From Studying Real Hummingbirds to Designing Hummingbird-Like Robots—A Literature Review <s> II. MUSCLE OF HUMMINGBIRD <s> The hovering ability, rapidity of maneuvers and upregulated aerobic capacity of hummingbirds have long attracted the interest of flight biologists. The range of intra- and interspecific variation in flight performance among hummingbirds, however, is equally impressive. A dominant theme in hummingbird evolution is progressive invasion of higher-elevation habitats. Hypobaric challenge is met behaviorally through compensatory changes in wingbeat kinematics, particularly in stroke amplitude. Over evolutionary time scales, montane colonization is associated with increases in body mass and relative wing area. Hovering ability has been well-studied in several North American hummingbird taxa, yet the broad range of interspecific variation in hummingbird axial and appendicular anatomy remains to be assessed mechanistically. Such varied features as tail length, molt condition and substantial weight change due to lipid-loading can dramatically alter various features of the flight envelope. Compared with our present knowledge of hovering performance in hummingbirds, the mechanics of forward flight and maneuvers is not well understood. Relationships among flight-related morphology, competitive ability and foraging behavior have been the focus of numerous studies on tropical and temperate hummingbirds. Ecologists have hypothesized that the primary selective agents on hummingbird flight-related morphology are the behaviors involved in floral nectar consumption. However, flight behaviors involved in foraging for insects may also influence the evolution of wing size and shape. Several comparisons of hummingbird communities across elevational gradients suggest that foraging strategies and competitive interactions within and among species vary systematically across elevations as the costs of flight change with body size and wing shape. <s> BIB001 </s> From Studying Real Hummingbirds to Designing Hummingbird-Like Robots—A Literature Review <s> II. MUSCLE OF HUMMINGBIRD <s> Studies of medium- and large-bodied avian species have suggested that variation in flight muscle composition is related to differences in flight behavior. For example, slow-twitch or tonic fibers are generally found only in the flight muscles of non-volant or soaring/gliding birds. However, we know comparatively little about fiber composition of the muscles of the smallest birds. Here we describe the fiber composition of muscles from the wings, shoulders, and legs of two small avian species, which also display very high wingbeat frequencies: Anna's hummingbirds (Calypte anna) and zebra finches (Taeniopygia guttata). All flight muscles examined in both species contained exclusively fast oxidative glycolytic (FOG) fibers. These unique results suggest that fast oxidative fibers are both necessary and sufficient for the full range of flight behaviors in these small-bodied birds. Like all other studied birds, the zebra finch gastrocnemius, a tarsometatarsal extensor, contained a mixture of FOG (27.1%), slow oxidative (SO, 12.7%), and fast glycolytic (FG, 60.2%) fibers. By contrast, the hummingbird gastrocnemius lacked FG fibers (85.5% FOG, 14.5% SO), which may reflect the reduced role of the hindlimb during take-off. We further hypothesize that thermogenic requirements constrain fiber type heterogeneity in these small endothermic vertebrates. <s> BIB002 </s> From Studying Real Hummingbirds to Designing Hummingbird-Like Robots—A Literature Review <s> II. MUSCLE OF HUMMINGBIRD <s> 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. <s> BIB003
The hummingbird's flight pattern is unique and insect-like, and they can easily hover, manoeuvre and even fly backwards. One reason is that they have a special physiological structure of muscles applied to control or modulate wing and body posture when flying. Another is that hummingbirds' aerodynamics allows for lift production in each half of stroke and achieves the characterized flight pattern by high wingbeat frequency, small muscle strains, and a highly supinated wing orientation during each end of strokes BIB001 . A hummingbird has massive muscles, shown in Fig. 3 . However, the wing is mainly moved by a pair of powerful muscles: the pectoralis major (''depressor'' muscle or breast muscle) powers the downstroke and supracoracoideus muscles (''elevator'' muscles) are responsible for upstroke BIB003 . The breast muscle originates from the sternum like the breastbone and attaches near the bottom of the humerus (the upper arm bone), whereas the supracoracoideus muscle connects between the keel of the sternum and the top humerus. The wings flap down when the pectoralis major contracts, and flap up when supracoracoideus muscle shortens, shown in Fig. 4 . The depressor is twice as heavy as the elevator, corresponding to the uneven lift production between downstroke and upstroke. The hummingbird muscles compose up to 30% of the body weight [37] . The pectoralis and supracoracoideus muscles are clearly shown in Fig. 3 . Muscles activity of hummingbirds in hovering is shaded when flapping in the downstroke. The pectoralis is shown in Fig. 3 (A), whereas supracoracoideus muscles are displayed in Fig. 3 (B) and the pectoralis muscle is removed. Birds separately operate muscles of pectoralis and supracoracoideus to flap downstroke and upstroke. The size of supracoracoideus in most of the birds is 1/5 th that of the pectoralis, which results in upstroke limitation aerodynamically. However, the flight muscle construction of hummingbird differs and they have almost the same size as pectoralis and supracoracoideus. The extreme proportion of two types of muscles is applied to complete the lift force generation in each half of stroke BIB002 . The reason that hummingbird is capable of flapping with high wingbeat frequencies and high aerobic power is mainly due to these large flight muscles widely include fast oxidative-glycolytic fibers as well as giant mitochondria, nearly occupying half of the total volume. Besides, the hummingbird is the highest mass-specific metabolic rates flyers, which means that hummingbird could switch fuels since high rates of sugar and fatty acid oxidation can satisfy high requirements of adenosine-triphosphate (ATP). For instance, the small hummingbirds have the highest known mass-specific metabolism for a vertebrate of around 40 ml oxygen per gram per hour (falling at rest to about 3 ml oxygen per gram per hour) when hovering [1] . Meanwhile, their flight muscles comprise 25-30% of their total body weight, a higher proportion than that of any other birds, and a higher density of mitochondria in flight muscles is 30% in hummingbirds, 40% in flies. Therefore, such special construction and contraction of flight muscle in hummingbirds contribute to a distinctive behavioral pattern. So to speak, the muscle composition ensures high wing beat frequency and required stroke amplitudes. By studying the hummingbirds hovering flight, it is discovered that hummingbird always chooses two patterns to stay hovering, which are varying the wing-beat frequency and changing wing-motion stroke amplitude according to the density of surrounding air flow and additional mass of body BIB003 . However, due to physiological limitations of muscles, the stretching frequency and distances of muscles are inconsistent. Namely, the hummingbirds via the pectoralis and supracoracoideus muscles stretching cannot accomplish both in a high wing-beat frequency and larger wing-motion amplitude, which is paradoxical in physiological limitations. Therefore, there must be an optimal coupling value of each frequency and amplitude for hummingbirds when flapping BIB003 .