Bioenergetics and the origin of hominid bipedalism

Compared to most quadrupedal mammals, humans are energetically inefficient when running at high speeds. This fact can be taken to mean that human bipedalism evolved for reasons other than to reduce relative energy cost during locomotion. Recalculation of the energy expended during human walking at normal speeds shows that (1) human bipedalism is at least as efficient as typical mammalian quadrupedalism and (2) human gait is much more efficient than bipedal or quadrupedal locomotion in the chimpanzee. We conclude that bipedalism bestowed an energetic advantage on the Miocene hominoid ancestors of the Hominidae.     

Bipedality in chimpanzee (Pan troglodytes) and bonobo (Pan paniscus): testing hypotheses on the evolution of bipedalism

A host of ecological, anatomical, and physiological selective pressures are hypothesized to have played a role in the evolution of hominid bipedalism. A referential model, based on the chimpanzee (Pan troglodytes) and bonobo (Pan paniscus), was used to test through experimental manipulation four hypotheses on the evolution of hominid bipedalism. The introduction of food piles (Carry hypothesis) increased locomotor bipedality in both species. Neither the introduction of branches (Display hypothesis) nor the construction of visual barriers (Vigilance hypothesis) altered bipedality in either species. Introduction of raised foraging structures (Forage hypothesis) increased postural bipedality in chimpanzees. These experimental manipulations provided support for carrying of portable objects and foraging on elevated food-items as plausible mechanisms that shaped bipedalism in hominids.     

Men and women adopt similar walking mechanics and muscle activation patterns during load carriage

Although numerous studies have investigated the effects of load carriage on gait mechanics, most have been conducted on active military men. It remains unknown whether men and women adapt differently to carrying load. The purpose of this study was to compare the effects of load carriage on gait mechanics, muscle activation patterns, and metabolic cost between men and women walking at their preferred, unloaded walking speed. We measured whole body motion, ground reaction forces, muscle activity, and metabolic cost from 17 men and 12 women. Subjects completed four walking trials on an instrumented treadmill, each five minutes in duration, while carrying no load or an additional 10%, 20%, or 30% of body weight. Women were shorter (p<0.01), had lower body mass (p=0.01), and had lower fat-free mass (p=0.02) compared to men. No significant differences between men and women were observed for any measured gait parameter or muscle activation pattern. As load increased, so did net metabolic cost, the duration of stance phase, peak stance phase hip, knee, and ankle flexion angles, and all peak joint extension moments. The increase in the peak vertical ground reaction force was less than the carried load (e.g. ground force increased approximately 6% with each 10% increase in load). Integrated muscle activity of the soleus, medial gastrocnemius, lateral hamstrings, vastus medialis, vastus lateralis, and rectus femoris increased with load. We conclude that, despite differences in anthropometry, men and women adopt similar gait adaptations when carrying load, adjusted as a percentage of body weight.     

The metabolic cost of walking in humans, chimpanzees, and early hominins

Bipedalism is a defining feature of the hominin lineage, but the nature and efficiency of early hominin walking remains the focus of much debate. Here, we investigate walking cost in early hominins using experimental data from humans and chimpanzees. We use gait and energetics data from humans, and from chimpanzees walking bipedally and quadrupedally, to test a new model linking locomotor anatomy and posture to walking cost. We then use this model to reconstruct locomotor cost for early, ape-like hominins and for the A.L. 288 Australopithecus afarensis specimen. Results of the model indicate that hind limb length, posture (effective mechanical advantage), and muscle fascicle length contribute nearly equally to differences in walking cost between humans and chimpanzees. Further, relatively small changes in these variables would decrease the cost of bipedalism in an early chimpanzee-like biped below that of quadrupedal apes. Estimates of walking cost in A.L. 288, over a range of hypothetical postures from crouched to fully extended, are below those of quadrupedal apes, but above those of modern humans. These results indicate that walking cost in early hominins was likely similar to or below that of their quadrupedal ape-like forebears, and that by the mid-Pliocene, hominin walking was less costly than that of other apes. This supports the hypothesis that locomotor energy economy was an important evolutionary pressure on hominin bipedalism.     

Do highly trained monkeys walk like humans? A kinematic study of bipedal locomotion in bipedally trained Japanese macaques

In this study, we examined the kinematics of bipedal walking in macaque monkeys that have been highly trained to stand and walk bipedally, and compared them to the kinematics of bipedal walking in ordinary macaques. The results revealed that the trained macaques walked with longer and less frequent strides than ordinary subjects. In addition, they appear to have used inverted pendulum mechanics during bipedal walking, which resulted in an efficient exchange of potential and kinetic energy. These gait characteristics resulted from the relatively more extended hindlimb joints of the trained macaques. By contrast, the body of the ordinary macaques translated downward during the single-limb stance phase due to more flexed hindlimb joints. This resulted in almost in-phase fluctuations of potential and kinetic energy, which indicated that energy transformation was less efficient in the ordinary macaques. The findings provide two insights into the early stage of the evolution of human bipedalism. First, the finding that training considerably improved bipedal walking a posteriori may explain why the very first bipeds that might not yet have been morphologically adapted to bipedal walking continued to walk bipedally. The evolutionary transition from quadrupedalism to bipedalism might not be as difficult as has been envisioned. In addition, the finding that macaques, which are phylogenetically distant from humans and in which bipedal walking is unlike human walking, could develop humanlike gait characteristics with training, provides strong support for the commonly held but unproven idea that the characteristics of the human gait are advantageous to human bipedalism.     

Physiological responses to prolonged treadmill walking with external loads

Limited information is available regarding the physiological responses to prolonged load carriage. This study determined the energy cost of prolonged treadmill walking (fixed distance of 12 km) at speeds of 1.10 m.s-1, 1.35 m.s-1, and 1.60 m.s-1, unloaded (clothing mass 5.2 kg) and with external loads of 31.5 and 49.4 kg. Fifteen male subjects performed nine trials in random order over a 6-week period. Oxygen uptake (VO2) was determined at the end of the first 10 min and every 20 min thereafter. A 10-min rest period was allowed following each 50 min of walking. No changes occurred in VO2 over time in the unloaded condition at any speed. The 31.5 and 49.4 kg loads, however, produced significant increases (ranging from 10 to 18%) at the two fastest and at all three speeds, respectively, even at initial exercise intensities less than 30% VO2max. In addition, the 49.4 kg load elicited a significantly higher (P less than 0.05) VO2 than did the 31.5 kg load at all speeds. The measured values of metabolic cost were also compared to those predicted using the formula of Pandolf et al. In trials where VO2 increased significantly over time, predicted values underestimated the actual metabolic cost during the final minute by 10-16%. It is concluded that energy cost during prolonged load carriage is not constant but increases significantly over time even at low relative exercise intensities. It is further concluded that applying the prediction model which estimates energy expenditure from short-term load carriage efforts to prolonged load carriage can result in significant underestimations of the actual energy cost.     

The metabolic costs of 'bent-hip, bent-knee' walking in humans

The costs of different modes of bipedalism are a key issue in reconstructing the likely gait of early human ancestors such as Australopithecus afarensis. Some workers, on the basis of morphological differences between the locomotor skeleton of A. afarensis and modern humans, have proposed that this hominid would have walked in a 'bent-hip, bent-knee' (BHBK) posture like that seen in the voluntary bipedalism of untrained chimpanzees. Computer modelling studies using inverse dynamics indicate that on the basis of segment proportions AL-288-1 should have been capable of mechanically effective upright walking, but in contrast predicted that BHBK walking would have been highly ineffective. The measure most pertinent to natural selection, however, is more likely to be the complete, physiological, or metabolic energy cost. We cannot measure this parameter in a fossil. This paper presents the most complete investigation yet of the metabolic and thermoregulatory costs of BHBK walking in humans. Data show that metabolic costs including the basal metabolic rate (BMR) increase by around 50% while the energy costs of locomotion and blood lactate production nearly double, heat load is increased, and core temperature does not return to normal within 20 minutes rest. Net effects imply that a resting period of 150% activity time would be necessary to prevent physiologically intolerable heat load. Preliminary data for children suggest that scaling effects would not significantly reduce relative costs for hominids of AL-288-1's size. Data from recent studies using forwards dynamic modelling confirm that similar total (including BMR) and locomotor metabolic costs would have applied to BHBK walking by AL-288-1. We explore some of the ecological consequences of our findings.     

The energetic cost of locomotion: humans and primates compared to generalized endotherms

A wide range of selective pressures have been advanced as possible causes for the adoption of bipedalism in the hominin lineage. One suggestion has been that because modern human walking is relatively efficient compared to that of a typical quadruped, the ancestral quadruped may have reaped an energetic advantage when it walked on two legs. While it has become clear that human walking is relatively efficient and human running inefficient compared to "generalized endotherms", workers differ in their opinion of how the cost of human bipedal locomotion compares to that of a generalized primate walking quadrupedally. One view is that human walking is particularly efficient in comparison to other primates. The present study addresses this by comparing the cost of human walking and running to that of the eight primate species for which data are available and by comparing cost in primates to that of a "generalized endotherm". There is no evidence that primate locomotion is more costly than that of a generalized endotherm, although more data on adult Old World monkeys and apes would be useful. Further, human locomotion does not appear to be particularly efficient relative to that of other primates.     

Limb morphology,bipedal gait,and the energetics of hominid locomotion

How viable is the argument that increased locomotor efficiency was an important agent in the origin of hominid bipedalism? This study reviews data from the literature on the cost of human bipedal walking and running and compares it to data on quadrupedal mammals including several non-human primate species. Literature data comparing the cost of bipedal and quadrupedal locomotion in trained capuchin monkeys and chimpanzees are also considered. It is concluded that increased energetic efficiency would not have accrued to early bipeds. Presumably, however, selection for improved efficiency in the bipedal stance would have occurred once the transition was made. Would such a process have included selection for increased limb length? Data on the cost of locomotion vs. limb length reveal no significant relationship between these variables in 21 species of mammals or in human walking or running. © 1996 Wiley-Liss, Inc.     

Manual digital pressures during knuckle‐walking in chimpanzees (Pan troglodytes)

Considerable attention has been given to hand morphology and function associated with knuckle‐walking in the African apes because of the implications they have for the evolution of bipedalism in early hominins. Knuckle‐walking is associated with a unique suite of musculoskeletal features of the wrist and hand, and numerous studies have hypothesized that these anatomical features are associated with the dynamics of load distribution across the digits during knuckle‐walking. We collected dynamic digital pressures on two chimpanzees during terrestrial and simulated arboreal locomotion. Comparisons were made across substrates, limb positions, hand positions, and age categories. Peak digital pressures were similar on the pole and on the ground but were distributed differently across the digits on each substrate. In young animals, pressure was equally high on digits 2–4 on the ground but higher on digits 3 and 4 on the pole. Older animals experience higher pressures on digits 2 and 3 on the ground. Hand posture (palm‐in vs. palm‐back) influenced the distribution and timing of peak pressures. Age‐related increases in body mass also result in higher overall pressures and increased variation across the digital row. In chimpanzees, digit 5 typically bears relatively little load regardless of hand position or substrate. These are the first quantitative data on digital pressures during knuckle‐walking in hominoids, and they afford the opportunity to develop hypotheses about variation among hominoids and biomechanical models of wrist and forearm loading. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

Interactions among paternal behavior, steroid hormones, and parental experience in male marmosets (Callithrix kuhlii)

Male black tufted-ear marmosets (Callithrix kuhlii) contribute to the rearing of their offspring. Here we evaluated predictions of hypotheses suggesting that (1) T and E2 influence infant-care behavior in male marmosets, (2) levels of T and E2 are modulated by paternal experience, and (3) paternal behavior and levels of T and E2 in male marmosets covary with stress. We observed the behavior of marmosets in their family groups following the birth of infants and evaluated urinary concentrations of T, E2, and the stress hormone cortisol (CORT) among fathers before and after the birth of young. Urinary levels of T, E2, and CORT were lower among males who carried infants at high rates than males who carried at low rates, and T and CORT levels were negatively correlated with carrying rates across all males. Males had significantly lower T levels while carrying the second compared to the first litter and slightly lower rates of infant-carrying, possibly due to assistance provided by offspring of the first litter. There were increases in CORT levels of fathers after the birth of the first litter, but decreases in CORT after the birth of the second. Our results suggest a relationship in C. kuhlii between paternal behavior, hormones, and paternal experience. Rates of infant-carrying appear to be linked to hormone levels, and hormone levels in turn are affected by experience caring for young. Our data also suggest that T, E2, and CORT have synergistic influences on infant-carrying behavior or alternatively that associations between T and E2 and rates of infant-carrying are influenced by stress or other glucocorticoid-related variables. Finally, we propose a hypothesis suggesting that experience-related changes in hormones reinforce the commitment of males to successful breeding partnerships.     

Effects of load carrying on metabolic cost and hindlimb muscle dynamics in guinea fowl (Numida meleagris).

The goal of this study was to test whether the contractile patterns of two major hindlimb extensors of guinea fowl are altered by load-carrying exercise. We hypothesized that changes in contractile pattern, specifically a decrease in muscle shortening velocity or enhanced stretch activation, would result in a reduction in locomotor energy cost relative to the load carried. We also anticipated that changes in kinematics would reflect underlying changes in muscle strain. Oxygen consumption, muscle activation intensity, and fascicle strain rate were measured over a range of speeds while animals ran unloaded vs. when they carried a trunk load equal to 22% of their body mass. Our results showed that loading produced no significant (P > 0.05) changes in kinematic patterns at any speed. In vivo muscle contractile strain patterns in the iliotibialis lateralis pars postacetabularis and the medial head of the gastrocnemius showed a significant increase in active stretch early in stance (P < 0.01), but muscle fascicle shortening velocity was not significantly affected by load carrying. The rate of oxygen consumption increased by 17% (P < 0.01) during loaded conditions, equivalent to 77% of the relative increase in mass. Additionally, relative increases in EMG intensity (quantified as mean spike amplitude) indicated less than proportional recruitment, consistent with force enhancement via stretch activation, in the proximal iliotibialis lateralis pars postacetabularis; however, a greater than proportional increase in the medial gastrocnemius was observed. As a result, when averaged for the two muscles, EMG intensity increased in direct proportion to the fractional increase in load carried.     

How do load carriage and walking speed influence trunk coordination and stride parameters?

To determine the effects of load carriage and walking speed on stride parameters and the coordination of trunk movements, 12 subjects walked on a treadmill at a range of walking speeds (0.6-1.6 m s(-1)) with and without a backpack containing 40% of their body mass. It was hypothesized that compared to unloaded walking, load carriage decreases transverse pelvic and thoracic rotation, the mean relative phase between pelvic and thoracic rotations, and increases hip excursion. In addition, it was hypothesized that these changes would coincide with a decreased stride length and increased stride frequency. The findings supported the hypotheses. Dimensionless analyses indicated that there was a significantly larger contribution of hip excursion and smaller contribution of transverse plane pelvic rotation to increases in stride length during load carriage. In addition, there was a significant effect of load carriage on the amplitudes of transverse pelvic and thoracic rotation and the relative phase of pelvic and thoracic rotation. It was concluded that the shorter stride length and higher stride frequency observed when carrying a backpack is the result of decreased pelvic rotation. During unloaded walking, increases in pelvic rotation contribute to increases in stride length with increasing walking speed. The decreased pelvic rotation during load carriage requires an increased hip excursion to compensate. However, the increase in hip excursion is insufficient to fully compensate for the observed decrease in pelvis rotation, requiring an increase in stride frequency during load carriage to maintain a constant walking speed.     

Optimal rate of work for mountaineers

The physiological responses of seven young male highlanders were recorded at high altitude while they were carrying loads (0, 25, 35, 45, and 55 kg) on snow at different speeds, supporting the loads on their backs by circular straps around the forehead. The rates of work calculated from the gross weight (body weight plus actual load in kg) multiplied by the speed of walking, m.min-1, ranged from 4,460 to 8,440 kg.m.min-1. The relationship between the rate of work and energy expenditure was rectilinear within the present range of values. The oxygen consumption (51.6 and 59.7 ml.min-1.kg-1 BW) for 55-kg load (at 4.09 and 4.64 km.h-1) possibly reached maximal aerobic capacity. At higher energy output at high altitude the subjects were exhausted after a short period of work. The proportion of increase of oxygen consumption per kg gross weight carried or per kg.m was almost constant up to a 55-kg experimental load. It is suggested that for day-to-day operations work should not be undertaken at more than 30-40% of maximal work capacity; a rate of work around 4,000 kg.m.min-1 (25-30 kg actual load at 3.0 to 3.5 km.h-1) may be considered as optimal for highlanders and porters at high altitude.     

Forward dynamic simulation of bipedal walking in the Japanese macaque: investigation of causal relationships among limb kinematics, speed, and energetics of bipedal locomotion in a nonhuman primate

Japanese macaques that have been trained for monkey performances exhibit a remarkable ability to walk bipedally. In this study, we dynamically reconstructed bipedal walking of the Japanese macaque to investigate causal relationships among limb kinematics, speed, and energetics, with a view to understanding the mechanisms underlying the evolution of human bipedalism. We constructed a two-dimensional macaque musculoskeletal model consisting of nine rigid links and eight principal muscles. To generate locomotion, we used a trajectory-tracking control law, the reference trajectories of which were obtained experimentally. Using this framework, we evaluated the effects of changes in cycle duration and gait kinematics on locomotor efficiency. The energetic cost of locomotion was estimated based on the calculation of mechanical energy generated by muscles. Our results demonstrated that the mass-specific metabolic cost of transport decreased as speed increased in bipedal walking of the Japanese macaque. Furthermore, the cost of transport in bipedal walking was reduced when vertical displacement of the hip joint was virtually modified in the simulation to be more humanlike. Human vertical fluctuations in the body's center of mass actually contributed to energy savings via an inverted pendulum mechanism.     

Bipedal tool use strengthens chimpanzee hand preferences

The degree to which non-human primate behavior is lateralized, at either individual or population levels, remains controversial. We investigated the relationship between hand preference and posture during tool use in chimpanzees (Pan troglodytes) during bipedal tool use. We experimentally induced tool use in a supported bipedal posture, an unsupported bipedal posture, and a seated posture. Neither bipedal tool use nor these supported conditions have been previously evaluated in apes. The hypotheses tested were 1) bipedal posture will increase the strength of hand preference, and 2) a bipedal stance, without the use of one hand for support, will elicit a right hand preference. Results supported the first, but not the second hypothesis: bipedalism induced the subjects to become more lateralized, but not in any particular direction. Instead, it appears that subtle pre-existing lateral biases, to either the right or left, were emphasized with increasing postural demands. This result has interesting implications for theories of the evolution of tool use and bipedalism, as the combination of bipedalism and tool use may have helped drive extreme lateralization in modern humans, but cannot alone account for the preponderance of right-handedness.     

THE EVOLUTION OF BIPEDALISM IN JERBOAS (RODENTIA: DIPODOIDEA): ORIGIN IN HUMID AND FORESTED ENVIRONMENTS

Mammalian bipedalism has long been thought to have arisen in response to arid and open environments. Here, we tested whether bipedalism coevolved with environmental changes using molecular and paleontological data from the rodent superfamily Dipodoidea and statistical methods for reconstructing ancestral characteristics and past climates. Our results show that the post‐Late Miocene aridification exerted selective pressures on tooth shape, but not on leg length of bipedal jerboas. Cheek tooth crown height has increased since the Late Miocene, but the hind limb/head‐body length ratios remained stable and high despite the environmental change from humid and forested to arid and open conditions, rather than increasing from low to high as predicted by the arid‐bipedalism hypothesis. The decoupling of locomotor and dental character evolution indicates that bipedalism evolved under selective pressure different from that of dental hypsodonty in jerboas. We reconstructed the habitats of early jerboas using floral and faunal data, and the results show that the environments in which bipedalism evolved were forested. Our results suggest that bipedalism evolved as an adaptation to humid woodlands or forests for vertical jumping. Running at high speeds is likely a by‐product of selection for jumping, which became advantageous in open environments later on.     

Effect of stable and unstable load carriage on walking gait variability,dynamic stability and muscle activity of older adults

Load carriage perturbs the neuromuscular system, which can be impaired due to ageing. The ability to counteract perturbations is an indicator of neuromuscular function but if the response is insufficient the risk of falls will increase. However, it is unknown how load carriage affects older adults. Fourteen older adults (65 ± 6 years) attended a single visit during which they performed 4 min of walking in 3 conditions, unloaded, stable backpack load and unstable backpack load. During each walking trial, 3-dimensional kinematics of the lower limb and trunk movements and electromyographic activity of 6 lower limb muscles were recorded. The local dynamic stability (local divergence exponents), joint angle variability and spatio-temporal variability were determined along with muscle activation magnitudes. Medio-lateral dynamic stability was lower (p = 0.018) and step width (p = 0.019) and step width variability (p = 0.015) were greater in unstable load walking and step width variability was greater in stable load walking (p = 0.009) compared to unloaded walking. However, there was no effect on joint angle variability. Unstable load carriage increased activity of the Rectus Femoris (p = 0.001) and Soleus (p = 0.043) and stable load carriage increased Rectus Femoris activity (p = 0.006). These results suggest that loaded walking alters the gait of older adults and that unstable load carriage reduces dynamic stability compared to unloaded walking. This can potentially increase the risk of falls, but also offers the potential to use unstable loads as part of fall prevention programmes.     

Carrying, Sharing, and Hand Preference in Tufted Capuchins (Cebus apella)

We examined the relationship among carrying, food-sharing, and hand preference in tufted capuchins (Cebus apella). The rationale was to evaluate further the use of Cebus as an alternative primate model to Pan for behavior relevant to early hominid evolution. We first examined bipedalism and food-sharing within an established social group, and then examined the direction and strength of hand preference for food carrying in an expanded sample. Several aspects of capuchin behavior warrant discussion. First, bipedal carrying and food-sharing occurred more frequently when we provided bulky foods than when we provided smaller foods. Second, food-sharing was characterized by passive tolerance, rather than active giving, between subjects. Third, subjects shared food primarily with immatures and followed a pattern of reciprocal exchange. Finally, we found no evidence for population-level hand preference for carrying. We posit that an array of behavioral similarities among Cebus, Pan, and Homo evolved through convergent processes, and in this regard capuchins can be seen as an alternative primate model to chimpanzees for the evolution of early hominid behavior.     

Effect of load on preferred speed and cost of transport.

Horses have a tendency to utilize a relatively narrow set of speeds near the middle of a much broader range they are capable of using within a particular gait, i.e., a preferred speed. Possible explanations for this behavior include minimizing musculoskeletal stresses and maximizing metabolic economy. If metabolic economy (cost of transport, CT) and preferred speeds are linked, then shifts in CT should produce shifts in preferred speed. To test this hypothesis, preferred speed was measured in trotting horses (n = 7) unloaded on the level and loaded with 19% of their body weight on the level. The preferred speed on the level was 3.33 +/- 0.09 (SE) m/s, and this decreased to 3.13 +/- 0.11 m/s when loaded. In both conditions (no load and load), the rate of O2 consumption (n = 3) was a curvilinear function of speed that produced a minimum CT (i.e., speed at which trotting is most economical). When unloaded, the speed at which CT was minimum was very near the preferred speed. With a load, CT decreased and the minimum was also near the preferred speed of horses while carrying a load.