Primary Flight Muscles Research Articles

Reduction of wing area affects estimated stress in the primary flight muscles of chickens.

In flying birds, the pectoralis (PECT) and supracoracoideus (SUPRA) generate most of the power required for flight, while the wing feathers create the aerodynamic forces. However, in domestic laying hens, little is known about the architectural properties of these muscles and the forces the wings produce. As housing space increases for commercial laying hens, understanding these properties is important for assuring safe locomotion. We tested the effects of wing area loss on mass, physiological cross-sectional area (PCSA), and estimated muscle stress (EMS) of the PECT and SUPRA in white-feathered laying hens. Treatments included Unclipped (N = 18), Half-Clipped with primaries removed (N = 18) and Fully-Clipped with the primaries and secondaries removed (N = 18). The mass and PCSA of the PECT and SUPRA did not vary significantly with treatment. Thus, laying hen muscle anatomy may be relatively resistant to changes in external wing morphology. We observed significant differences in EMS among treatments, as Unclipped birds exhibited the greatest EMS. This suggests that intact wings provide the greatest stimulus of external force for the primary flight muscles.

Solving the thoracic inverse problem in the fruit fly

In many insect species, the thoracic exoskeletal structure plays a crucial role in enabling flight. In the dipteran indirect flight mechanism, thoracic cuticle acts as a transmission link between the flight muscles and the wings, and is thought to act as an elastic modulator: improving flight motor efficiency thorough linear or nonlinear resonance. But peering closely into the drivetrain of tiny insects is experimentally difficult, and the nature of this elastic modulation is unclear. Here, we present a new inverse-problem methodology to surmount this difficulty. In a data synthesis process, we integrate literature-reported rigid-wing aerodynamic and musculoskeletal data into a planar oscillator model for the fruit fly Drosophila melanogaster, and use this integrated data to identify several surprising properties of the fly’s thorax. We find that fruit flies likely have an energetic need for motor resonance: absolute power savings due to motor elasticity range from 0%–30% across literature-reported datasets, averaging 16%. However, in all cases, the intrinsic high effective stiffness of the active asynchronous flight muscles accounts for all elastic energy storage required by the wingbeat. The D. melanogaster flight motor should be considered as a system in which the wings are resonant with the elastic effects of the motor’s asynchronous musculature, and not with the elastic effects of the thoracic exoskeleton. We discover also that D. melanogaster wingbeat kinematics show subtle adaptions that ensure that wingbeat load requirements match muscular forcing. Together, these newly-identified properties suggest a novel conceptual model of the fruit fly’s flight motor: a structure that is resonant due to muscular elasticity, and is thereby intensely concerned with ensuring that the primary flight muscles are operating efficiently. Our inverse-problem methodology sheds new light on the complex behaviour of these tiny flight motors, and provides avenues for further studies in a range of other insect species.

Musculoskeletal wing-actuation model of hummingbirds predicts diverse effects of primary flight muscles in hovering flight.

Hummingbirds have evolved to hover and manoeuvre with exceptional flight control. This is enabled by their musculoskeletal system that successfully exploits the agile motion of flapping wings. Here, we synthesize existing empirical and modelling data to generate novel hypotheses for principles of hummingbird wing actuation. These may help guide future experimental work and provide insights into the evolution and robotic emulation of hummingbird flight. We develop a functional model of the hummingbird musculoskeletal system, which predicts instantaneous, three-dimensional torque produced by primary (pectoralis and supracoracoideus) and combined secondary muscles. The model also predicts primary muscle contractile behaviour, including stress, strain, elasticity and work. Results suggest that the primary muscles (i.e. the flight 'engine') function as diverse effectors, as they do not simply power the stroke, but also actively deviate and pitch the wing with comparable actuation torque. The results also suggest that the secondary muscles produce controlled-tightening effects by acting against primary muscles in deviation and pitching. The diverse effects of the pectoralis are associated with the evolution of a comparatively enormous bicipital crest on the humerus.

In vivo X-ray diffraction and simultaneous EMG reveal the time course of myofilament lattice dilation and filament stretch.

Muscle function within an organism depends on the feedback between molecular and meter-scale processes. Although the motions of muscle's contractile machinery are well described in isolated preparations, only a handful of experiments have documented the kinematics of the lattice occurring when multi-scale interactions are fully intact. We used time-resolved X-ray diffraction to record the kinematics of the myofilament lattice within a normal operating context: the tethered flight of Manduca sexta As the primary flight muscles of M.sexta are synchronous, we used these results to reveal the timing of in vivo cross-bridge recruitment, which occurred 24 ms (s.d. 26) following activation. In addition, the thick filaments stretched an average of 0.75% (s.d. 0.32) and thin filaments stretched 1.11% (s.d. 0.65). In contrast to other in vivo preparations, lattice spacing changed an average of 2.72% (s.d. 1.47). Lattice dilation of this magnitude significantly affects shortening velocity and force generation, and filament stretching tunes force generation. While the kinematics were consistent within individual trials, there was extensive variation between trials. Using a mechanism-free machine learning model we searched for patterns within and across trials. Although lattice kinematics were predictable within trials, the model could not create predictions across trials. This indicates that the variability we see across trials may be explained by latent variables occurring in this naturally functioning system. The diverse kinematic combinations we documented mirror muscle's adaptability and may facilitate its robust function in unpredictable conditions.

Evolution of avian flight: muscles and constraints on performance.

Competing hypotheses about evolutionary origins of flight are the 'fundamental wing-stroke' and 'directed aerial descent' hypotheses. Support for the fundamental wing-stroke hypothesis is that extant birds use flapping of their wings to climb even before they are able to fly; there are no reported examples of incrementally increasing use of wing movements in gliding transitioning to flapping. An open question is whether locomotor styles must evolve initially for efficiency or if they might instead arrive due to efficacy. The proximal muscles of the avian wing output work and power for flight, and new research is exploring functions of the distal muscles in relation to dynamic changes in wing shape. It will be useful to test the relative contributions of the muscles of the forearm compared with inertial and aerodynamic loading of the wing upon dynamic morphing. Body size has dramatic effects upon flight performance. New research has revealed that mass-specific muscle power declines with increasing body mass among species. This explains the constraints associated with being large. Hummingbirds are the only species that can sustain hovering. Their ability to generate force, work and power appears to be limited by time for activation and deactivation within their wingbeats of high frequency. Most small birds use flap-bounding flight, and this flight style may offer an energetic advantage over continuous flapping during fast flight or during flight into a headwind. The use of flap-bounding during slow flight remains enigmatic. Flap-bounding birds do not appear to be constrained to use their primary flight muscles in a fixed manner. To improve understanding of the functional significance of flap-bounding, the energetic costs and the relative use of alternative styles by a given species in nature merit study.This article is part of the themed issue 'Moving in a moving medium: new perspectives on flight'.

Heat dissipation during hovering and forward flight in hummingbirds.

Flying animals generate large amounts of heat, which must be dissipated to avoid overheating. In birds, heat dissipation is complicated by feathers, which cover most body surfaces and retard heat loss. To understand how birds manage heat budgets during flight, it is critical to know how heat moves from the skin to the external environment. Hummingbirds are instructive because they fly at speeds from 0 to more than 12 m s−1, during which they transit from radiative to convective heat loss. We used infrared thermography and particle image velocimetry to test the effects of flight speed on heat loss from specific body regions in flying calliope hummingbirds (Selasphorus calliope). We measured heat flux in a carcass with and without plumage to test the effectiveness of the insulation layer. In flying hummingbirds, the highest thermal gradients occurred in key heat dissipation areas (HDAs) around the eyes, axial region and feet. Eye and axial surface temperatures were 8°C or more above air temperature, and remained relatively constant across speeds suggesting physiological regulation of skin surface temperature. During hovering, birds dangled their feet, which enhanced radiative heat loss. In addition, during hovering, near-body induced airflows from the wings were low except around the feet (approx. 2.5 m s−1), which probably enhanced convective heat loss. Axial HDA and maximum surface temperature exhibited a shallow U-shaped pattern across speeds, revealing a localized relationship with power production in flight in the HDA closest to the primary flight muscles. We conclude that hummingbirds actively alter routes of heat dissipation as a function of flight speed.

Fibre types in primary ‘flight’ muscles of the African Penguin (Spheniscus demersus)

AbstractThe African penguin (Spheniscus demersus) is an endangered seabird that resides on the temperate southern coast of Africa. Like all penguins it is flightless, instead using its specialized wings for underwater locomotion termed ‘aquatic flight’. While musculature and locomotion of the large Antarctic penguins have been well studied, smaller penguins show different biochemical and behavioural adaptations to their habitats. We used histochemical and immunohistochemical methods to characterize fibre type composition of the African penguin primary flight muscles, the pectoralis and supracoracoideus. We hypothesized the pectoralis would contain predominantly fast oxidative–glycolytic (FOG) fibres, with mainly aerobic subtypes. As the supracoracoideus and pectoralis both power thrust, we further hypothesized these muscles would have a similar fibre type complement. Our results supported these hypotheses, also showing an unexpected slow fibre population in the deep parts of pectoralis and supracoracoideus. The latissimus dorsi was also examined as it may contribute to thrust generation during aquatic flight, and in other avian species typically contains definitive fibre types. Unique among birds studied to date, the African penguin anterior latissimus dorsi was found to consist mainly of fast fibres. This study shows the African penguin has specialized flight musculature distinct from other birds, including large Antarctic penguins.

Neuromuscular control of hovering wingbeat kinematics in response to distinct flight challenges in the ruby-throated hummingbird (Archilochus colubris)

While producing one of the highest sustained mass-specific power outputs of any vertebrate, hovering hummingbirds must also precisely modulate the activity of their primary flight muscles to vary wingbeat kinematics and modulate lift production. Although recent studies have begun to explore how pectoralis (the primary downstroke muscle) neuromuscular activation and wingbeat kinematics are linked in hummingbirds, it is unclear whether different species modulate these features in similar ways, or consistently in response to distinct flight challenges. In addition, little is known about how the antagonist, the supracoracoideus, is modulated to power the symmetrical hovering upstroke. We obtained simultaneous recordings of wingbeat kinematics and electromyograms from the pectoralis and supracoracoideus in ruby-throated hummingbirds (Archilochus colubris) hovering under the following conditions: (1) ambient air, (2) air density reduction trials, (3) submaximal load-lifting trials and (4) maximal load-lifting trials. Increased power output was achieved through increased stroke amplitude during air density reduction and load-lifting trials, but wingbeat frequency only increased at low air densities. Overall, relative electromyographic (EMG) intensity was the best predictor of stroke amplitude and is correlated with angular velocity of the wingtip. The relationship between muscle activation intensity and kinematics was independent of treatment type, indicating that reduced drag on the wings in hypodense air did not lead to high wingtip angular velocities independently of increased muscle work. EMG bursts consistently began and ended before muscle shortening under all conditions. During all sustained hovering, spike number per burst consistently averaged 1.2 in the pectoralis and 2.0 in the supracoracoideus. The number of spikes increased to 2.5-3 in both muscles during maximal load-lifting trials. Despite the relative kinematic symmetry of the hovering downstroke and upstroke, the supracoracoideus was activated ~1 ms earlier, EMG bursts were longer (~0.9 ms) and they exhibited 1.6 times as many spikes per burst. We hypothesize that earlier and more sustained activation of the supracoracoideus fibres is necessary to offset the greater compliance resulting from the presence of the supracoracoid tendon.

Biological Investigation of Wing Motion of the Manduca Sexta

An investigation was conducted assessing the feasibility of reproducing the biological flapping motion of the wings of the hawkmoth, Manduca sexta (M.sexta) by artificially stimulating the flight muscles for Micro Air Vehicle research. Electromyographical signals were collected using bipolar intramuscular fine wire electrodes inserted into the primary flight muscles, the dorsal longitudinal and dorsal ventral muscles, of the adult M.sexta. These signals were recorded and associated with wing movement using high speed video. The signals were reapplied into the corresponding muscle groups with the intention of reproducing similar flapping motion. A series of impulse signals were also directed into the primary flight muscles as a means of observing muscle response through measured forewing angles. This study pioneered electromyographic research on M.sexta at the Air Force Institute of Technology with tests conducted with fine wire electrodes. Through this process, the research showed the deformational structural changes that take place when a wing is removed from an insect and proved that muscular stimulation is a viable method for generating wing movement. This study also assisted in developing an understanding related to the role that a thorax-like fuselage could play in future micro aircraft designs. This study has shown that partial neuromuscular control of the primary flight muscles of M.sexta is possible with electrical stimulants which could be used to directly control insect flight.

Muscle function in avian flight: achieving power and control

Flapping flight places strenuous requirements on the physiological performance of an animal. Bird flight muscles, particularly at smaller body sizes, generally contract at high frequencies and do substantial work in order to produce the aerodynamic power needed to support the animal's weight in the air and to overcome drag. This is in contrast to terrestrial locomotion, which offers mechanisms for minimizing energy losses associated with body movement combined with elastic energy savings to reduce the skeletal muscles' work requirements. Muscles also produce substantial power during swimming, but this is mainly to overcome body drag rather than to support the animal's weight. Here, I review the function and architecture of key flight muscles related to how these muscles contribute to producing the power required for flapping flight, how the muscles are recruited to control wing motion and how they are used in manoeuvring. An emergent property of the primary flight muscles, consistent with their need to produce considerable work by moving the wings through large excursions during each wing stroke, is that the pectoralis and supracoracoideus muscles shorten over a large fraction of their resting fibre length (33-42%). Both muscles are activated while being lengthened or undergoing nearly isometric force development, enhancing the work they perform during subsequent shortening. Two smaller muscles, the triceps and biceps, operate over a smaller range of contractile strains (12-23%), reflecting their role in controlling wing shape through elbow flexion and extension. Remarkably, pigeons adjust their wing stroke plane mainly via changes in whole-body pitch during take-off and landing, relative to level flight, allowing their wing muscles to operate with little change in activation timing, strain magnitude and pattern.

Morphology and histochemistry of primary flight muscles in Rhinolophus mehelyii

Two primary flight muscles of Rhinolophus mehelyii were studied using morphological and histochemical analysis. Two fast-twitch fiber types are histochemically identified in pectoralis muscles of R. mehelyii. These were classified as type IIa and type IIb according to glycine-calcium-formalin preincubation staining protocol for myosin ATPase. The primary flight muscles, serratus ventralis included type I, type IIa and type IIb fibers. Type I fibers were highly oxidative, as stained dark for NADHTR. Type IIa fibers exhibited relatively weak staining properties for NADH-TR and SDH, indicating an intermediate oxidative capacity. Type IIb fibers showed low oxidative capacity, as indicated by weak reaction for NADH-TR.

Biomechanics of bird flight

Power output is a unifying theme for bird flight and considerable progress has been accomplished recently in measuring muscular, metabolic and aerodynamic power in birds. The primary flight muscles of birds, the pectoralis and supracoracoideus, are designed for work and power output, with large stress (force per unit cross-sectional area) and strain (relative length change) per contraction. U-shaped curves describe how mechanical power output varies with flight speed, but the specific shapes and characteristic speeds of these curves differ according to morphology and flight style. New measures of induced, profile and parasite power should help to update existing mathematical models of flight. In turn, these improved models may serve to test behavioral and ecological processes. Unlike terrestrial locomotion that is generally characterized by discrete gaits, changes in wing kinematics and aerodynamics across flight speeds are gradual. Take-off flight performance scales with body size, but fully revealing the mechanisms responsible for this pattern awaits new study. Intermittent flight appears to reduce the power cost for flight, as some species flap-glide at slow speeds and flap-bound at fast speeds. It is vital to test the metabolic costs of intermittent flight to understand why some birds use intermittent bounds during slow flight. Maneuvering and stability are critical for flying birds, and design for maneuvering may impinge upon other aspects of flight performance. The tail contributes to lift and drag; it is also integral to maneuvering and stability. Recent studies have revealed that maneuvers are typically initiated during downstroke and involve bilateral asymmetry of force production in the pectoralis. Future study of maneuvering and stability should measure inertial and aerodynamic forces. It is critical for continued progress into the biomechanics of bird flight that experimental designs are developed in an ecological and evolutionary context.

Bat flight-muscle mass: implications for foraging strategy

The primary flight muscles of the chest, shoulder, back and upper arms were weighed for 29 species of Australian bat, representing two suborders and six families. Values of muscle masses were found to be between 9 and 23% of the mass of the bat (mbat) and aligned into three statistically distinct classes that relate foraging strategy with morphology when plotted against mbat. These classes represent 'high-energy', 'general' and 'low-energy' foraging strategies. The above relationships were visible in both the wing downstroke and upstroke muscle groups, but not in the shoulder and elbow flex/extend groups. Differences in the foraging ecologies and geographical distributions of Western Australian bats are reflected in 'flight motor power output' as well as the bats' 'airframe design' attributes. Based on these attributes and ecologies, a method is presented for estimating the mass of flight muscle.

Morphology, Velocity, and Intermittent Flight in Birds1

Body size, pectoralis composition, aspect ratio of the wing, and forward speed affect the use of intermittent flight in birds. During intermittent non-flapping phases, birds extend their wings and glide or flex their wings and bound. The pectoralis muscle is active during glides but not during bounds; activity in other primary flight muscles is variable. Mechanical power, altitude, and velocity vary among wingbeats in flapping phases; associated with this variation are changes in neuromuscular recruitment, wingbeat frequency, amplitude, and gait. Species of intermediate body mass (35–158 g) tend to flap-glide at slower speeds and flap-bound at faster speeds, regardless of the aspect ratio of their wings. Such behavior may reduce mechanical power output relative to continuous flapping. Smaller species (<20 g) with wings of low aspect ratio may flap-bound at all speeds, yet existing models do not predict an aerodynamic advantage for the flight style at slow speeds. The behavior of these species appears to be due to wing shape rather than pectoralis physiology. As body size increases among species, percent time spent flapping increases, and birds much larger than 300 g do not flap-bound. This pattern may be explained by adverse scaling of mass-specific power or lift per unit power output available from flight muscles. The size limit for the ability to bound intermittently may be offset somewhat by the scaling of pectoralis composition. The percentage of time spent flapping during intermittent flight also varies according to flight speed.

Anatomy and histochemistry of flight muscles in a wing-propelled diving bird, the Atlantic puffin, Fratercula arctica.

Twenty-three species within the avian family Alcidae are capable of wing-propelled flight in the air and underwater. Alcids have been viewed as Northern Hemisphere parallels to penguins, and have often been studied to see if their underwater flight comes at a cost, compromising their aerial flying ability. We examined the anatomy and histochemistry of select wing muscles (Mm. pectoralis, supracoracoideus, latissimus dorsi caudalis, coracobrachialis caudalis, triceps scapularis, and scapulohumeralis caudalis) from Atlantic puffins (Fratercula arctica) to assess if the muscle fiber types reveal the existence of a compromise associated with "dual-medium" flight. Pectoralis was found to be proportional in size with that of nondiving species, although the supracoracoideus was proportionally larger in puffins. Muscle fiber types were largely aerobic in both muscles, with two distinct fast-twitch types demonstrable: a smaller, aerobic, moderately glycolytic population (FOg), and a larger, moderately aerobic, glycolytic population (FoG). The presence of these two fiber types in the primary flight muscles of puffins suggests that aerial and underwater flight necessitate a largely aerobic fiber complement. We suggest that alcids do not represent an adaptive compromise, but a stable adaptation for wing-propelled locomotion both in the air and underwater.

NEUROMUSCULAR CONTROL AND KINEMATICS OF INTERMITTENT FLIGHT IN BUDGERIGARS (MELOPSITTACUS UNDULATUS)

Kinematic and electromyographic data were collected from budgerigars (parakeets), Melopsittacus undulatus, flying at different speeds in a variable-speed wind tunnel. Birds exhibited flap-gliding at low speeds and flap-bounding at high speeds. The percentage of time spent flapping generally decreased at intermediate speeds. These behavior patterns are consistent with minimizing energy expenditure according to aerodynamic theory. During intermittent glides, the pectoralis exhibited an isometric contraction while the supracoracoideus was inactive. During bounds, both muscles were inactive. Contrary to earlier work, our studies indicate that budgerigars do not exhibit simultaneous twitch contractions of the pectoralis during each wingbeat, but rather generate typical multiple-spike electromyographic bursts that represent motor unit action potential trains or asynchronous twitch contractions from different motor units. The relative intensity of electromyographic bursts from the primary flight muscles increased with flight speed. This may indicate an increase in force production. Our observations of isometric contractions during glides, along with patterns of variation in muscle activity and wingbeat frequency, do not support the hypothesis that small birds such as the budgerigar use flap-bounding as their only means of reducing power output during flight.

Musculotopic innervation of the primary flight muscles, the pectoralis (Pars thoracicus) and supracoracoideus, of the pigeon (Columba livia): a WGA-HRP Study.

The distribution of motoneurons innervating the primary depressor and elevator muscles of the wing of the domestic pigeon (Columba livia) was studied by using the retrograde axonal tracer lectin-conjugated horseradish peroxidase (WGA-HRP). Injection of WGA-HRP into the pectoralis (pars thoracicus) labeled neurons in the ventromedial corner of the lateral motor column of the spinal cord. These neurons were arranged in a column extending from spinal segment X or XI to spinal segment XII or XIII. The pectoralis, the primary depressor muscle of the wing, consists of two parts which are anatomically and functionally distinct, the sternobrachialis (SB) and thoracobrachialis (TB). Injection into the SB labeled neurons in the rostral and middle regions of the pectoralis motoneuron column. In contrast, injection into the TB labeled neurons in the middle and caudal regions of the pectoralis motoneuron column. Injection into the primary elevator muscle of the wing, the supracoracoideus, labeled neurons in the lateral motor column in spinal segments X and XI. These motoneurons were located dorsolateral to motoneurons labeled following pectoralis injection. These data demonstrate musculotopic segregation of the motoneurons innervating the primary flight muscles in the pigeon and, further, illustrate that the SB and TB subregions of the pectoralis are innervated by discrete aggregations of motoneurons.

Histochemistry of flight muscles in the jamaican fruit bat, Artibeus jamaicensis: Implications for motor control

Two fast-twitch fiber types are histochemically identified in the primary flight muscles of Artibeus jamaicensis. These are classified as type IIa and IIb according to an acid-preincubation staining protocol for myosin ATPase. All fibers in the bat flight muscles exhibit relatively intense staining properties for NADH-TR, suggesting a high oxidative capacity. The glycolytic potential of all fibers is rather low, as assessed by stains for alpha-GPD. This two-type histochemical profile appears to parallel biphasic electromyographic patterns observed in these muscles and leads us to propose that flight muscle histochemistry and activation are mediated by a "two-gear" neuromuscular control system. In contrast, earlier studies on Tadarida brasiliensis demonstrate the existence of a "one-gear" neuromuscular control system, exemplified by the presence of one fiber type. These observations are discussed with respect to the natural history and flight styles of several species.

Morphology and Histochemistry of Flight Muscles in Free-Tailed Bats, Tadarida brasiliensis

Three primary and two accessory flight muscles of Tadarida brasiliensis were studied using gross dissection and histochemical analysis. The pectoralis, subscapularis, and serratus ventralis thoracis muscles were composed entirely of fast oxidative fibers (FO), except for a restricted caudal portion of the latter muscle that included a small percentage of slow fibers (SO). The accessory flight muscles, triceps brachii and biceps brachii, included predominantly FO fibers except for deep-lying fascicles where a mixture of FO and SO fibers occurred. The exclusive presence of FO fibers in the primary flight muscles reflects the metabolic demands for high-speed flight over extended periods of time. The monotypic histochemical profile in these muscles represents a one-gear mechanical system for force production. Mixed populations of fiber types in the accessory flight muscles reflect the maintenance of postural or tonic role within these muscle groups. No fast glycolytic (FG) fibers were observed in any of the muscles studied, thus emphasizing the importance of oxidative metabolism in the flight muscles.