Levels Of Which Of The Following Are Functions Of The Total Muscle Mass Of An Animal?
Philos Trans R Soc Lond B Biol Sci. 2011 May 27; 366(1570): 1496–1506.
Muscle function in avian flight: achieving power and control
Abstract
Flapping flight places strenuous requirements on the physiological performance of an animal. Bird flying muscles, particularly at smaller body sizes, generally contract at high frequencies and practice substantial piece of work in lodge 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 free energy losses associated with body movement combined with elastic free energy savings to reduce the skeletal muscles' work requirements. Muscles also produce substantial ability during swimming, but this is mainly to overcome torso elevate rather than to back up the animal'southward 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 command wing motion and how they are used in manoeuvring. An emergent property of the primary flying muscles, consistent with their need to produce considerable work by moving the wings through large excursions during each fly 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 strength development, enhancing the work they perform during subsequent shortening. 2 smaller muscles, the triceps and biceps, operate over a smaller range of contractile strains (12–23%), reflecting their role in controlling fly shape through elbow flexion and extension. Remarkably, pigeons adjust their wing stroke plane mainly via changes in whole-torso pitch during take-off and landing, relative to level flying, allowing their wing muscles to operate with little change in activation timing, strain magnitude and pattern.
Keywords: bird flight, neuromuscular function, muscle ability, fascicle strain
1. Introduction
Birds power flying primarily by big pectoralis muscles that depress the wings at the shoulder. The ascendant role and large size of the pectoralis musculus, therefore, enable a critical assessment of how muscle role is tailored to meet the mechanical ability requirements of flapping flight over a range of flying conditions. The smaller supracoracoideus muscle of birds, about one-fifth the size of the pectoralis, is the primary wing elevator agile during upstroke, especially at wearisome to moderate speeds and during hovering (at faster flying speeds, wing elevation is probably produced passively by aerodynamic forces acting on the wings, which remain extended during upstroke to maintain lift through bound circulation [1,2]). Smaller extrinsic and intrinsic wing muscles help in modulating fly orientation and controlling wing shape. These muscles probably contribute to adjustments of the wing'due south performance equally an aerofoil [3–7] and, thus, may indirectly touch on flight power requirements. However, because of their small size, the intrinsic muscles of the wing probably contribute lilliputian boosted mechanical power for flight.
Prior analyses of muscle–tendon architecture have shown that muscles differ widely in their design for irresolute length while producing forcefulness, just because of their bourgeois properties for force product and relative fibre strain (ratio of activated length alter relative to resting fibre length), skeletal muscles generally perform about the same corporeality of piece of work in proportion to their mass [viii–11]. Longer fibred muscles, such as the avian pectoralis, still, are well suited to producing the larger movements required for moving the wings to produce effective aerodynamic power for weight support and to overcome drag. In addition to having longer fibres, greater operating strains as well heighten the range of movement that a muscle generates. Thus, the operating strains of certain flight muscles are expected to be greater than those of muscles that back up an animal's weight during terrestrial locomotion [12] that contract over more limited strain ranges, allowing more than economical force production. Muscles, having short fibres that adhere to a longer tendon such as those plant in the legs of terrestrial animals, produce large forces and tin recover substantial elastic energy from their tendon and aponeurosis [12–xv]. These muscles are best used for movements that require little net shortening or lengthening of the musculus. Consequently, pinnate muscles having these architectural features are commonly found in distal limb regions. The intrinsic wing muscles of birds are usually brusque fibred and pinnate, and have long tendons. This enables these muscles to control distal movements of the wing while, at the same time, existence small and lightweight. Their function has not been much studied to date, across a few comparative functional anatomical descriptions [seven,16,17] and assessment of their neuromuscular activeness patterns [3,16,17]. Even so, these studies are important considering they provide a framework for future studies that seek to assess how the smaller intrinsic wing muscles are used to achieve flight across different weather condition, and in birds with differing wing designs and flight styles.
In the context of this before work, the functions of the two primary flight muscles of birds, the pectoralis and supracoracoideus, are reviewed here in relation to the mechanical power needed to come across the aerodynamic requirements for flapping flight. The vast majority of morphological and physiological work has largely focused on the pectoralis because of its dominant function in powering avian flight. Consequently, much of the review of avian muscle function will focus on the pectoralis, with particular comparison to its antagonist, the supracoracoideus. Preliminary in vivo analyses of the triceps and biceps muscles, which control wing shape via elbow extension and flexion, are also considered in relation to changes in flight performance required for have-off, landing and manoeuvring flight. Time to come directions for research to ameliorate our understanding of the neuromuscular control and functional design of avian flying are also identified.
ii. Functional anatomy of principal avian flight muscles
The pectoralis is a large musculus (approx. 8–11% body mass; [15,16]) that attaches to the humerus of the wing at the deltopectoral crest (DPC; figure 1). Its main portion (sternobrachialis, SB) originates from an enlarged sternal keel, with more anterior fibres arising from the furcula, or 'wishbone'. A much smaller portion (thoracobrachialis, TB) originates dorsally from ribs. The fibres of the TB and the posterior region of the SB insert on an internal aponeurosis that merges with the more anterior SB fibres before attaching to the DPC. In addition to producing mechanical work during downstroke, the pectoralis also pronates the fly. The smaller supracoracoideus lies deep to the pectoralis, besides originating from the keel of the sternum, and is almost one-5th of the pectoralis in mass (approx. ii% body mass). By means of its tendon, which inserts and acts dorsally at the shoulder as a pulley, the supracoracoideus elevates and supinates the wing during upstroke [18–21]. Whereas the pectoralis is composed of mostly long fibres with modest pinnation (pigeon: 31–67 mm, hateful 41 mm), the supracoracoideus is a classic bipinnate muscle with short fibres (pigeon: 16–23 mm, mean 20 mm). It produces elevation and supination of the wing by means of a long tendon that passes dorsally over the shoulder, via the triosseal foramen of the avian pectoral girdle, before attaching to the dorsal surface of the proximal humerus adjacent to the DPC. The pectoralis is composed mainly of fast-oxidative (blazon IIa) fibres (approx. 85% in pigeons) with a smaller component of fast-glycolytic (type IIb) fibres [twenty,21]. Fibre-type composition of the supracoracoideus, to my noesis, has not been examined in pigeons, but in the European starling is composed of a greater fraction (68%) of fast-glycolytic versus fast-oxidative fibres [22]; whereas, in zebra finches, Anna's hummingbirds [23] and Atlantic puffins [24], the supracoracoideus is exclusively equanimous of fast-oxidative fibres.
(a) Anatomical organization of avian wing musculature (adapted from Punch [3]), showing key muscles that have been studied, and (b) showing the general sites used to record pectoralis force via deltopectoral crest (DPC) os strain, pectoralis fascicle strain and neuromuscular activation (EMG).
3.In vivo assessment of avian musculus function during flight
Because of its focal insertion on the ventral surface of the DPC in pigeons (figure one b), doves, cockatiels, budgerigars, magpies and sure other species of birds, forces produced past the pectoralis can be estimated directly by means of strains recorded using a strain approximate bonded to the dorsal surface of the DPC (in several avian species, the pectoralis also inserts along the ventral proximal shaft of the humerus, preventing this approach). Details for exposing and attaching metal foil strain gauges to obtain strain-calibrated in vivo recordings of pectoralis force are described elsewhere [25,26]. Although some doubtfulness exists in the calibration of DPC strain to pectoralis muscle force [27], such recordings provide a reliable and temporally detailed recording of time-varying musculus force. Other methods for obtaining musculus strength and estimates of mechanical ability output for bird flight as well take their limitations [28,29]. A similar skeletal-strain-based arroyo to excerpt the fourth dimension-varying force transmitted past the supracoracoideus musculus via the muscle'due south tendinous insertion on to the proximal dorsal shaft of the humerus has also been used [30].
In combination with DPC strain-force recordings of the pectoralis and the supracoracoideus, in vivo measurements of muscle fascicle strain are obtained in localized muscle sites by means of sonomicrometry, a technique based on measurements of the propagation of sound pulses within the muscle to determine length changes [31]. Because the sonomicrometry transducers lie adjacent to muscle fascicle bundles, they provide a mensurate of fascicle strain rather than muscle fibre strain per se. Nevertheless, the two measures are likely to be quite similar. In the large pectoralis, sonometric measurements obtained from multiple sites (anterior and posterior SB and TB) in pigeons showed similar fascicle strain levels in the larger SB portion of the muscle, but smaller strains in the near posterior SB and TB portions of the muscle [32]. By averaging the sonomicrometry data for fascicle strain beyond recording sites (weighted by the estimated fraction of muscle mass that each site represents) or by relying on a single recording site inside the musculus and bold the site is representative for the muscle as a whole, the total work of the muscle can be assessed based on the muscle's length modify. Musculus work is therefore determined past fascicle strain multiplied by boilerplate fascicle length, in relation to the fourth dimension-varying force the muscle produces. The product of muscle fascicle length change and force is visualized equally a piece of work loop over the class of a wingbeat, or musculus contraction, bike. The timing of muscle activation is recorded simultaneously using fine-wire electromyography (EMG) electrodes inserted into and anchored adjacent to those fascicles for which a sonometric evaluation of strain is recorded [31]. The EMG provides a measure of the timing of musculus activation and relative motor recruitment in relation to muscle strength and length change. In total, the force, strain and neuromuscular activation recorded from the muscle serve to describe the temporal dynamics of the muscle'southward contractile operation beyond a range of flight conditions.
4. Functional analysis of pectoralis and supracoracoideus muscles during flight
The pectoralis muscle is activated to contract late in the upstroke, prior to wing reversal (figure 2 a). Forcefulness development follows shortly later on the first of activation (approx. two–8 ms in pigeons and cockatiels) and peaks early on in the downstroke, continuing until the end of the downstroke. The pectoralis undergoes a slight stretch or remains near isometric (depending on the species and flight condition studied), as force develops tardily in the upstroke and through wing reversal to brainstorm the downstroke (figures2 and 3). By developing force while nearly isometric or being briefly stretched, the rate of force rise and the magnitude of peak strength are appreciably enhanced owing to force–velocity effects [35,36]. As a upshot, the work that the pectoralis performs is substantially increased while the muscle shortens during the remainder of the downstroke. Deactivation of the pectoralis occurs early in the downstroke, almost ancillary with the timing of tiptop forcefulness generation. This allows the musculus to relax to about zero force prior to beingness stretched passively in the upstroke. Importantly, this reduces the antagonistic ('negative') work required of the supracoracoideus to drag the fly. The timing of pectoralis deactivation relative to its continuing force production points to the problematic nature of inferring muscle force production based on EMG recordings alone.
Representative in vivo recordings of pectoralis fascicle strain, neuromuscular activation (EMG) and force for three wingbeats in a cockatiel flying at seven m due south−1 in a current of air tunnel. Solid line, wrist; dotted line, wingtip. Adapted from Hedrick et al. [33].
Representative in vivo work-loop patterns produced by the (a) pectoralis of cockatiels (Nymphicus hollandicus) at iii dissimilar flight speeds (adjusted from Hedrick et al. [33]), and (b) the pectoralis of iii other species: ring-cervix doves (Streptopelia risoria), pigeons (Columba livia) and mallard ducks (Anas platyrynchos) (adapted from Tobalske et al. [27], Biewener et al. [31] and Williamson et al. [34]). The force produced by the muscle is plotted confronting its fascicle strain (L/Fifty o, where L o is the muscle'south resting length: strain = i.0). In the first panel of (a), the dashed rectangle denotes the maximum piece of work that the muscle could produce for its maximum forcefulness and strain; the realized work of the muscle is 68% of its theoretical maximum. The strain range for all muscles is the same (0.9–i.iii, or 40% range of muscle length change), but strength ranges differ in (b) owing to the dissimilar-sized muscles. The assuming grey portion of each work loop represents the period of neuromuscular activation measured past EMG. Arrows announce the management of strength and fascicle length changes.
For those species studied [27,33,34], the in vivo force–length work behaviour of the pectoralis is generally similar beyond a range of flight speeds and conditions (effigy three). Equally noted above, activation of the pectoralis in these species occurs belatedly in upstroke, as the muscle is being lengthened (this is most extreme in the mallard, figure 3 b) or is nearly isometric, allowing the muscle to develop force rapidly for a given level of activation. In dissimilarity to classical expectations for the operating fascicle strain of a muscle (approx. 10–fifteen% of resting length based on isometric force–length properties [35,36]), the pectoralis of these species undergoes strains of 32–40% during different flight conditions (accept-off, ascending and descending flight and changes in speed during level flight), stretching 20–30% beyond the musculus's resting length (measured when the wings are folded against the bird's body on the perch), and shortening viii–12% less than the resting length. This large strain circuit underlies the ability of the pectoralis to perform substantial piece of work during the downstroke of each contraction cycle. Forces produced by the pigeon pectoralis were found to vary about twoscore per cent across flight conditions, ranging from take-off and ascending flying to landing and descending flight [26]. Forces produced by the cockatiel pectoralis during level flight beyond speeds ranging from 1 to 14 m due south−1 in a air current tunnel were found to vary by 65 per cent [33]. These forces are estimated to be less than xl–60% of the peak isometric force that the muscle tin generate [26], reflecting in part the rapid shortening that the muscle undergoes to produce piece of work. In cockatiels, doves and pigeons, the pectoralis achieves 58–73% of the maximum theoretical work output possible for the observed force and active strain range [30,33] (figure 3 a).
Non surprisingly, the supracoracoideus of pigeons exhibits mirror-like force, length and activation timing patterns relative to the pectoralis [30] (figure 4). As the main upstroke muscle, the supracoracoideus is activated belatedly in downstroke merely prior to wing reversal. The muscle develops forcefulness rapidly while being nearly isometric, reaching peak strength very early in the upstroke. The early onset of strength development by the supracoracoideus probably reflects its role in decelerating and re-accelerating the fly during the downstroke–upstroke transition, also every bit its part in wing supination [xix]. Estimates of the elastic energy storage within the supracoracoideus tendon (51 ± 62 mJ during level and 88 ± 85 mJ during ascending flight) are consistent with this role, given that the magnitude of inertial kinetic energy exceeds the amount of elastic energy stored and returned by the supracoracoideus tendon [30]. The boosted inertial power of the fly'due south motility is probably transformed into useful aerodynamic ability mainly in the downstroke, as has been traditionally assumed [37]. The rapid supination of the wing produced by the supracoracoideus is important for achieving a short-elapsing upstroke, with the potential for positive lift generation in birds with wing-tip reversal flying kinematics [38] or for minimizing unwanted negative lift. It also maximizes the duration of downstroke lift product and was probably an important feature in the development of an active flapping flight stroke [19]. Rapid supination of the fly to initiate upstroke in rufous hummingbirds [39] is key to this species' power to generate positive upstroke lift, which has been estimated to exist 25–33% of their full lift product [xl]. In pigeons, the amount of force produced antagonistically betwixt the 2 muscles was estimated to be minor [30]. During slow level flight, the negative work of the pigeon pectoralis just prior to the finish of the upstroke is about eighteen per cent of the positive piece of work the musculus performs during the downstroke. This may well reflect a part in arresting inertial energy of the wing as it is decelerated late in upstroke [30]. By comparison, negative work of the pigeon supracoracoideus is fourteen per cent of the positive piece of work that the muscle performs and occurs late in downstroke to decelerate the wing at this time.
Representative recordings of the pigeon supracoracoideus (wing height) fascicle strain, EMG and strength, and pectoralis (fly depression) fascicle strain, EMG and force recorded during take-off from an elevated perch platform and level gratuitous flying at approximately 4.five yard southward−1 (seven wingbeats are shown). Grey panels correspond the downstroke for the initial iv wingbeat cycles, with the upstroke on a white groundwork (adapted from Tobalske & Biewener [30]).
The short fibres of the bipinnate supracoracoideus muscle require them to operate over large strains, similar to those of the pectoralis. Supracoracoideus fascicle strains range from 33 to 40 per cent of the musculus's resting length during descending, ascending and level flight [thirty]. The supracoracoideus fascicles also undergo a smaller degree of stretch relative to their residue length (half-dozen–12% beyond flight weather) compared with their cyberspace shortening strain (−27% for all flying conditions). This design of fascicle length change relative to resting length is opposite to the pattern of strain observed inside pectoralis fascicles, which lengthen past 20–30% of their resting length earlier shortening to approximately 10 per cent less than rest at the end of downstroke (figure 4). Interestingly, the modulation of muscle strain in the supracoracoideus reflects mainly differences in the degree of wing depression (stretching the supracoracoideus and its tendon) that occur at the end of downstroke across the iii flying conditions that were studied. Considering of its relatively small size, the dove supracoracoideus generates 1.6 times the mass-specific muscle power output of the pectoralis. This reflects the much greater operating stresses (strength normalized to physiological cross-sectional area) of the supracoracoideus, which ranged from 85 to 125 kPa for descending versus ascending flight, compared with stresses of l–58 kPa in the pectoralis across the same flight status [30], and 57–76 kPa in an earlier study of the pigeon pectoralis when corrected for the muscle's estimated myofibrillar area [26].
v. Comparative data for avian pectoralis ability output versus speed
Considering the pectoralis is the dominant avian flight musculus (in pigeons, the pectoralis represents 60% of total wing muscle mass, A. A. Biewener 2010, unpublished information), the musculus's power output can be used to assess how whole-body power output and, indirectly, aerodynamic power output vary every bit a function of flight condition and speed in a bird. Measurements of pectoralis mechanical power output and wingbeat frequency have been published for black-billed magpies (Pica pica), cockatiels (Nymphicus hollandicus) and ringed-neck doves (Streptopelia risoria) across a range of flight speeds while flying level and steady in a current of air tunnel [27,41] (figure 5). Except for magpies, the other ii species showed a U-shaped power versus flying speed curve, generally consequent with aerodynamic theory. This reflects high induced power costs at slow flight speeds and hovering that decease as speed increases, and loftier profile and parasite power costs (attributable to increasing wing and body elevate) at higher flight speeds. The absenteeism of an observed increase in pectoralis muscle ability at higher flight speeds in magpies may reflect either an disability of this species, with its lower aspect ratio and less pointed wings, to achieve sufficient thrust in order to overcome the contour and parasite drag costs information technology incurs at higher flying speeds limiting the elevation speed that it tin can reach [27], or that the birds were unwilling to fly at faster speeds in the current of air tunnel. Although the current of air tunnel used to study the magpies was smaller (50% less in cross-dimensions of the working section) than that used to study the cockatiels and doves, artefacts such every bit a possible footing or wall event [42] were not judged by the authors to exist the basis for the magpies' lower power cost at faster flight speeds. In the 2 other species (cockatiels and doves), pectoralis muscle power output at the fastest flight speeds exceeded that produced when the birds were nearly hovering (effigy 5). Thus, although pectoralis power output was high as expected during 1 m s−1 flight in the magpies, it remains unclear why the musculus's ability output did not reach or exceed this level at faster flight speeds.
Comparative flight power curves for three avian species, showing changes in pectoralis mass-specific muscle ability (determined from calibrated DPC-strain-strength and fascicle strain recordings) versus flight speed in a wind tunnel (adapted from Tobalske et al. [27]).
Given that other muscles are involved in flapping flight and do mechanical work, it is certainly the example that the total muscle mechanical ability requirement for flight is greater than estimates based on the pectoralis alone. In the study of pigeons, for which pectoralis and supracoracoideus muscle ability output were both determined [xxx], inclusion of supracoracoideus power output increases the total power output of flight past nearly 25 per cent. Pectoralis power output beyond flight modes was three.2 times greater than that of the supracoracoideus but less than the nearly fivefold difference in muscle mass. Together, these two muscles represent 71 per cent (A. A. Biewener 2010, unpublished information) of the total fight muscle mass of a pigeon. If the remaining smaller extrinsic and intrinsic wing muscles perform the same relative mass-specific work, this would suggest a total power requirement that may be nigh 40 per cent greater than that determined for the pectoralis solitary.
Aerodynamic models for estimating the ability requirements of the flying of birds at different speeds [43–45] are usually used to infer ecological strategies for maximizing a bird's flight range or minimizing the metabolic power requirement for flying as a role of time [46]. Although measurements of pectoralis muscle mechanical power output are consistent with the full general change in ability versus flying speed (beingness highest at slow and fast speeds, with a minimum at an intermediate flight speed), the absolute magnitude of the power cost for flapping flight across species and speeds remains uncertain. Arguments for i approach and/or method being superior to another remain unconvincing. This is due to assumptions and simplifications that quasi-steady aerodynamic theory makes to guess flight ability requirements, and uncertainties in the scale of pectoralis force and assessment of regional fascicle strain profiles from localized fascicle recordings on the experimental side. More recent attempts to approximate muscle power output based on isolated work-loop muscle measurements in relation to EMG recordings made during flight [28,29] also have their limitations. These include estimating musculus recruitment from relative EMG magnitude across flight speeds to adjust the maximally stimulated muscle power measurements derived from in vitro work experiments. Such an approach necessarily determines the alter in flight power requirements based on changes in recorded EMG intensity. Information technology as well results in lower estimates of flight muscle power requirements of cockatiels (minimum power cost = approx. forty W kg−ane at 7 m southward−1) compared with those (74–79 W kg−ane at 5–7 g southward−1) obtained using DPC-based strength measurements [27,33]. Additional studies that refine the use of these approaches, or employ other methods [47], will improve our ability to quantify the absolute ability costs of flapping flight for particular species operating across various flight conditions. Consistent with the in vitro musculus work and EMG intensity results that ascribe change in muscle power output across flight speed owing to changes in EMG intensity [28,29], results based on in vivo fascicle strain, EMG and DPC-strain-calibrated force recordings [27,33] also showed EMG intensity to be highly correlated with muscle strength (R 2 = 0.92). In the latter studies, changes in EMG intensity accounted for 65 per cent of the modulation of muscle power, with changes in fascicle strain amplitude accounting for 25 per cent and changes in wingbeat frequency only 10 per cent of the modulation in muscle power [27,33].
Using measurements of DPC-strain-calibrated pectoralis forcefulness and fascicle strain to determine in vivo pectoralis power output, the comparative power curves for the unlike species studied to date propose that wing loading, as well equally wing and tail shape, is probably an of import determinant of a species' relative muscle ability cost. Doves accept the highest wing loading (36 N m−2) of the species studied to date [2] and correspondingly have the highest relative flying power toll over a broad range of speeds (figure 5). Magpies have the lowest aspect ratio wings (5.0; versus budgerigars: seven.iii, cockatiels: 7.0 and doves: 5.vii) and rounded wingtips, which probably helps to lower their muscle mass-specific power requirements merely may also limit the fastest speeds they can attain.
Now, it would be imprudent to place heavy reliance on the accuracy of experimental or theoretical modelling results to specify precisely whether a species has a minimum power cost at a detail flight speed, given the dubiety and limitations to the resolution and accurateness of currently available approaches used to estimate flight power costs. For example, whereas oxygen consumption data for cockatiels [48,49] bespeak a minimum metabolic ability cost at 10 m s−one, measurements of pectoralis muscle power data suggest a minimum in the range of 5–7 m s−1 [27,29]. Combining the metabolic ability results for cockatiels with their mechanical muscle power results [49] indicates that muscle efficiency increases with flying speed, ranging from vi.nine to eleven.ii per cent based on the muscle ability information of Morris & Askew [29], or from 12.two to 28.3 per cent based on the DPC-pectoralis force and fascicle strain recordings of Tobalske et al. [27].
Differences in muscle efficiency are likely given that the shortening velocity of the pectoralis musculus fascicles varies with flight speed. For cockatiels [27,33], fascicle shortening velocities ranged from 5.xix to 6.73 muscle lengths per 2nd across flight speeds from 1 to 13 m s−1. The range of efficiencies derived from in vitro musculus measurements adjusted for EMG intensity [29] are low compared with those expected for vertebrate skeletal muscle, which range from 20 to 28 per cent at optimal shortening velocities [50]. Information technology seems surprising that the evolution of flight musculus function in cockatiels and other birds would be constrained to substantially lower efficiencies. Although wingbeat frequency varies only slightly beyond flight speeds (10% in cockatiels), the magnitude of pectoralis fascicle strain changes in a shallow U-shaped blueprint, paralleling changes in pectoralis force [29], which results in the overall muscle power versus speed human relationship that is observed for cockatiels (figure v). Although fascicle strain charge per unit varies with flight speed, the generally compatible contractile properties of the pectoralis across a range of flight speeds [27,29] (figure 3) reverberate the strikingly uniform fibre-type characteristics of the avian pectoralis [21–23]. This is in dissimilarity to the much larger change in fascicle shortening velocity with running speed that occurs in the leg muscles of terrestrial animals [51–54].
vi. Muscle function in relation to the control of take-off, landing and manoeuvring flying
Whereas the pectoralis and supracoracoideus are mainly responsible for producing the mechanical power required for sustained flapping flight in birds, it is unclear whether the activity of these large flight muscles is modulated to achieve manoeuvring flight behaviours, or whether the smaller wing extrinsic and intrinsic muscles are recruited to arrange wing orientation and wing shape. By piece of work based on three-dimensional kinematics, muscle forcefulness and EMG recordings suggest two possibilities. In pigeons [6,55], left and correct pectoralis muscles appear to exhibit differential timing of force development and magnitude, with downstroke of the exterior wing phase advanced relative to the inside fly of a turn. In rose-breasted galahs [5], little difference in the kinematic timing of downstroke or pectoralis EMG activity was noted during 90° turns. Instead, there was show of differential activation of the left and right biceps muscles, with the inside biceps showing stronger action, indicative of increased elbow flexion and reduction of inside wing span. In both sets of studies, however, more than detailed kinematics of wing shape and motion during these manoeuvres was not available given the limited resolution of the motion-analysis systems used at the fourth dimension. Hereafter work will benefit from improved kinematic resolution during turning flying, combined with farther study of left fly versus right wing muscle contractile asymmetry.
In studies of pigeons taking-off from an elevated perch platform, flying level and landing on a similar perch, measurements of wing, trunk and tail kinematics reveal little change in fly or tail movements relative to the bird's trunk [56]. Instead, near of the changes in global orientations of the tail, fly and wing stroke airplane, which determine the aerodynamic properties of the bird's flight stroke, are achieved by changes in body pitch (figure 6 a). During take-off, pigeons pitch frontward (head down) inclining their stroke plane to a more vertical orientation to provide increased thrust for acceleration after the take-off jump from the perch. During landing, the dove pitches dorsum (head up), changing its stroke plane to a more horizontal orientation to aid decelerate equally it lands. Changes in the global stroke plane angle during take-off and landing are significantly greater and less, respectively, than observed during level flight.
(a) Changes in wing stroke airplane (SPAloc) and trunk pitch angle (in global infinite) of a dove during successive wingbeats of take-off, mid-level flight and landing (adapted from Berg & Biewener [56]). The strong correlation of wing stroke plane bending versus torso angle is shown to the right. Filled triangles, body angles; filled squares, SPAloc. (b) Representative in vivo recordings of muscle strain and activation (EMG) of extrinsic and intrinsic wing muscles of a dove during take-off, level (approx. 4.5 m s−1) and landing flight corresponding to a similar sequence shown in (a) above (adapted from Berg [57]).
The uniform motion of the pigeon's wings relative to its body during accept-off, level and landing flight suggests that the control of fly and trunk movement beyond these key phases of flight relies on subtle shifts in aerodynamic and inertial forces produced by the tail and wings relative to the torso to control body pitch. The pitch moment of inertia of a bird, though greater than its roll moment of inertia, is all the same quite small-scale. Equally a result, slight shifts in the orientation of net aerodynamic force produce the observed pitch acceleration. In pigeons, the shift in the management of cyberspace aerodynamic force need simply be approximately viii mm relative to its centre of mass to produce the observed pitch moment [56]. Consequent with this, no meaning differences were observed in the neuromuscular activation (EMG) or contractile strain behaviour of the wing muscles examined (figure 6 b) [57]. This result suggests that the control of body orientation and fly movement relative to the trunk does not require substantial changes in flying muscle activation and contractile part. Instead, the highly manoeuvrable bodies of many birds (low pitch, roll and yaw moments of inertia) enable them to achieve changes in trunk and wing orientation that allow rapid sharp turning, or to shift from take-off to landing flying, with subtle changes in neuromuscular function that are likely to bear witness challenging to identify.
seven. Discussion and summary
Muscle function in bird flying depends on the production of substantial mechanical work performed at a high rate. Although skeletal muscles generally have a similar capacity for generating mass-specific work, the avian pectoralis is well suited to performing work with large length excursions. This is a prerequisite for powering flying considering the wings must motion through a large circuit during downstroke to produce effective aerodynamic elevator. The pectoralis achieves this by having relatively long fascicles that shorten over a large fraction (up to 42%) of their length. The timing of muscle activation late in upstroke also allows the pectoralis to rapidly develop forcefulness nether near isometric or stretching weather. This elevates the work that the muscle performs equally it shortens (figure 3).
Considering of its large size and principal part in producing aerodynamic lift, the contractile function of the avian pectoralis provides a valuable index for the power requirements of flight based on measurements of its force production, contractile strain and neuromuscular activation. This is in contrast to the multiple musculus groups in the limbs of running animals that contribute to muscle power for motility. Nevertheless, a functional examination of the broader suite of wing muscles is needed in lodge to understand how flight movements, particularly those during manoeuvring, are controlled. Although much smaller wing muscles may not contribute significantly to the mechanical power underlying flight, by adjusting the orientation and shape of the wing, they can alter the fly'southward aerodynamic properties and, thus, influence how aerodynamic forces and power are shifted between the wings for manoeuvring.
An unexpected outcome is that shifts in body, tail and wing movement during accept-off, level and landing flight of pigeons are achieved mainly by changes in whole-body pitch, rather than by changes in fly or tail motility relative to the body itself. The degree to which turning flight is achieved past left versus right asymmetries of smaller fly muscles, acting to 'steer' the bird effectually a turn, as opposed to modulation of the larger power-producing pectoralis and/or supracoracoideus muscles remains unclear. Evidence exists that both sets of muscles may contribute to the necessary aerodynamic asymmetries that effect in a turning manoeuvre. The low moments of inertia and highly manoeuvrable bodies of birds mean that left versus right asymmetries in turning flying, or fore-aft asymmetries in aerodynamic forcefulness production during take-off and landing flight, are likely to exist pocket-size and challenging to identify.
Future studies will do good from improved imaging that will allow detailed changes in wing shape, orientation and move to be quantified and related to the timing and magnitude of muscle activation, and where possible, changes in muscle length, strength and work. These measurements go increasingly difficult for smaller muscles, located more than distally in the wing. Force measurements, in item, are hard to obtain for near muscles, hampering the ability to assess muscle forcefulness and piece of work output in relation to manoeuvring flight. In the case where muscles are too small, or forces cannot exist recorded straight, in vitro or in situ measurements of muscle strength [29] tin can play an important role for assessing the muscle'due south contractile properties and role(southward) in flight. The remarkable ability of birds to fly over a range of speeds while ofttimes manoeuvring through circuitous environments makes understanding the neuromuscular and aerodynamic features of these flight behaviours of considerable interest to physiologists, biomechanists and aeronautical engineers.
Similarly, the aerodynamic and metabolic power requirements for flight are of considerable involvement to avian and evolutionary ecologists interested in the strategies that birds employ to forage and drift to ensure a successful life history. For this reason, boosted gratuitous flight data on bird metabolism, characteristic flying speeds and behaviour need to exist linked to additional experimental assessments of flying energy metabolism and musculoskeletal office. While quasi-static aerodynamic models tin can provide a rough estimate of flight costs, the importance of not-steady aerodynamic effects on flight ability costs is now well recognized and cannot exist ignored. Thus, additional modelling and experimental studies that seek to yield improved measurements of muscle function and aerodynamic power output are needed.
Acknowledgements
The author cheers his many past students, postdocs and collaborators for the fun and exciting piece of work shared to understand bird musculus function in relation to flight performance. He besides thanks Mr Pedro Ramirez for his expert and devoted help in caring for the birds. Much of the writer'due south work has been funded by the National Science Foundation, nigh recently past IOS-0744056.
Footnotes
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