Observation of Mammalian Similarity Through Allometric Scaling Laws

We discuss the problem of observation of natural similarity in skeletal evolution of terrestrial mammals. Analysis is given by means of testing of the power scaling laws established in long bone allometry, which describe development of bones (of length $L$ and diameter $D$) with body mass in terms of the growth exponents, \QTR{it}{e.g.} $\lambda =d\log L/d\log D$. The bone-size evolution scenario given three decades ago by McMahon was quiet explicit on the geometrical-shape and mechanical-force constraints that predicted $\lambda =2/3$. This remains too far from the mammalian allometric exponent $\lambda ^{(\exp)}=0.80\pm 0.2$, recently revised by Christiansen, that is a chief puzzle in long bone allometry. We give therefore new insights into McMahon's constraints and report on the first observation of the critical-elastic-force, bending-deformation, muscle-induced mechanism that underlies the allometric law with estimated $\lambda =0.80\pm 0.3$. This mechanism governs the bone-size evolution with avoiding skeletal fracture caused by muscle-induced peak stresses and is expected to be unique for small and large mammals.Comment: Keywords: allometric scaling, long bones, muscles, mammals 21 pages, 1 Table, 2 Figure

Dynamics of leg muscle function in tammar wallabies (M. eugenii) during level versus incline hopping

The goal of our study was to examine whether the in vivo force-length behavior, work and elastic energy savings of distal muscle-tendon units in the legs of tammar wallabies (Macropus eugenii) change during level versus incline hopping. To address this question, we obtained measurements of muscle activation (via electromyography), fascicle strain (via sonomicrometry) and muscle-tendon force (via tendon buckles) from the lateral gastrocnemius (LG) and plantaris (PL) muscles of tammar wallabies trained to hop on a level and an inclined (10°, 17.4% grade) treadmill at two speeds (3.3 m s^(-1) and 4.2 m s^(-1)). Similar patterns of muscle activation, force and fascicle strain were observed under both level and incline conditions. This also corresponded to similar patterns of limb timing and movement (duty factor, limb contact time and hopping frequency). During both level and incline hopping, the LG and PL exhibited patterns of fascicle stretch and shortening that yielded low levels of net fascicle strain [LG: level, -1.0±4.6% (mean ± s.e.m.) vs incline, 0.6±4.5%; PL: level, 0.1±1.0% vs incline, 0.4±1.6%] and muscle work (LG: level, -8.4±8.4 J kg^(-1) muscle vs incline, -6.8±7.5 J kg^(-1) muscle; PL: level, -2.0±0.6 J kg^(-1) muscle vs incline, -1.4±0.7 J kg^(-1) muscle). Consequently, neither muscle significantly altered its contractile dynamics to do more work during incline hopping. Whereas electromyographic (EMG) phase, duration and intensity did not differ for the LG, the PL exhibited shorter but more intense periods of activation, together with reduced EMG phase (P<0.01), during incline versus level hopping. Our results indicate that design for spring-like tendon energy savings and economical muscle force generation is key for these two distal muscle-tendon units of the tammar wallaby, and the need to accommodate changes in work associated with level versus incline locomotion is achieved by more proximal muscles of the limb

Gearing effects of the patella (knee extensor muscle sesamoid) of the helmeted guineafowl during terrestrial locomotion

Human patellae (kneecaps) are thought to act as gears, altering the mechanical advantage of knee extensor muscles during running. Similar sesamoids have evolved in the knee extensor tendon independently in birds, but it is unknown if these also affect the mechanical advantage of knee extensors. Here, we examine the mechanics of the patellofemoral joint in the helmeted guineafowl Numida meleagris using a method based on muscle and tendon moment arms taken about the patella's rotation centre around the distal femur. Moment arms were estimated from a computer model representing hindlimb anatomy, using hip, knee and patellar kinematics acquired via marker‐based biplanar fluoroscopy from a subject running at 1.6 ms−1 on a treadmill. Our results support the inference that the patella of Numida does alter knee extensor leverage during running, but with a mechanical advantage generally greater than that seen in humans, implying relatively greater extension force but relatively lesser extension velocity

Optic flow stabilizes flight in ruby-throated hummingbirds

Flying birds rely on visual cues for retinal image stabilization by negating rotation-induced optic flow, the motion of the visual panorama across the retina, through corrective eye and head movements. In combination with vestibular and proprioceptive feedback, birds may also use visual cues to stabilize their body during flight. Here, we test whether artificially induced wide-field motion generated through projected visual patterns elicits maneuvers in body orientation and flight position, in addition to stabilizing vision. To test this hypothesis, we present hummingbirds flying freely within a 1.2 m cylindrical visual arena with a virtual surround rotated at different speeds about its vertical axis. The birds responded robustly to these visual perturbations by rotating their heads and bodies with the moving visual surround, and by adjusting their flight trajectories, following the surround. Thus, similar to insects, hummingbirds appear to use optic flow cues to control flight maneuvers as well as to stabilize their visual inputs

Fatigue Alters in Vivo Function Within and Between Limb Muscles During Locomotion

Muscle fatigue, a reduction in force as a consequence of exercise, is an important factor for any animal that moves, and can result from both peripheral and/or central mechanisms. Although much is known about whole-limb force generation and activation patterns in fatigued muscles under sustained isometric contractions, little is known about the in vivo dynamics of limb muscle function in relation to whole-body fatigue. Here we show that limb kinematics and contractile function in the lateral (LG) and medial (MG) gastrocnemius of helmeted guineafowl (Numida meleagris) are significantly altered following fatiguing exercise at 2 m sK1 on an inclined treadmill. The two most significant findings were that the variation in muscle force generation, measured directly from the muscles’ tendons, increased significantly with fatigue, and fascicle shortening in the proximal MG, but not the distal MG, decreased significantly with fatigue. We suggest that the former is a potential mechanism for decreased stability associated with fatigue. The region-specific alteration of fascicle behaviour within the MG as a result of fatigue suggests a complex response to fatigue that probably depends on muscle–aponeurosis and tendon architecture not previously explored. These findings highlight the importance of studying the integrative in vivo dynamics of muscle function in response to fatigue.Organismic and Evolutionary Biolog

Contractile properties of the pigeon supracoracoideus during different modes of flight

The supracoracoideus (SUPRA) is the primary upstroke muscle for avian flight and is the antagonist to the downstroke muscle, the pectoralis (PECT). We studied in vivo contractile properties and mechanical power output of both muscles during take-off, level and landing flight. We measured muscle length change and activation using sonomicrometry and electromyography, and muscle force development using strain recordings on the humerus. Our results support a hypothesis that the primary role of the SUPRA is to supinate the humerus. Antagonistic forces exerted by the SUPRA and PECT overlap during portions of the wingbeat cycle, thereby offering a potential mechanism for enhancing control of the wing. Among flight modes, muscle strain was approximately the same in the SUPRA (33–40%) and the PECT (35–42%), whereas peak muscle stress was higher in the SUPRA $(85–126 N m^{–2})$ than in the PECT $(50–58 N m^{–2})$. The SUPRA mainly shortened relative to resting length and the PECT mainly lengthened. We estimated that elastic energy storage in the tendon of the SUPRA contributed between 28 and 60% of the net work of the SUPRA and 6–10% of the total net mechanical work of both muscles. Mechanical power output in the SUPRA was congruent with the estimated inertial power required for upstroke, but power output from the PECT was only 42–46% of the estimated aerodynamic power requirements for flight. There was a significant effect of flight mode upon aspects of the contractile behavior of both muscles including strain, strain rate, peak stress, work and power.Organismic and Evolutionary BiologyOther Research Uni

Wing and Body Kinematics of Takeoff and Landing Flight in the Pigeon (Columba livia)

Takeoff and landing are critical phases in a flight. To better understand the functional importance of the kinematic adjustments birds use to execute these flight modes, we studied the wing and body movements of pigeons (Columba livia) during short-distance free-flights between two perches. The greatest accelerations were observed during the second wingbeat of takeoff. The wings were responsible for the majority of acceleration during takeoff and landing, with the legs contributing only one-quarter of the acceleration. Parameters relating to aerodynamic power output such as downstroke amplitude, wingbeat frequency and downstroke velocity were all greatest during takeoff flight and decreased with each successive takeoff wingbeat. This pattern indicates that downstroke velocity must be greater for accelerating flight to increase the amount of air accelerated by the wings. Pigeons used multiple mechanisms to adjust thrust and drag to accelerate during takeoff and decelerate during landing. Body angle, tail angle and wing plane angles all shifted from more horizontal orientations during takeoff to near-vertical orientations during landing, thereby reducing drag during takeoff and increasing drag during landing. The stroke plane was tilted steeply downward throughout takeoff (increasing from −60±5 deg. to −47±1 deg.), supporting our hypothesis that a downward-tilted stroke plane pushes more air rearward to accelerate the bird forward. Similarly, the stroke plane tilted upward during landing (increasing from −1±2 deg. to 17±7 deg.), implying that an upward-tilted stroke plane pushes more air forward to slow the bird down. Rotations of the stroke plane, wing planes and tail were all strongly correlated with rotation of the body angle, suggesting that pigeons are able to redirect aerodynamic force and shift between flight modes through modulation of body angle alone.Organismic and Evolutionary BiologyOther Research Uni

Mechanics of limb bone loading during terrestrial locomotion in the green iguana (Iguana iguana) and American alligator (Alligator mississippiensis)

In vivo measurements of strain in the femur and tibia of Iguana iguana (Linnaeus) and Alligator mississippiensis (Daudin) have indicated three ways in which limb bone loading in these species differs from patterns observed in most birds and mammals: (i) the limb bones of I. iguana and A. mississippiensis experience substantial torsion, (ii) the limb bones of I. iguana and A. mississippiensis have higher safety factors than those of birds or mammals, and (iii) load magnitudes in the limb bones of A. mississippiensis do not decrease uniformly with the use of a more upright posture. To verify these patterns, and to evaluate the ground and muscle forces that produce them, we collected three-dimensional kinematic and ground reaction force data from subadult I. iguana and A. mississippiensis using a force platform and high-speed video. The results of these force/kinematic studies generally confirm the loading regimes inferred from in vivo strain measurements. The ground reaction force applies a torsional moment to the femur and tibia in both species; for the femur, this moment augments the moment applied by the caudofemoralis muscle, suggesting large torsional stresses. In most cases, safety factors in bending calculated from force/video data are lower than those determined from strain data, but are as high or higher than the safety factors of bird and mammal limb bones in bending. Finally, correlations between limb posture and calculated stress magnitudes in the femur of I. iguana confirm patterns observed during direct bone strain recordings from A. mississippiensis: in more upright steps, tensile stresses on the anterior cortex decrease, but peak compressive stresses on the dorsal cortex increase. Equilibrium analyses indicate that bone stress increases as posture becomes more upright in saurians because the ankle and knee extensor muscles exert greater forces during upright locomotion. If this pattern of increased bone stress with the use of a more upright posture is typical of taxa using non-parasagittal kinematics, then similar increases in load magnitudes were probably experienced by lineages that underwent evolutionary shifts to a non-sprawling posture. High limb bone safety factors and small body size in these lineages could have helped to accommodate such increases in limb bone stress

In vivo locomotor strain in the hind limb bones of Alligator mississipiensis and Iguana iguana: implications for the evolution of limb bone safety factor and non-sprawling limb posture.

Limb postures of terrestrial tetrapods span a continuum from sprawling to fully upright; however, most experimental investigations of locomotor mechanics have focused on mammals and ground-dwelling birds that employ parasagittal limb kinematics, leaving much of the diversity of tetrapod locomotor mechanics unexplored. This study reports measurements of in vivo locomotor strain from the limb bones of lizard (Iguana iguana) and crocodilian (Alligator mississippiensis) species, animals from previously unsampled phylogenetic lineages with non-parasagittal limb posture and kinematics. Principal strain orientations and shear strain magnitudes indicate that the limb bones of these species experience considerable torsion during locomotion. This contrasts with patterns commonly observed in mammals, but matches predictions from kinematic observations of axial rotation in lizard and crocodilian limbs. Comparisons of locomotor load magnitudes with the mechanical properties of limb bones in Alligator and Iguana indicate that limb bone safety factors in bending for these species range from 5.5 to 10.8, as much as twice as high as safety factors previously calculated for mammals and birds. Limb bone safety factors in shear (3.9-5.4) for Alligator and Iguana are also moderately higher than safety factors to yield in bending for birds and mammals. Finally, correlations between limb posture and strain magnitudes in Alligator show that at some recording locations limb bone strains can increase during upright locomotion, in contrast to expectations based on size-correlated changes in posture among mammals that limb bone strains should decrease with the use of an upright posture. These data suggest that, in some lineages, strain magnitudes may not have been maintained at constant levels through the evolution of a non-sprawling posture unless the postural change was accompanied by a shift to parasagittal kinematics or by an evolutionary decrease in body size

Muscle function during takeoff and landing flight in the pigeon (Columba livia)

This study explored the muscle strain and activation patterns of several key flight muscles of the pigeon (Columba livia) during takeoff and landing flight. Using electromyography (EMG) to measure muscle activation, and sonomicrometry to quantify muscle strain, we evaluated the muscle function patterns of the pectoralis, biceps, humerotriceps and scapulotriceps as pigeons flew between two perches. These recordings were analyzed in the context of three-dimensional wing kinematics. To understand the different requirements of takeoff, midflight and landing, we compared the activity and strain of these muscles among the three flight modes. The pectoralis and biceps exhibited greater fascicle strain rates during takeoff than during midflight or landing. However, the triceps muscles did not exhibit notable differences in strain among flight modes. All observed strain, activation and kinematics were consistent with hypothesized muscle functions. The biceps contracted to stabilize and flex the elbow during the downstroke. The humerotriceps contracted to extend the elbow at the upstroke-downstroke transition, followed by scapulotriceps contraction to maintain elbow extension during the downstroke. The scapulotriceps also appeared to contribute to humeral elevation. Greater muscle activation intensity was observed during takeoff, compared with mid-flight and landing, in all muscles except the scapulotriceps. The timing patterns of muscle activation and length change differed among flight modes, yet demonstrated that pigeons do not change the basic mechanical actions of key flight muscles as they shift from flight activities that demand energy production, such as takeoff and midflight, to maneuvers that require absorption of energy, such as landing. Similarly, joint kinematics were consistent among flight modes. The stereotypy of these neuromuscular and joint kinematic patterns is consistent with previously observed stereotypy of wing kinematics relative to the pigeon's body (in the local body frame) across these flight behaviors. Taken together, these observations suggest that the control of takeoff and landing flight primarily involves modulation of overall body pitch to effect changes in stroke plane angle and resulting wing aerodynamics.Organismic and Evolutionary Biolog