Impact Protection Potential of Mammalian Hair: Testing the Pugilism Hypothesis for the Evolution of Human Facial Hair.

Because facial hair is one of the most sexually dimorphic features of humans (Homo sapiens) and is often perceived as an indicator of masculinity and social dominance, human facial hair has been suggested to play a role in male contest competition. Some authors have proposed that the beard may function similar to the long hair of a lion's mane, serving to protect vital areas like the throat and jaw from lethal attacks. This is consistent with the observation that the mandible, which is superficially covered by the beard, is one of the most commonly fractured facial bones in interpersonal violence. We hypothesized that beards protect the skin and bones of the face when human males fight by absorbing and dispersing the energy of a blunt impact. We tested this hypothesis by measuring impact force and energy absorbed by a fiber epoxy composite, which served as a bone analog, when it was covered with skin that had thick hair (referred to here as "furred") versus skin with no hair (referred to here as "sheared" and "plucked"). We covered the epoxy composite with segments of skin dissected from domestic sheep (Ovis aries), and used a drop weight impact tester affixed with a load cell to collect force versus time data. Tissue samples were prepared in three conditions: furred (n = 20), plucked (n = 20), and sheared (n = 20). We found that fully furred samples were capable of absorbing more energy than plucked and sheared samples. For example, peak force was 16% greater and total energy absorbed was 37% greater in the furred compared to the plucked samples. These differences were due in part to a longer time frame of force delivery in the furred samples. These data support the hypothesis that human beards protect vulnerable regions of the facial skeleton from damaging strikes.

The influence of foot posture on the cost of transport in humans.

Although humans appear to be specialized for endurance running, the plantigrade posture of our feet, in which the heel contacts the substrate at the beginning of a step, seems incompatible with economical running. In this study, we tested the hypothesis that plantigrade foot posture reduces the energetic cost of transport (COT) during walking in humans. When human subjects walked with their heels slightly elevated in a 'low-digitigrade' posture, COT increased by 53% above that of normal plantigrade walking. By contrast, there was no difference in COT when subjects ran with digitigrade versus plantigrade foot posture. Stride frequency increased and stride length decreased when subjects switched to digitigrade walking; however, this change did not influence the COT. Additionally, we found that possible reductions in postural stability appear not to have caused the elevated cost of digitigrade walking. Digitigrade walking, however, did (1) increase the external mechanical work performed by the limbs; (2) reduce the pendular exchange of kinetic and potential energy of the center of mass; (3) increase the average ground reaction force moment at the ankle joint; and (4) increase the recruitment of major extensor muscles of the ankle, knee, hip and back. These observations suggest that plantigrade foot posture improves the economy of walking. Relative to other mammals, humans are economical walkers, but not economical runners. Given the great distances hunter-gatherers travel, it is not surprising that humans retained a foot posture, inherited from our more arboreal great ape ancestors, that facilitates economical walking.

Functional trade-offs in the limb bones of dogs selected for running versus fighting.

The physical demands of rapid and economical running differ from the demands of fighting in ways that may prevent the simultaneous evolution of optimal performance in these two behaviors. Here, we test an hypothesis of functional trade-off in limb bones by measuring mechanical properties of limb bones in two breeds of domestic dog (Canis lupus familiaris L.) that have undergone intense artificial selection for running (greyhound) and fighting (pit bull) performance. The bones were loaded to fracture in three-point static bending. To correct for the effect of shear, we estimated the shear stress in the cross section and added energy due to shear stress to the tensile energy. The proximal limb bones of the pit bulls differed from those of the greyhounds in having relatively larger second moments of area of mid-diaphyseal cross sections and in having more circular cross-sectional shape. The pit bulls exhibited lower stresses at yield, had lower elastic moduli and failed at much higher levels of work. The stiffness of the tissue of the humerus, radius, femur and tibia was 1.5-2.4-fold greater in the greyhounds than in the pit bulls. These bones from the pit bulls absorbed 1.9-2.6-fold more energy before failure than did those of the greyhounds. These differences between breeds were not observed in the long bones of the feet, metacarpals and metatarsals. Nevertheless, the results of this analysis suggest that selection for high-speed running is associated with the evolution of relatively stiff, brittle limb bones, whereas selection for fighting performance leads to the evolution of limb bones with relatively high resistance to failure.

Activity of three muscles associated with the uncinate processes of the giant Canada goose Branta canadensis maximus.

The activity of three muscles associated with the uncinate processes, (i) external intercostal, (ii) appendicocostalis and (iii) external oblique, were examined using patch and sew-through electrodes during sitting, standing and moderate speed treadmill running in the giant Canada goose. The external intercostal muscles demonstrated no respiratory activity, being active only during running, suggesting they play some role in trunk stabilisation. The appendicocostalis and external oblique muscles are respiratory muscles, being active during inspiration and expiration, respectively. The activity of the appendicocostalis muscles increased during sitting, suggesting that the uncinate processes in birds play an important role in facilitating lateral flaring of the rib cage when sternal rocking is prevented. We suggest that the uncinate processes in birds facilitate movements of the ribs and sternum during breathing and therefore are integral to the breathing mechanics of birds.

Functional trade-offs in the limb muscles of dogs selected for running vs. fighting.

The physical demands of rapid and economical running differ from those of physical fighting such that functional trade-offs may prevent simultaneous evolution of optimal performance in both behaviours. Here we test three hypotheses of functional trade-off by measuring determinants of limb musculoskeletal function in two breeds of domestic dogs that have undergone intense artificial selection for running (Greyhound) or fighting performance (Pit Bull). We found that Greyhounds differ from Pit Bulls in having relatively less muscle mass distally in their limbs, weaker muscles in their forelimbs than their hindlimbs, and a much greater capacity for elastic storage in the in-series tendons of the extensor muscles of their ankle joints. These observations are consistent with the hypothesis that specialization for rapid or economical running can limit fighting performance and vice versa. We suggest that functional trade-offs that prevent simultaneous evolution of optimal performance in both locomotor and fighting abilities are widespread taxonomically.

Epaxial muscle function in trotting dogs.

One of the features that distinguish mammals from other groups of terrestrial vertebrates is the structure and relative size of their epaxial muscles. Yet we have only a superficial understanding of the role these muscles play in locomotion. To address their locomotor function, we recorded the electrical activity of the iliocostalis, longissimus dorsi and multifidus muscles of trotting dogs. Activity was monitored at both lumbar and thoracic sites. To develop and evaluate hypotheses of epaxial muscle function, we quantified footfall patterns and sagittal trunk kinematics from high-speed videos, and the magnitude and orientation of ground reaction forces from force-plate recordings. All three epaxial muscles tended to exhibit a double-bursting (biphasic) activity pattern, with the exception of the iliocostalis muscle at the thoracic site (which was uniphasic). In general, a large burst of activity in each muscle occurred during the second half of the support phase of the ipsilateral hindlimb, and was active for an average of 30% of the locomotor cycle. A smaller burst of activity occurred during the second half of the support phase of the contralateral hindlimb, and was active for an average of 15% of the locomotor cycle. Analysis of ground reaction forces and sagittal trunk kinematics led us to the hypothesis that the epaxial muscles do not directly stabilize the trunk against the vertical and horizontal components of the ground reaction force. Instead, the epaxial muscles appear to counteract the tendency of the trunk to rebound (flex) in the sagittal plane during the latter half of the support phase. This hypothesis of epaxial muscle function was supported by loading experiments performed on the longissimus dorsi muscle in the lumbar region.

Function of the oblique hypaxial muscles in trotting dogs.

In trotting dogs, the pattern of activity of the obliquely oriented hypaxial muscles is consistent with the possible functions of (i) stabilization against vertical accelerations that cause the trunk to sag in the sagittal plane and (ii) stabilization against forces that tend to shear the trunk in the sagittal plane. To test these hypotheses, we compared the amount of activity of the intercostal and abdominal oblique muscles (i) when dogs carried additional mass (8-15% of body mass) supported over the limb girdles versus supported mid-trunk (test of sagittal bounce), and (ii) when dogs trotted up versus down a 10 degrees slope (test of sagittal shear). In response to the loading manipulations, only the internal oblique muscle responded in a manner that was consistent with stabilization of the trunk against forces that cause the trunk to sag sagittally. In contrast, when the fore-aft forces were manipulated by running up- and downhill, all four of the monitored muscles changed their activity in a manner consistent with stabilization of the trunk against sagittal shearing. Specifically, muscles with a craniodorsal orientation (external oblique and external intercostal muscles) showed an increase in activity when the dogs ran downhill and a decrease when they ran uphill. Muscles with a cranioventral orientation (internal oblique and internal intercostal muscles) exhibited the opposite pattern: increased activity when the dogs ran uphill and decreased activity when they ran downhill. Changes in activity of two extrinsic appendicular muscles, the serratus ventralis and deep pectoralis, during uphill and downhill running were also consistent with the sagittal shearing hypothesis. In contrast, changes in the level of recruitment of the oblique hypaxial muscles were not consistent with stabilization of the trunk against torques that induce yaw at the girdles. Hence, we suggest that the oblique hypaxial muscles of trotting dogs act to stabilize the trunk against sagittal shearing torques induced by limb retraction (fore-aft acceleration) and protraction (fore-aft deceleration).

Entraining the natural frequencies of running and breathing in guinea fowl (Numida meleagris).

Lung ventilation of tetrapods that synchronize their locomotory and ventilatory cycles during exercise could be economized if the resonant frequency of the respiratory system matched the animal's preferred step frequency. To test whether animals utilize this strategy, the input impedance of the respiratory system of five anesthetized, supine guinea fowl (Numida meleagris) was measured using a forced oscillation technique. The resonant frequency of the respiratory system was 7.12+/-0.27 Hz (N=5, mean +/- S.E.M.). No statistically significant difference was found between the resonant frequency of the respiratory system and the panting frequency used by guinea fowl at rest (6.67+/-0.16 Hz, N=11) or during treadmill locomotion (6.71+/-0.12 Hz, N=8) or to their preferred step frequency (6.73+/-0.09 Hz, N=7) (means +/- S.E.M.). These observations suggest (i) that, at rest and during exercise, panting guinea fowl maximize flow while expending minimal mechanical effort, and (ii) that natural selection has tuned the natural frequencies of the respiratory and locomotor systems to similar frequencies.

Influence of rotational inertia on turning performance of theropod dinosaurs: clues from humans with increased rotational inertia.

The turning agility of theropod dinosaurs may have been severely limited by the large rotational inertia of their horizontal trunks and tails. Bodies with mass distributed far from the axis of rotation have much greater rotational inertia than bodies with the same mass distributed close to the axis of rotation. In this study, we increased the rotational inertia about the vertical axis of human subjects 9.2-fold, to match our estimate for theropods the size of humans, and measured the ability of the subjects to turn. To determine the effect of the increased rotational inertia on maximum turning capability, five subjects jumped vertically while attempting to rotate as far as possible about their vertical axis. This test resulted in a decrease in the average angle turned to 20 % of the control value. We also tested the ability of nine subjects to run as rapidly as possible through a tight slalom course of six 90 degrees turns. When the subjects ran with the 9.2-fold greater rotational inertia, the average velocity through the course decreased to 77% of the control velocity. When the subjects ran the same course but were constrained as to where they placed their feet, the average velocity through the course decreased to 65 % of the control velocity. These results are consistent with the hypothesis that rotational inertia may have limited the turning performance of theropods. They also indicate that the effect of rotational inertia on turning performance is dependent on the type of turning behavior. Characters such as retroverted pubes, reduced tail length, decreased body size, pneumatic vertebrae and the absence of teeth reduced rotational inertia in derived theropods and probably, therefore, improved their turning agility. To reduce rotational inertia, theropods may have run with an arched back and tail, an S-curved neck and forelimbs held backwards against the body.

Influence of increased rotational inertia on the turning performance of humans.

The rotational inertia of an animal can be expected to influence directly its ability to execute rapid turning maneuvers. We hypothesized that a ninefold increase in rotational inertia would reduce maximum turning performance to one-ninth of control values. To test this prediction, we increased rotational inertia about the vertical axis of six human subjects and measured their ability to turn during maximum-effort jump turns. We measured the free moment about a vertical (i.e. yaw) axis as the subjects performed maximum-effort jump turns under three conditions: (i) unencumbered, (ii) wearing a backpack with a control weight and (iii) wearing a backpack of the same mass that increased the rotational inertia of the subject to 9.2 times that with the control weight. Rotational inertia measurements allowed us to estimate the angle turned during the take-off period (i.e. from jump initiation until the feet leave the ground) and the angular power and work of the maximum-effort turns. Surprisingly, the angle turned during take-off in the increased inertia trials was 44.7 % of that of the control trials, rather than the 10.9 % (9.2-fold reduction) expected on the basis of the increase in rotational inertia. When the subjects turned with increased rotational inertia, the maximum and mean torques exerted were, on average, 142 % and 190 %, respectively, of the values recorded during the control trials. Maximum torques during increased rotational inertia trials actually approached isometric maxima. In the increased rotational inertia trials, the angular impulse was 252 % of that of the control trials and the take-off period was 130 % of that of the control trials. By exerting larger torques over longer take-off periods, the subjects were able partially to compensate for the excess rotational inertia. In contrast to the observed changes in torque, maximum and mean angular power were highest in the unencumbered trials and lowest in the increased inertia trials. On the basis of a decreased ability to generate vertical force when turning and of our estimates of angular power, we speculate that the greater than expected turning performance was due (i) to adjustments in the pattern of muscle recruitment and (ii) to a reduction in the velocity of muscle shortening that resulted in increased muscle forces.

Ventilation and gas exchange during treadmill locomotion in the American alligator (Alligator mississippiensis).

A number of anatomical characters of crocodilians appear to be inconsistent with their lifestyle as sit-and-wait predators. To address this paradoxical association of characters further, we measured lung ventilation and respiratory gas exchange during walking in American alligators (Alligator mississippiensis). During exercise, ventilation consisted of low-frequency, large-volume breaths. The alligators hyperventilated severely during walking with respect to their metabolic demands. Air convection requirements were among the highest and estimates of lung P(CO2) were among the lowest known in air-breathing vertebrates. Air convection requirements dropped immediately with cessation of exercise. These observations indicate that the ventilation of alligators is not limited by their locomotor movements. We suggest that the highly specialized ventilatory system of modern crocodilians represents a legacy from cursorial ancestors rather than an adaptation to a lifestyle as amphibious sit-and-wait predators.

Pelvic aspiration in the American alligator (Alligator mississippiensis).

The pelvis of crocodilians is highly derived in that the pubic bones are isolated from the acetabulum and are attached to the ischia via moveable joints. We examined the possible role of this unusual morphology in lung ventilation by measuring ventilation, abdominal pressure and the electrical activity of several abdominal and pelvic muscles in the American alligator (Alligator mississippiensis). We found that the activity of two pelvic muscles, the ischiopubis and ischiotruncus muscles, was correlated with inspiration; these muscles rotate the pubes ventrally and thereby increase abdominal volume. During expiration, contraction of the rectus abdominis and transversus abdominis rotates the pubes dorsally. We suggest that this mechanism facilitates diaphragmatic breathing by creating space for caudal displacement of the viscera during inspiration. Because birds also use a dorso-ventral movement of the pelvis to effect ventilation, some form of pelvic aspiration may be plesiomorphic for archosaurs.

Respiration and gas exchange during recovery from exercise in the American alligator.

Low respiratory exchange ratios (R) occur in reptiles. In crocodilians they have been attributed to the loss of respiratory CO2 into the urine and to the immediate exercise-history of an animal. In this study, expired ventilation (V(E)), oxygen consumption (V(O2)), and carbon dioxide excretion (V(CO2)) were measured during recovery from treadmill-exercise in the American alligator. Both V(O2) and V(CO2) decreased exponentially during recovery, but the decrease of V(CO2) was greater than that of V(O2). By 55 min into recovery R fell to 0.3 +/- 0.02 (mean +/- S.E.M). These low values of R may be partially attributable to hyperventilation that occurred during exercise. These data suggest that both hyperventilation during exercise and a metabolic acidosis deplete blood bicarbonate stores, contributing to a low R during recovery. We propose that the right to left cardiac shunt could facilitate restoration of these alkaline reserves and blood pH.

Dynamic gearing in running dogs.

Dynamic gearing is a mechanism that has been suggested to enhance the performance of skeletal muscles by maintaining them at the shortening velocities that maximize their power or efficiency. We investigated this hypothesis in three domestic dogs during trotting and galloping. We used ground force recordings and kinematic analysis to calculate the changes in gear ratio that occur during the production of the external work of locomotion. We also monitored length changes of the vastus lateralis muscle, an extensor muscle of the knee, using sonomicrometry in four additional dogs to determine the nature and rate of active shortening of this muscle. During both trotting and galloping, the gear ratios of the extensor muscles of the elbow, wrist and ankle joints were relatively constant early in limb support, but decreased rapidly during the second half of support. The gear ratio at the hip exerted an extensor moment initially, but decreased throughout limb support and became negative midway through support. This pattern of decreasing gear ratio during the second half of support indicates that dynamic gearing does not maximize muscle power or efficiency at the elbow, wrist, hip and ankle joints. In contrast, the extensor muscles of the shoulder and knee joints exhibited an increase in gear ratio during limb support. In two dogs, the vastus lateralis muscle shortened at a relatively constant rate of 3.7-4 lengths s-1 during intermediate-speed galloping. This pattern of increasing gear ratio and constant velocity of muscle shortening at the knee joint is consistent with the hypothesis of dynamic gearing. Given the amount of work done at the knee and shoulder joints of running dogs, dynamic gearing may contribute to the economy of constant-speed running and may be important to integrated limb function.

External work and potential for elastic storage at the limb joints of running dogs.

The storage and recovery of elastic strain energy in muscles and tendons increases the economy of locomotion in running vertebrates. In this investigation, we compared the negative and positive external work produced at individual limb joints of running dogs to evaluate which muscle-tendon systems contribute to elastic storage and to determine the extent to which the external work of locomotion is produced by muscles that shorten actively rather than by muscles that function as springs. We found that the negative and positive external work of the extensor muscles is not allocated equally among the different joints and limbs. During both trotting and galloping, the vast majority of the negative work was produced by the two distal joints, the wrist and ankle. The forelimb produced most of the negative work in both the trot and the gallop. The hindlimb produced most of the positive work during galloping, but not during trotting. With regards to elastic storage, our results indicate that the forelimb of dogs displays a greater potential for storage and recovery of elastic energy than does the hindlimb. Elastic storage appears to be more important during trotting than during galloping, and elastic storage appears to be more pronounced in the extensor muscles of the distal joints than in the extensor muscles of the proximal joints. Furthermore, our analysis indicates that a significant portion of the external work of locomotion, 26 % during trotting and 56 % during galloping, is produced by actively shortening muscles. We conclude that, although elastic storage of energy is extremely important to the economy of running gaits, actively shortening muscles do make an important contribution to the work of locomotion.

Ventilation and gas exchange in lizards during treadmill exercise.

The extent to which lizards ventilate their lungs during locomotion is controversial. Direct measurements of airflow across the nostrils suggest a progressive reduction in tidal volume and minute ventilation with increased running speed, while other studies have demonstrated that arterial PO2 remains constant during exercise. To resolve these conflicting findings, we measured minute ventilation and gas exchange rate in five specimens of Varanus exanthematicus and five specimens of Iguana iguana during treadmill locomotion at speeds between 0.14 and 1.11ms-1 at 35 degrees C. These speeds are much lower than maximal running speeds, but are greater than the maximal aerobic speed. In both species, the ventilatory pattern during locomotion was highly irregular, indicating an interference between locomotion and lung ventilation. In Varanus exanthematicus, treadmill locomotion elicited a six- to eightfold increase in minute ventilation from a pre-exercise level of 102mlkg-1min-1, whereas the rate of oxygen uptake increased approximately threefold (from 3.9 to 12.6mlkg-1min-1). After exercise, both minute ventilation and gas exchange rate decreased immediately. Because minute ventilation increased more than did oxygen consumption, an increase in lung PO2 during exercise is predicted and, thus, Varanus exanthematicus appears effectively to ventilate its lungs to match the increased metabolic rate during locomotion at moderate speed. In Iguana iguana, both minute ventilation and gas exchange rate increased above resting values during locomotion at 0.28ms-1, but both decreased with further increases in locomotor speed. Furthermore, following exercise, both minute ventilation and oxygen uptake rate increased significantly. Iguana iguana, therefore, appears to be unable to match the increased oxygen demand with adequate ventilation at moderate and higher speeds.

Lack of locomotor-cardiac coupling in trotting dogs.

Coupling of locomotor and cardiac cycles has been suggested to facilitate effective arterial delivery and venous return during vigorous exercise. In an attempt to document locomotor-cardiac coupling, we ran five dogs on a motorized treadmill while monitoring heart activity with surface electrocardiogram electrodes and locomotor events with high-speed video and an accelerometer mounted on the dog's back. Analysis of the cardiac and locomotor frequencies revealed that heart rate was usually slightly greater than stride frequency. Hence the timing of the cardiac cycles varied with respect to the phase of the locomotor cycles, and therefore consistent coupling of the locomotor and cardiac cycles was not observed in any of the dogs. However, the period of the cardiac cycle sometimes varied in a rhythmic way that caused brief periods of transient coupling of the locomotor and cardiac cycles in three of the five dogs. These brief periods of coupling (5-20 heartbeats) occurred at approximately the same phase relationship in each of the three dogs. We hypothesize that the variation in cardiac period and the resulting transient coupling are a function of locomotor and ventilatory influences on venous return and/or ventricular ejection. Because venous return and ejection fraction are likely to vary in an unpredictable manner when animals run in a complex environment, we suggest that reflex control of heart rate will be important during locomotion and strict integer coupling of the locomotor and cardiac cycles is unlikely to evolve.

Function of the intercostal muscles in trotting dogs: ventilation or locomotion?

Although the intercostal muscles play an important role in lung ventilation, observations from fishes and ectothermic tetrapods suggest that their primary function may be locomotion. To provide a broader understanding of the role these muscles play in locomotion, I measured ventilatory airflow at the mouth and activity of the fourth and ninth intercostal muscles in four dogs trotting on a treadmill. During rest and thermoregulatory panting, activity of the intercostal muscles was associated with inspiratory and expiratory airflow. However, during trotting, activity of the interosseous portions of the intercostal muscles was correlated with locomotion. When ventilation and stride cycles were not synchronized, activity of the interosseous intercostal muscles stayed locked to the locomotor events and drifted in time relative to ventilation. In contrast, activity of the parasternal portion of the internal intercostal muscles was always associated with inspiratory airflow. These observations suggest that, in dogs, locomotion is the dominant function of the interosseous portions of the intercostal muscles. However, the parasternal intercostal muscles are primarily inspiratory in function.

Variable gearing during locomotion in the human musculoskeletal system.

Human feet and toes provide a mechanism for changing the gear ratio of the ankle extensor muscles during a running step. A variable gear ratio could enhance muscle performance during constant-speed running by applying a more effective prestretch during landing, while maintaining the muscles near the high-efficiency or high-power portion of the force-velocity curve during takeoff. Furthermore, during acceleration, variable gearing may allow muscle contractile properties to remain optimized despite rapid changes in running speed. Forceplate and kinematic analyses of running steps show low gear ratios at touchdown that increase throughout the contact phase.