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OBJECTIVE: An experiment was conducted to determine if modifying habitual activities to involve mechanical loading from more diverse directions can enhance the growing skeleton. METHODS: Growing female C57BL/6J mice were housed individually for 3 months in enclosures designed to accentuate either non-linear locomotion (diverse-orientation loading) or linear locomotion (stereotypic-orientation loading) (n=10/cage type). Behavioral assessments were performed daily to quantify cage activity level. Following the experiment, trabecular and cortical bone structure in the humeral head and distal femoral metaphysis were analyzed with µCT. RESULTS: Throughout the experiment, groups did not differ in cage activity level. Yet, following the experiment, the proximal humeri of mice that experienced increased diverse-orientation loading had significantly greater trabecular bone volume fraction (p=0.004), greater cortical bone area (p=0.005), greater cortical area fraction (p=0.0007), and thicker cortices (p=0.002). No significant group differences were detected in the distal femoral metaphysis. CONCLUSIONS: Diverting habitual activities to entail loading from more diverse orientations can augment the growing mouse skeleton. This study suggests that low-intensity activities that produce loads from diverse directions may represent a viable alternative to vigorous, high-impact exercise as a means of benefiting skeletal health during growth.

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Little ontogenetic data exist to indicate whether muscular organization of neonates reflects adult locomotion (e.g., leaping) or infant activities like clinging or the initial quadrupedal phase of locomotion that typifies most infant primates. In the present study, five species of primates with contrasting modes of locomotion were examined. Twenty-eight preserved neonatal and adult cadavers were studied by careful dissection of the hip, thigh, and leg muscles. Wet weights were taken of limb muscles after removal, and the muscles were combined into major functional groups (e.g., flexors, extensors) of each limb segment. Results demonstrate that the distribution of muscle mass within the thigh and within the leg are similar between neonates and adults for all species, with major groups varying by 5% or less in all but two age comparisons. Crural indices of the neonates are nearly identical to those of the adults, but leg/thigh muscle mass ratios were higher in the neonates. Species vary greatly in the percentage of adult limb segment muscle mass present in neonates, with Tarsius syrichta having the greatest percentage for all segments and two lemurids showing the least. These results primarily track differences in relative body mass at birth rather than developmental differences. The adaptive distribution of muscle, as discussed previously for adult prosimians, appears to be established at birth. Neonates of leaping species already have much larger quadriceps muscles than quadrupeds. Differences between large- and small-bodied leapers (e.g., pronounced superficial plantarflexor masses in tarsiers and pronounced deep plantarflexor masses in sifakas) also are present in neonates. Ratios of muscle mass over body mass are smaller in all neonates than in their adult counterparts, suggesting that the neonates are relatively poorly muscled, and that muscle mass must increase with positive allometry during growth.

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Modern humans exhibit increasing relative enamel thickness from M1 to M3. Some biomechanical (basic lever) models predict that the more distal molars in humans encounter higher occlusal forces, and it has been postulated that this provides a functional explanation for the observed gradient in relative enamel thickness. However, constrained three-dimensional models and experimental observations suggest that there is a reduction in bite force potential from M1 to M3, which would be consistent with the tendency for humans to reduce the size of the distal molars. In this regard, it has been postulated that the distal increase in enamel thickness is a consequence of crown size reduction; thus, it is unnecessary to invoke functional scenarios to explain this phenomenon. We assess these competing proposals by examining relative enamel thickness in a catarrhine primate (Papio ursinus) that exhibits crown size increase from M1 to M3. The molar row of P. ursinus is positioned relatively far forward of the temporomandibular joint, which results in the baboon being able to exert relatively greater muscle forces during posterior biting in comparison to modern humans. Thus, a significant distalward gradient of increasing enamel thickness would be expected in P. ursinus according to the hypothesis that posits it to be functionally related to bite force. The present study reveals no significant difference in relative enamel thickness along the molar row in P. ursinus. This finding lends support to the notion that the relatively thicker enamel of human distal molars is related primarily to their reduction in size. This carries potential implications for the interpretation of enamel thickness in phylogenetic reconstructions: the relatively thick molar enamel shared by modern humans and some of our fossil relatives may not be strictly homologous, in that it may result from different underlying developmental mechanisms.

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The strain environment of the tibial midshaft of two female macaques was evaluated through in vivo bone strain experiments using three rosette gauges around the circumference of the bones. Strains were collected for a total of 123 walking and galloping steps as well as several climbing cycles. Principal strains and the angle of the maximum (tensile) principal strain with the long axis of the bone were calculated for each gauge site. In addition, the normal strain distribution throughout the cross section was determined from the longitudinal normal strains (strains in the direction of the long axis of the bone) at each of the three gauge sites, and at the corresponding cross-sectional geometry of the bone. This strain distribution was compared with the cross-sectional properties (area moments) of the midshaft. For both animals, the predominant loading regime was found to be bending about an oblique axis running from anterolateral to posteromedial. The anterior and part of the medial cortex are in tension; the posterior and part of the lateral cortex are in compression. The axis of bending does not coincide with the maximum principal axis of the cross section, which runs mediolaterally. The bones are not especially buttressed in the plane of bending, but offer the greatest strength anteroposteriorly. The cross-sectional geometry therefore does not minimize strain or bone tissue. Peak tibial strains are slightly higher than the peak ulnar strains reported earlier for the same animals (Demes et al. [1998] Am J Phys Anthropol 106:87-100). Peak strains for both the tibia and the ulna are moderate in comparison to strains recorded during walking and galloping activities in nonprimate mammals.

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Much research has been devoted to spinal kinematics of nonmammalian vertebrates, while comparatively little is known about the locomotor role of spinal movements in mammals, especially primates. This study, conducted at the Duke University Primate Center, examines the function of lateral spinal bending during quadrupedal walking among a diverse sample of strepsirhines. The taxa studied include Loris tardigradus (1), Nycticebus coucang (1), N. pygmaeus (1), Cheirogaleus medius (2), Varecia variegata (2), Eulemur fulvus (2), and a total sample size of 261 strides. Lateral bending varies among the taxa with respect to both magnitude and effects of velocity, and does not appear to be correlated with body size. In addition, the timing of lateral bending during a stride appears to differ from that reported for other (nonmammalian) tetrapods. On average, maximum lateral flexion occurs just after ipsilateral foot touchdown, which may be functionally associated with touchdown of the contralateral forelimb during diagonal sequence gait. For some of the taxa, lateral flexion coincides more closely with foot touchdown as velocity increases, suggesting a functional role in increasing hindlimb stride length. Both of these timing patterns contrast with those reported for lizards. Finally, although lorids as a group have been described as having a "sinuous" gait, this study shows more pronounced lateral flexion in Nycticebus than in Loris.

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The thickness of the inferior and superior cortices of the femoral neck was measured on X-rays of 181 strepsirhine primate femora representing 24 species. Neck length, neck depth and neck-shaft angle were also measured. The strength of the femoral neck in frontal bending was estimated by modeling the neck as a hollow cylinder, with neck depth as the outer diameter and cortical thickness representing the superior and inferior shell dimensions. Results indicate that the inferior cortex is always thicker than the superior cortex. The ratio of superior to inferior cortical thickness is highly variable but distinguishes two of the three locomotor groups in the sample. Vertical clingers and leapers have higher ratios (i.e., a more even distribution of cortical bone) than quadrupeds. The slow climbers tend to have the lowest ratios, although they do not differ significantly from the leapers and quadrupeds. These results do not confirm prior theoretical expectations and reported data for anthropoid primates that link greater asymmetry of the cortical shell to more stereotypical hip excursions. The ratio of superior to inferior cortical thickness is unrelated to body mass, femoral neck length, and neck-shaft angle, calling into question whether the short neck of strepsirhine primates acts as a cantilever beam in bending. On the other hand, the estimated section moduli are highly correlated with body mass and neck length, a correlation that is driven primarily by body mass. In conclusion, we believe that an alternative interpretation to the cantilever beam model is needed to explain the asymmetry in bone distribution in the femoral neck, at least in strepsirhine primates (e.g., a thicker inferior cortex is required to reinforce the strongly curved inferior surface). As in prior studies of cross-sectional geometry of long bones, we found slightly positive allometry of cortical dimensions with body mass.

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The cross-sectional properties of mammalian limb bones provide an important source of information about their loading history and locomotor adaptations. It has been suggested, for instance, that the cross-sectional strength of primate limb bones differs from that of other mammals as a consequence of living in a complex arboreal environment (Kimura, 1991, 1995). In order to test this hypothesis more rigorously, we have investigated cross-sectional properties in samples of humeri and femora of 71 primate species, 30 carnivorans and 59 rodents. Primates differ from carnivorans and rodents in having limb bones with greater cross-sectional strength than mammals of similar mass. This might imply that primates have stronger bones than carnivorans and rodents. However, primates also have longer proximal limb bones than other mammals. When cross-sectional dimensions are regressed against bone length, primates appear to have more gracile bones than other mammals. These two seemingly contradictory findings can be reconciled by recognizing that most limb bones experience bending as a predominant loading regime. After regressing cross-sectional strength against the product of body mass and bone length, a product which should be proportional to the bending moments applied to the limb, primates are found to overlap considerably with carnivorans and rodents. Consequently, primate humeri and femora are similar to those of nonprimates in their resistance to bending. Comparisons between arboreal and terrestrial species within the orders show that the bones of arboreal carnivorans have greater cross-sectional properties than those of terrestrial carnivorans, thus supporting Kimura's general notion. However, no differences were found between arboreal and terrestrial rodents. Among primates, the only significant difference was in humeral bending rigidity, which is higher in the terrestrial species. In summary, arboreal and terrestrial species do not show consistent differences in long bone reinforcement, and Kimura's conclusions must be modified to take into account the interaction of bone length and cross-sectional geometry.

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Knowledge of the forces animals generate and are exposed to during locomotion is an important prerequisite for understanding the musculoskeletal correlates of locomotor modes. We recorded takeoff and landing forces for 14 animals representing seven species of strepsirhine primates with a compliant force pole. Our sample included both specialized vertical clingers and leapers and more generalized species. Takeoff forces are higher than landing forces. Peak forces during acceleration for takeoff ranged from 6 to 12 times body weight, and the peak impact forces at landing are between 5 and 9 times body weight. There is a size-related trend in peak force magnitudes. Both takeoff and landing forces decrease with increasing body size in our sample of animals from 1 kg to over 5 kg. Peak forces increase with distance leapt. The distance effect is less clear, probably due to the narrow range of distances represented in our sample. A comparison of subadult and adult animals of two species of sifakas reveals a tendency for the young animals to exert relatively higher peak forces in comparison to their adult conspecifics. Finally, Lemur catta and Eulemur rubriventer, the "generalists" in our sample, tend to generate higher forces for equal tasks than the specialized vertical clingers and leapers (i.e., the indriids and Hapalemur).A broad-scale comparison of peak leaping forces and peak forces for quadrupedal and bipedal walking and running shows that leaping at small body size is associated with exceptionally high forces. Whereas relative forces (i.e., forces divided by body weight) decrease with increasing body mass for leaping, forces for walking and running do not change much with size. Leaping forces in our sample scale to (mass)(-1/3), which is consistent with expectations derived from geometric similarity models. Forces associated with other locomotor activities do not appear to follow this pattern. The very high forces found in strepsirhine leapers do not seem to be matched by bone robusticity beyond that documented for quadrupedal species.

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In vivo bone strain experiments were performed on the ulnae of three female rhesus macaques to test how the bone deforms during locomotion. The null hypothesis was that, in an animal moving its limbs predominantly in sagittal planes, the ulna experiences anteroposterior bending. Three rosette strain gauges were attached around the circumference of the bone slightly distal to midshaft. They permit a complete characterization of the ulna's loading environment. Strains were recorded during walking and galloping activities. Principal strains and strain directions relative to the long axis of the bone were calculated for each gauge site. In all three animals, the lateral cortex experienced higher tensile than compressive principal strains during the stance phase of walking. Compressive strains predominated at the medial cortex of two animals (the gauge on this cortex of the third animal did not function). The posterior cortex was subject to lower strains; the nature of the strain was highly dependent on precise gauge position. The greater principal strains were aligned closely with the long axis of the bone in two animals, whereas they deviated up to 45 degrees from the long axis in the third animal. A gait change from walk to gallop was recorded for one animal. It was not accompanied by an incremental change in strain magnitudes. Strains are at the low end of the range of strain magnitudes recorded for walking gaits of nonprimate mammals. The measured distribution of strains in the rhesus monkey ulna indicates that mediolateral bending, rather than anteroposterior bending, is the predominant loading regime, with the neutral axis of bending running from anterior and slightly medial to posterior and slightly lateral. A variable degree of torsion was superimposed over this bending regime. Ulnar mediolateral bending is apparently caused by a ground reaction force vector that passes medial to the forearm. The macaque ulna is not reinforced in the plane of bending. The lack of buttressing in the loaded plane and the somewhat counterintuitive bending direction recommend caution with regard to conventional interpretations of long bone cross-sectional geometry.

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Although the skeletal correlates of vertical clinging and leaping behavior in primates have been studied in great detail, myological information on this locomotor group is not readily available. We here provide relative muscle mass data for the hindlimb of four prosimian leapers, representing indriids as well as the small-bodied tarsiers and galagos. Wet weights of all hindlimb muscles, with the exception of the intrinsic muscles of the foot, were determined. For comparative purposes muscle weights were also gathered for Varecia, an arboreal quadruped, and previously unpublished dry muscle weights of several monkeys are included as well. The specialized leapers are characterized by a predominance of muscles for hindlimb joint extensions. Indriids have larger hip extensors than ankle plantarflexors, whereas the galago and tarsier display the reverse condition. This dichotomy in relative muscle mass corresponds to a dichotomy in leaping kinematics, with indriids going through a greater range of movement at the hip joint and galagos and tarsiers at the ankle joint. However, the most striking result is the overwhelming dominance of the quadriceps femoris muscle in both groups. This suggests that power may be transferred from the knee and thigh to adjacent joints and segments. In contrast, quadrupedal primates have more extensor musculature at the hip, suggesting that the need for a short swing phase pendulum constrains muscle mass distribution within the limb of quadrupeds. Total muscle mass of the hindlimb as well as the mass of the propulsive muscles scale with body mass at exponents below the functional equivalence expectation. Larger-bodied leapers therefore have less muscle force available per unit body weight to be propelled than their smaller-bodied counterparts.

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Our current knowledge about the forces leapers generate and absorb is very limited and based exclusively on rigid force platform measurements. In their natural environments, however, leapers take off and land on branches and tree trunks, and these may be compliant. We evaluated the influence of substrate properties on leaping kinetics in prosimian leapers by using a combined field and laboratory approach. Tree sway and the timing of takeoffs relative to the movements of trees were documented for animals under natural conditions in Madagascar. Field data collected on three species (Indri indri, Propithecus diadema, Propithecus verreauxi) indicate that in the majority of takeoffs, the substrate sways and the animals takeoff before the elastic rebound of the substrate. This implies that force is "wasted" to deform supports. Takeoff and landing forces were measured in an experimental setting with a compliant force pole at the Duke University Primate Center. Forces were recorded for 2 Propithecus verreauxi and 3 Hapalemur griseus. Peak takeoff forces were 9.6 (P. verreauxi) and 10.3 (H. griseus) times body weight, whereas peak landing forces were 6.7 (P. verreauxi) and 8.4 (H. griseus) times body weight. As part of the impulse generated does not translate into leaping distance but is used to deform the pole, greater effort is required to reach a given target substrate, and, consequently, takeoff forces are high. The landing forces, on the other hand, are damped by the pole/substrate yield that increases the time available for deceleration. Our results contrast with previous studies of leaping forces recorded with rigid platform measuring systems that usually report higher landing than takeoff forces. We conclude that 1) Leapers generate and are exposed to exceptionally high locomotory forces. The takeoff forces are higher than the landing forces when using compliant supports, indicating that the takeoff rather than the landing may be critical in interpreting leaping behavior and related aspects of musculoskeletal design. 2) Large-bodied vertical clingers and leapers do not usually take advantage of the elastic energy stored in substrates. Rather, force (and energy) is wasted to deform compliant supports. 3) A compliant force pole approximates the conditions faced by large-bodied vertical clingers and leapers in the wild more closely than do rigid force platforms.

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A quantitative analysis that employs randomization methods and distance statistics has been undertaken in an attempt to clarify the taxonomic affinities of the partial Homo cranium (SK 847) from Member 1 of the Swartkrans Formation. Although SK 847 has been argued to represent early H. erectus, exact randomization tests reveal that the magnitude of differences between it and two crania that have been attributed to that taxon (KNM-ER 3733 and KNM-WT 15000) is highly unlikely to be encountered in a modern human sample drawn from eastern and southern Africa. Some of the variables that differentiate SK 847 from the two early H. erectus crania (e.g., nasal breadth, frontal breadth, mastoid process size) have been considered to be relevant characters in the definition of that taxon. Just as the significant differences between SK 847 and the two early H. erectus crania make attribution of the Swartkrans specimen to that taxon unlikely, the linkage of SK 847 to KNM-ER 1813, and especially Stw 53, suggests that the Swartkrans cranium may have its closest affinity with H. habilis sensu lato. Differences from KNM-ER 1813, however, hint that the South African fossils may represent a species of early Homo that has not been sampled in the Plio-Pleistocene of eastern Africa. The similarity of SK 847 and Stw 53 may support faunal evidence which suggests that Sterkfontein Member 5 and Swartkrans Member 1 are of similar geochronological age.

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Considerable debate has surrounded the adaptive significance of Neandertal craniofacial morphology. Numerous unique morphological features of this form have been interpreted as indicating an adaptation to intense anterior tooth use. Conversely, it has been argued that certain features related to muscle position imply a reduced mechanical advantage for producing bite forces on the incisors and canines. In this study, hypotheses about morphological specializations for anterior tooth use have been derived from a biomechanical model of Greaves (1978). These hypotheses were tested by performing separate pairwise comparisons of Neandertals and early Homo sapiens, and Inuits and Native Americans from Utah. Inuits are known to have produced repeated and high magnitude forces on their anterior dentition and therefore serve as a good model for a hominid adapted to intensive anterior tooth use. Biomechanically relevant dimensions of the masticatory system were measured using a computer-driven video analysis system and compared between the two taxa in each comparison. The results of this study reveal a number of similarities between the morphological specializations exhibited by Neandertals and Inuits that can be related to intensified anterior tooth use. The hypothesis that Neandertals were poorly designed for producing masticatory forces is rejected. Specializations that differ between the two groups are interpreted as being the result of differential functional demands placed on the postcanine dentition in Neandertals and Inuits. It is suggested that many of the unique morphological features of the Neandertal face are a response to intensified use of the anterior dentition and the need to retain a sufficiently large postcanine occlusal area necessary for a relatively high attrition diet.

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The geometry of the midshaft cross-sections of the femur and humerus of five indriid species was analysed. Internal (marrow cavity) and external diameters were measured on X-rays in the anteroposterior (a-p) and mediolateral (m-l) planes; cross-sectional areas, second moments of area, and section moduli were calculated using formulae for a hollow ellipse. Cortical thickness, robusticity indices (relating external diameters to the length of the bones), and a-p/m-l shape variables were also calculated. Model II regression was supplemented by analyses of correlation between size and shape. Indriids are saltatory, i.e., their locomotion is dominated by the hind limbs. Accordingly, the femur is more rigid than the humerus, and it shows a consistent difference between the a-p and m-l planes in measures related to bending strength. Cortical thickness varies considerably both within and across species. The type specimen of the new species Propithecus tattersalli is virtually indistinguishable from P. verreauxi on the basis of its long bone cross-sectional geometry. Femoral robusticity is uncorrelated with size, but humeral robusticity decreases significantly with increasing size. Femoral shape variables (a-p/m-l) are all negatively correlated with body size, indicating that m-l dimensions of the femur increase at a faster rate than do a-p dimensions. The highly loaded plane of movement seems to be more reinforced in the smaller species. Contrary to static biomechanical scaling predictions of positive allometry, all cross-sectional parameters scale relatively close to isometry. It is concluded that either changes in locomotor performance must compensate for the weight-related increase in forces and moments or that the larger-bodied animals operate appreciably closer to the limits of their safety margins.

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Leaping primates often assume a horizontal position while airborne. When the limbs are spread out in such maneuvers, skin folds between the upper limbs and the trunk are exposed. This has led to the assumption that the animals make use of aerodynamic forces for either gliding, steering, or braking before the landing. In terms of physics, aerodynamic lift or aerodynamic drag can cause the described effects. As coefficients of lift and drag are unknown for flying primates, we have calculated those values that give the animals either a 5% gain or loss in leaping distance. These turn out to be in the range of values for cylinder-shaped "blunt" (unstreamlined) bodies. A significant influence of aerodynamic forces on the flight path can therefore be assumed. The smaller-bodied species (e.g., galagos) are more strongly influenced by their great surface areas. Although frontal areas scale positively allometrically with respect to body mass, air speed gains importance in the larger-bodied species (e.g., sifakas). They cover absolutely greater distances and have the higher takeoff velocities. The actual importance of lift and drag cannot be derived from our theoretical calculations but must be determined experimentally.

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Body size has a dominant influence on locomotor performance and the morphology of the locomotor apparatus. In locomotion under the influence of gravity, body mass acts as weight force and is a mechanical variable. Accordingly, the application of biomechanical principles and methods allows a functional understanding of scaling effects in locomotion. This is demonstrated here using leaping primates as an example. With increasing body size, the decreasing ratio of muscle force available for acceleration during takeoff to the body mass that has to be accelerated dictates both the movement pattern and the proportions of the hindlimbs. In an arm-swinging movement, the long, heavy arms of the large-bodied leapers are effectively used to gain additional momentum. A new perspective on decreasing size identifies the absolutely small acceleration distance and time available for propulsion as factors limiting leaping distance and extensively determining locomotor behavior and body proportions. As the mechanical constraints differ according to body size for a given mode of locomotion, a typological approach to morphology in relation to locomotor category is ruled out. Across locomotor categories, dynamic similarity (sensu Alexander) can be expected if the propulsive mechanisms as well as the selective pressures acting upon locomotion are the same.

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How does body size determine the locomotor performance and proportions of leapers? In an analysis of the mechanics of leaping we derived two principles that explain the kinematic and morphological differences between leaping prosimian primates of different body size. 1. In small animals, the distance through which the body can be accelerated during take-off, and the time available for acceleration, are short. In small-bodied leapers we therefore find adaptations that increase the distance or length of time for propulsion and maximize speed. These are: great angular excursions at the joints of the hindlimb, long load arms of body weight and short power arms for the muscles, elongated hindlimbs with a disproportionate lengthening of the distal segments, and additional joints in the tarsus. 2. With increasing body size, the time for accelerating the body is no longer a problem. Instead, the ratio of muscle force available for acceleration to mass to be accelerated is unfavorable. Accordingly, large-bodied leapers have adaptations that allow optimal use of available muscle force. These include: acceleration in energetically profitable joint positions, avoidance of acute joint angles especially at the distal joints (where the muscles work against the highest percentage of body mass), only moderate elongation of the hindlimbs with rather short distal segments, and long lever arms of those muscles that extend the hindlimb joints. In addition, take-offs of the larger-bodied leapers are characterized by a regularly occurring arm swing movement, thus making additional use of nonhindlimb muscles for acceleration. The mass-dependent differences in forces and velocities have consequences for the energy budget. As the muscles of the small species must contract very rapidly against high loads, they consume more energy per unit of mechanical work. It is not possible to optimize speed and force in the same animal. Body size in conjunction with the laws of mechanics determines how maximum leaping potential will be realized.

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The external dimensions of the limb bones and the geometry of their midshaft cross-sections were determined for Loris tardigradus and Nycticebus coucang. Relative cortical thickness, cortical area, and second moment of area were calculated and contrasted with locomotor stresses. The difference in shape-related strength of the bones between the smaller- and the larger-bodied species is more pronounced than can be expected from stresses acting during normal locomotion. The Nycticebus skeleton has a much higher safety margin overall and seems to be dimensioned for infrequent but critical stresses of high magnitude. Lorisine gaits in general are characterized by low ground reaction forces, great mobility in all joints, and a nearly equal share in propulsion and weight-bearing by the fore- and hindlimb. Accordingly, the long bones of lorises (especially those of L. tardigradus) tend to be less rigid than those of other mammalian species (including other primates), they lack a preferential plane of higher bending strength, and femur and humerus do not differ markedly in their capacity to withstand mechanical stresses. External dimensions of the humerus and femur of the two African lorisine species parallel and corroborate these results. Some more general implications for the relationships between bone shape and locomotor stresses are also discussed.

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