output must be modulated. In birds with pectoralis muscles with a homogeneous fibre type composition, power output can be modulated at the level of the motor unit (via changes in muscle length trajectory and the pattern of activation), at the level of the muscle (via changes in the number of motor units recruited), and at the level of the whole animal (through the use of intermittent flight). Pectoralis muscle length trajectory and activity patterns were measured in vivo in the cockatiel (Nymphicus hollandicus) at a range of flight speeds (0–16 m s−1) using sonomicrometry and electromyography. The work loop technique was used to measure the mechanical power output of a bundle of fascicles isolated from the pectoralis muscle during simulated in vivo length change and activity patterns. The mechanical power–speed relationship was U-shaped, with a 2.97-fold variation in power output (40–120 W kg−1). In this species, modulation of neuromuscular activation is the primary strategy utilised to modulate pectoralis muscle power output. Maximum in vivo power output was 22% of the maximum isotonic power output (533 W kg−1) and was generated at a lower relative shortening velocity (0.28Vmax) than the maximum power output during isotonic contractions (0.34Vmax). It seems probable that the large pectoralis muscle strains result in a shift in the optimal relative shortening velocity in comparison with the optimum during isotonic contractions as a result of length–force effects.

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

SUMMARY Much of Bob Boutiliers 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 O2 lack and to advance our understanding of the ecological relevance of hypoxia tolerance in frogs. Work from Bobs 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 O2 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 O2 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 O2 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 Boutiliers 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.

Comparison between mechanical power requirements of flight estimated using an aerodynamic model and in vitro muscle performance in the cockatiel (Nymphicus hollandicus)

SUMMARY There have been few comparisons between the relationship between the mechanical power requirements of flight and flight speed obtained using different approaches. It is unclear whether differences in the power–speed relationships reported in the literature are due to the use of different techniques for determining flight power or due to inter-specific differences. Here we compare the power–speed relationships in cockatiels (Nymphicus hollandicus) determined using both an aerodynamic model and measurements of in vitro performance of bundles of pectoralis muscle fibres under simulated in vivo strain and activity patterns. Aerodynamic power was calculated using different ranges of values for the coefficients in the equations: induced power factor (k 1.0–1.4), the profile (CD,pro 0.01–0.03) and parasite drag (CD,par 0.05–0.195) coefficients. We found that the aerodynamic power-speed relationship was highly sensitive to the values assumed for these coefficients and best fit the power calculated from in vitro muscle performance when k=1.2, CD,pro=0.02 and CD,par=0.13.

The effects of asymmetric length trajectories on the initial mechanical efficiency of mouse soleus muscles

SUMMARY Asymmetric cycles with more than half of the cycle spent shortening enhance the mechanical power output of muscle during flight and vocalisation. However, strategies that enhance muscle mechanical power output often compromise efficiency. In order to establish whether a trade-off necessarily exists between power and efficiency, we investigated the effects of asymmetric muscle length trajectories on the maximal mechanical cycle-average power output and initial mechanical efficiency (Ei). Work and heat were measured in vitro in a mouse soleus muscle undergoing contraction cycles with 25% (Saw25%), 50% (Saw50%) and 75% (Saw75%) of the cycles spent shortening. Cycle-average power output tended to increase with the proportion of the cycle spent shortening at a given frequency. Maximum cycle-average power output was 102.9±7.6 W kg–1 for Saw75% cycles at 5 Hz. Ei was very similar for Saw50% and Saw75% cycles at all frequencies (approximately 0.27 at 5 Hz). Saw25% cycles had Ei values similar to those of Saw50% and Saw75% cycles at 1 Hz (approximately 0.20), but were much less efficient at 5 Hz (0.08±0.03). The lower initial mechanical efficiency of Saw25% cycles at higher frequencies suggests that initial mechanical efficiency is reduced if the time available for force generation and relaxation during shortening is insufficient. The similar initial mechanical efficiency of Saw50% and Saw75% cycles at all frequencies shows that increasing the proportion of the contraction cycle spent shortening is a strategy that allows an animal to increase muscle mechanical power output without compromising initial mechanical efficiency.