Limits to human locomotor performance: phylogenetic origins and comparative perspectives
1 Section of Integrative Biology, University of Texas at Austin, Austin, TX 78712-1064, USA and
2 Smithsonian Tropical Research Institute, Balboa, Republic of Panama
*e-mail: r_dudley{at}utxvms.cc.utexas.edu
Accepted June 28, 2001
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Summary |
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Key words: evolution, human, hummingbird, hypoxia, locomotion, metabolic rate.
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To know humans, study chimpanzees |
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Within evolutionary contexts, the energetic consequences of bipedalism are not well understood. In a widely cited study, Taylor and Rowntree (Taylor and Rowntree, 1973) measured the metabolic costs of locomotion on treadmills for juvenile chimpanzees running bipedally and quadrupedally; no significant differences were found between the two locomotor modes. However, this approach may underestimate the actual costs of locomotion on naturally occurring and potentially irregular substrata, for which use of four legs may provide an energetic advantage.
Quadrupedalism can enhance cursorial maneuverability (Lovejoy, 1981), particularly in the context of vegetated terrain. A similar situation pertains in the use by humans of hiking poles to enhance balance, although concomitant energetic costs appear to be context-dependent (Rodgers et al., 1995; Jacobson et al., 1997; Jacobson et al., 2000). Furthermore, the juvenile chimpanzees studied by Taylor and Rowntree (Taylor and Rowntree, 1973) may not have yielded locomotor metabolic rates representative of adults (Steudel, 1996). Bipedalism is actually an infrequent behavior in chimpanzees (Hunt, 1994), and comparison of the costs of locomotion in humans with those measured in trained chimpanzees (Rodman and McHenry, 1980) is not evolutionarily germane. Training itself may alter patterns of energetic expenditure through a reduction in kinematic variance. In summary, the energetic implications of the transition from knuckle-walking quadrupedalism to bipedalism remain speculative. Theoretical modelling of the mechanical costs of locomotion for known fossil morphologies and likely kinematic profiles (Willems et al., 1995; Kramer, 1999) may be the best method for resolving this important question.
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Paleolithic athletics and the domestication of Homo sapiens |
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Using the example of modern humans to infer the locomotor capacity of ancestral hominids might therefore be analogous to using domesticated canines in the phylogenetic reconstruction of canid exercise physiology. Potentially confounding effects of domestication on anatomical and physiological characteristics clearly cannot be excluded in such cases.
Instead, physiological inferences can be drawn from the study of extant hominid taxa and from the fossil record. Foraging strategies can, in particular, provide suggestive information concerning locomotor and energetic demands on ancestral humans. Phytophagy is the dominant feeding strategy of extant apes, although low-level inclusion of animal protein is also characteristic (Milton, 1999b). This pattern probably characterized early humans up to the origins of agriculture (approximately 10000 BCE=Before Common Era) (Diamond, 1999) and persists to the present time among hunter-gatherers who, with the exception of certain high-latitude groups, rely mostly on plant foods (Eaton and Konner, 1985; Eaton et al., 1997; Milton, 1999b; Milton, 2000). Superimposed upon foraging for somatic and reproductive plant structures was an increased tendency of ancestral hominids towards carcass-scavenging and active hunting (Blumenschine, 1987; Gordon, 1987). The higher caloric rewards could potentially have exceeded the increased anaerobic and aerobic costs of such activities. In turn, greater incorporation of higher-value plant products and of animal fat and protein may have facilitated energetically costly increases in brain size (Milton, 1988; Milton, 1993; Milton, 1999a; Foley and Lee, 1991; Aiello and Wheeler, 1995). Such increases occurred within the ecological context of a fairly constant vegetational mosaic of forest and grassland, albeit one characterized by greater aridity since 3 million years ago (Kingston et al., 1994; Vrba et al., 1994; deMenocal, 1995). Also, conditions of moderate hypoxia probably prevailed for much of human evolution, with concomitant implications for exercise physiology (see below).
Aforementioned foraging patterns and other contemporaneous locomotor behaviors deviate dramatically from contemporary conceptions of exercise in humans. Most hominid locomotion was probably intermittent rather than continuous and, very early in hominid evolution (i.e. from 4.5 to 3.5 million years ago), would have involved combinations of knuckle-walking and bipedal behavior. In modern humans and in other taxa, intermittent locomotion with variable exercise and rest periods reduces lactate build-up and increases overall endurance (Saltin et al., 1976). Movement over natural, irregular terrain can also dramatically alter metabolic expenditure. For example, the cost of transport increases several-fold moving on sand relative to firm substrata (Zamparo et al., 1992; Lejeune et al., 1998) and increases linearly with increasing angle of incline (Margaria, 1976). Carcass-hauling, offspring-carrying and related locomotor behaviors similarly represent additional avenues of energetic expenditure. Pathological conditions, including parasite and pathogen loads, gait disorders and bone breakages, may also influence locomotor performance. For example, approximately 31% of the gibbon skeletons examined by Schultz (Schultz, 1939) exhibited repaired long bones, and the majority of baboons studied by Bramblett (Bramblett, 1967) had at least one healed fracture. Ancestral humans were clearly not exempt from such pathologies or from their concomitant effects on locomotor mechanics and energetics. Contemporary knowledge of performance limits in well-fed, trained human athletes may therefore be unrepresentative of human ancestors living and moving within natural terrains. Similarly, no experimental attention has been given to the influence of the aforementioned biotic and abiotic factors on the exercise physiology of extant hominoid taxa.
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Scaling Mount Olympus: evolution at altitude |
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Hypobaric hypoxia is known to reduce maximal aerobic power in modern humans (Cerretelli and Hoppeler, 1996; West, 1996), whereas any number of ecological scenarios for ancient hominids are consistent with selection for enhanced aerobic capacity. It is therefore not surprising that the physiological traits underlying hypoxia-tolerance in modern humans are similar to those associated with greater endurance (Hochachka et al., 1998). More generally, atmospheric oxygen availability interacts with morphological and physiological factors underlying internal gas transport to constrain aerobic capacity. Athletic training in humans, for example, is known to increase the maximum rate of oxygen uptake, and yields correlated increases in the mass, myoglobin content and capillary density of skeletal muscles, together with increases in cardiac stroke volume. For birds and mammals, maximum cardiac output is a strong predictor of aerobic capacity for any given level of atmospheric oxygen availability (Bishop, 1997; Bishop, 1999). At least in humans, however, a variety of transport conductances supplemental to cardiac output also influence aerobic capacity, particularly at the lower oxygen partial pressures of higher elevations (Jones and Lindstedt, 1993; Wagner, 1996a; Wagner, 1996b).
One approach to identifying general constraints on aerobic capacity is to examine taxa with unusually high metabolic rates. Hummingbirds (family Trochilidae) are known for their extreme levels of oxygen consumption during flight (Suarez, 1992; Suarez, 1996), but less appreciated is the extent to which this group also comprises mostly mid-montane specialists. Hummingbirds are most typically found in the elevational range 10002500m, and relationships among the major trochilid lineages suggest progressive colonization of higher altitudes (Fig.2) (Bleiweiss, 1998a). Flight at such elevations requires substantial compensatory responses to reductions in both air density and oxygen partial pressure (Faraci, 1991; Dudley and Chai, 1996). In ruby-throated hummingbirds (Archilochus colubris), substantial resistance to hypoxia has been demonstrated in experimental studies of hovering flight in hypodense and hypoxic gas mixtures (Chai and Dudley, 1996). Ruby-throated hummingbirds sustain hovering flight at oxygen partial pressures corresponding to elevations of approximately 4000m, even when simultaneously challenged aerodynamically by air densities two-thirds the sea-level value. Flight failure in such gas mixtures clearly derives from reduced oxygen supply rather than from the aerodynamic limits that pertain in contexts of greater oxygen availability (Chai and Dudley, 1995; Chai et al., 1996).
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Knuckle-walking into the future |
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Finally, the ability to simulate elevational gradients in the laboratory and to decouple the effects of variable air density from those of oxygen availability (Dudley, 2000b) suggest that both short-term and evolutionary responses to hypobaria can be studied in diverse animal taxa, even including primates.
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Acknowledgments |
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References |
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