Comparative hindlimb myology of foot-propelled swimming birds.

Several groups of birds have convergently evolved the ability to swim using their feet despite facing trade-offs with walking. However, swimming relative to terrestrial performance varies across these groups. Highly specialized divers, such as loons and grebes, excel at swimming underwater but struggle to stand on land, whereas species that primarily swim on the water surface, such as Mallards, retain the ability to move terrestrially. The identification of skeletal features associated with a swimming style and conserved across independent groups suggests that the hindlimb of foot-propelled swimming birds has adapted to suit the physical challenges of producing propulsive forces underwater. But in addition to skeletal features, how do hindlimb muscles reflect swimming ability and mode? This paper presents the first comparative myology analysis associated with foot-based swimming. Our detailed dissections of 35 specimens representing eight species reveal trends in hindlimb muscle size and attachment location across four independent lineages of extant swimming birds. We expand upon our dissections by compiling data from historical texts and provide a key to any outdated muscle nomenclature used in these sources. Our results show that highly diving birds tuck the femur and proximal tibiotarsus next to the ribcage and under the skin covering the abdomen, streamlining the body. Several hindlimb muscles exhibit dramatic anatomical variation in diving birds, including the flexor cruris lateralis (FCL) and iliofibularis (IF), which reduce in size and shift distally along the tibiotarsus. The femorotibialis medius (FTM) extends along an expanded cnemial crest. The resulting increased moment arms of these muscles likely help stabilize the hip and knee while paddling. Additionally, distal ankle plantarflexors, including the gastrocnemius and digital flexors, are exceptionally large in diving birds in order to power foot propulsion. These patterns exist within distantly related lineages of diving birds and, to a lesser extent, in surface swimmers. Together, our findings verify conserved muscular adaptations to a foot-propelled swimming lifestyle. The association of muscle anatomy with skeletal features and biomechanical movement demands can inform functional interpretation of fossil birds and reveal selective pressures underlying avian diversification.

Differential segmental strain during active lengthening in a large biarticular thigh muscle during running.

The iliotibialis lateralis pars postacetabularis (ILPO) is the largest muscle in the hindlimb of the guinea fowl and is thought to play an important role during the stance phase of running, both absorbing and producing work. Using sonomicrometry and electromyography, we examined whether the ILPO experiences differential strain between proximal, central and distal portions of the posterior fascicles. When the ILPO is being lengthened while active, the distal portion was found to lengthen significantly more than either the proximal or central portions of the muscle. Our data support the hypothesis that the distal segment lengthened farther and faster because it began activity at shorter sarcomere lengths on the ascending limb of the length-tension curve. Probably because of the self-stabilizing effects of operating on the ascending limb of the length-tension curve, all segments reached the end of lengthening and started shortening at the same sarcomere length. During shortening, this similarity in sarcomere length among the segments was maintained, as predicted from force-velocity effects, and shortening strain was similar in all segments. The differential active strain during active lengthening is thus ultimately determined by differences in strain during the passive portion of the cycle. The sarcomere lengths of all segments of the fascicles were similar at the end of active shortening, but after the passive portion of the cycle the distal segment was shorter. Differential strain in the segments during the passive portion of the cycle may be caused by differential joint excursions at the knee and hip acting on the ends of the muscle and being transmitted differentially by the passive visco-elastic properties of the muscle. Alternatively, the differential passive strain could be due to the action of active or passive muscles in the thigh that transmit force to the IPLO in shear. Based on basic sarcomere dynamics we predict that differential strain is more likely to occur in muscles undergoing active lengthening at the beginning of contraction than those undergoing only shortening.

Mechanisms producing coordinated function across the breadth of a large biarticular thigh muscle.

We examined the hypothesis that structural features of the iliotibialis lateralis pars postacetabularis (ILPO) in guinea fowl allow this large muscle to maintain equivalent function along its anterior-posterior axis. The ILPO, the largest muscle in the hindlimb of the guinea fowl, is a hip and knee extensor. The fascicles of the ILPO originate across a broad region of the ilium and ischium posterior to the hip. Its long posterior fascicles span the length of the thigh and insert directly on the patellar tendon complex. However, its anterior fascicles are shorter and insert on a narrow aponeurosis that forms a tendinous band along the anterior edge of the muscle and is connected distally to the patellar tendon. The biarticular ILPO is actively lengthened and then actively shortened during stance. The moment arm of the fascicles at the hip increases along the anterior to posterior axis, whereas the moment arm at the knee is constant for all fascicles. Using electromyography and sonomicrometry, we examined the activity and strain of posterior and anterior fascicles of the ILPO. The activation was not significantly different in the anterior and posterior fascicles. Although we found significant differences in active lengthening and shortening strain between the anterior and posterior fascicles, the differences were small. The majority of shortening strain is caused by hip extension and the inverse relationship between hip moment arm and fascicle length along the anterior-posterior axis was found to have a major role in ensuring similar shortening strain. However, because the knee moment arm is the same for all fascicles, knee flexion in early stance was predicted to produce much larger lengthening strains in the short anterior fascicles than our measured values at this location. We propose that active lengthening of the anterior fascicles was lower than predicted because the aponeurotic tendon of insertion of the anterior fascicles was stretched and only a portion of the lengthening had to be accommodated by the active muscle fascicles.

Function of a large biarticular hip and knee extensor during walking and running in guinea fowl (Numida meleagris).

Physiological and anatomical evidence suggests that in birds the iliotibialis lateralis pars postacetabularis (ILPO) is functionally important for running. Incorporating regional information, we estimated the mean sarcomere strain trajectory and electromyographic (EMG) amplitude of the ILPO during level and incline walking and running. Using these data and data in the literature of muscle energy use, we examined three hypotheses: (1) active lengthening will occur on the ascending limb of the length-tension curve to avoid potential damage caused by stretch on the descending limb; (2) the active strain cycle will shift to favor active shortening when the birds run uphill and shortening will occur on the plateau and shallow ascending limb of the length-tension curve; and (3) measures of EMG intensity will correlate with energy use when the mechanical function of the muscle is similar. Supporting the first hypothesis, we found that the mean sarcomere lengths at the end of active lengthening during level locomotion were smaller than the predicted length at the start of the plateau of the length-tension curve. Supporting the second hypothesis, the magnitude of active lengthening decreased with increasing slope, whereas active shortening increased. In evaluating the relationship between EMG amplitude and energy use (hypothesis 3), we found that although increases in EMG intensity with speed, slope and loading were positively correlated with muscle energy use, the quantitative relationships between these variables differed greatly under different conditions. The relative changes in EMG intensity and energy use by the muscle probably varied because of changes in the mechanical function of the muscle that altered the ratio of muscle energy use to active muscle volume. Considering the overall function of the cycle of active lengthening and shortening of the fascicles of the ILPO, we conclude that the function of active lengthening is unlikely to be energy conservation and may instead be related to promoting stability at the knee. The work required to lengthen the ILPO during stance is provided by co-contracting knee flexors. We suggest that this potentially energetically expensive co-contraction serves to stabilize the knee in early stance by increasing the mechanical impedance of the joint.

Body stiffness and damping depend sensitively on the timing of muscle activation in lampreys.

Unlike most manmade machines, animals move through their world using flexible bodies and appendages, which bend due to internal muscle and body forces, and also due to forces from the environment. Fishes in particular must cope with fluid dynamic forces that not only resist their overall swimming movements but also may have unsteady flow patterns, vortices, and turbulence, many of which occur more rapidly than what the nervous system can process. Has natural selection led to mechanical properties of fish bodies and their component tissues that can respond very quickly to environmental perturbations? Here, we focus on the mechanical properties of isolated muscle tissue and of the entire intact body in the silver lamprey, Ichthyomyzon unicuspis. We developed two modified work loop protocols to determine the effect of small perturbations on the whole body and on isolated segments of muscle as a function of muscle activation and phase within the swimming cycle. First, we examined how the mechanical properties of the whole lamprey body change depending on the timing of muscle activity. Relative to passive muscle, muscle activation can modulate the effective stiffness by about two-fold and modulate the effective damping by >10-fold depending on the activation phase. Next, we performed a standard work loop test on small sections of axial musculature while adding low-amplitude sinusoidal perturbations at specific frequencies. We modeled the data using a new system identification technique based on time-periodic system analysis and harmonic transfer functions (HTFs) and used the resulting models to predict muscle function under novel conditions. We found that the effective stiffness and damping of muscle varies during the swimming cycle, and that the timing of activation can alter both the magnitude and timing of peak stiffness and damping. Moreover, the response of the isolated muscle was highly nonlinear and length dependent, but the body's response was much more linear. We applied the resulting HTFs from our experiments to explore the effect of pairs of antagonistic muscles. The results suggest that when muscles work against each other as antagonists, the combined system has weaker nonlinearities than either muscle segment alone. Together, these results begin to provide an integrative understanding of how activation timing can tune the mechanical response properties of muscles, enabling fish to swim effectively in their complex and unpredictable environment.

Blood flow in guinea fowl Numida meleagris as an indicator of energy expenditure by individual muscles during walking and running.

Running and walking are mechanically complex activities. Leg muscles must exert forces to support weight and provide stability, do work to accelerate the limbs and body centre of mass, and absorb work to act as brakes. Current understanding of energy use during legged locomotion has been limited by the lack of measurements of energy use by individual muscles. Our study is based on the correlation between blood flow and aerobic energy expenditure in active skeletal muscle during locomotion. This correlation is strongly supported by the available evidence concerning control of blood flow to active muscle, and the relationship between blood flow and the rate of muscle oxygen consumption. We used injectable microspheres to measure the blood flow to the hind-limb muscles, and other body tissues, in guinea fowl (Numida meleagris) at rest, and across a range of walking and running speeds. Combined with data concerning the various mechanical functions of the leg muscles, this approach has enabled the first direct estimates of the energetic costs of some of these functions. Cardiac output increased from 350 ml min(-1) at rest, to 1700 ml min(-1) at a running speed ( approximately 2.6 m s(-1)) eliciting a of 90% of . The increase in cardiac output was achieved via approximately equal factorial increases in heart rate and stroke volume. Approximately 90% of the increased cardiac output was directed to the active muscles of the hind limbs, without redistribution of blood flow from the viscera. Values of mass-specific blood flow to the ventricles, approximately 15 ml min(-1) g(-1), and one of the hind-limb muscles, approximately 9 ml min(-1) g(-1), were the highest yet recorded for blood flow to active muscle. The patterns of increasing blood flow with increasing speed varied greatly among different muscles. The increases in flow correlated with the likely fibre type distribution of the muscles. Muscles expected to have many high-oxidative fibres preferentially increased flow at low exercise intensities. We estimated substantial energetic costs associated with swinging the limbs, co-contraction to stabilize the knee and work production by the hind-limb muscles. Our data provide a basis for evaluating hypotheses relating the mechanics and energetics of legged locomotion.

Partitioning the energetics of walking and running: swinging the limbs is expensive.

Explaining the energetics of walking and running has been difficult because the distribution of energy use among individual muscles has not been known. We estimated energy use by measuring blood flow to the hindlimb muscles in guinea fowl. Blood flow to skeletal muscles is controlled locally and varies directly with metabolic rate. We estimate that the swing-phase muscles consume 26% of the energy used by the limbs and the stance-phase muscles consume the remaining 74%, independent of speed. Thus, contrary to some previous suggestions, swinging the limbs requires an appreciable fraction of the energy used during terrestrial legged locomotion. Models integrating the energetics and mechanics of running will benefit from more detailed information on the distribution of energy use by the muscles.