Structural adaptations of the femur and humerus to arboreal and terrestrial environments in three species of macaque

One reason to measure cross-sectional structural properties of primate long bones is to define mechanically relevant complexes of traits that describe the adaptation of bone to different biomechanical environments. This can be effectively accomplished when congeneric species having different postural and locomotor behaviors are compared. This paper compares the cross-sectional geometry of the femur and humerus in three behaviorally different macaque species as a basis for defining such patterns. Cross-sectional moments of inertia in the standard anatomical planes were calculated at five locations along the diaphyses of the femur and humerus in Macaca fascicularis, M. nemestrina, and M. mulatta. The data suggest that the "barrel-shaped" femur is associated with behaviors for which long limbs and small body size are an asset. This may be associated with, but is not restricted to, leaping behaviors. The data also suggest that structural rigidity of the femur and humerus is greater per unit body weight in primates that spend significant amounts of time in terrestrial environments than in those that are more restricted to climbing in arboreal environments.     

Skeletal allometry and interlimb scaling patterns in mustelid carnivorans

To address the effects of an evolutionary increase in body size on long bone skeletal allometry, scaling patterns relating body mass, bone length, limb length, midshaft diameters, and cross-sectional properties of the humerus and femur were analyzed for four species of scansorial mustelids. Humeral and, to a lesser extent, femoral allometry is consistent with expectations of elastic similarity: bone and limb length scale with negative allometry on body mass while bone robusticity (cross-sectional parameters against bone length) scales with strong positive allometry. Differences between fore- and hindlimb scaling patterns, however, are observed, with size-dependent increases in forelimb length and humeral strength and robusticity exceeding those of the hindlimb and femur. It is hypothesized that this greater fore- than hindlimb lengthening results in postural modifications that serve to straighten the hindlimb of larger bodied scansorial mustelids relative to smaller mustelids. Straightening of hindlimb joints would more precisely align the long axis of the femur with peak (vertical) ground reaction forces, thereby accounting for the reduction in relative bending stresses acting on the femur compared to the humerus. J. Morphol. 235:121–134, 1998. © 1998 Wiley-Liss, Inc.     

Which measures of diaphyseal robusticity are robust? A comparison of external methods of quantifying the strength of long bone diaphyses to cross‐sectional geometric properties

Measures of diaphyseal robusticity have commonly been used to investigate differences in bone strength related to body size, behavior, climate, and other factors. The most common methods of quantifying robusticity involve external diameters, or cross-sectional geometry. The data derived from these different methods are often used to address similar research questions, yet the compatibility of the resulting data has not been thoroughly tested. This study provides the first systematic comparison of externally derived measures of postcranial robusticity, with those based upon cross-sectional geometry. It includes sections taken throughout the skeleton, comparisons of prediction errors associated with different measurements, and analysis of the implications of different methods of body size standardization on the prediction of relative bone strength. While the results show reasonable correlations between diaphyseal diameters and strengths derived from cross-sectional geometry, considerable prediction errors are found in many cases. A new approach to externally based quantification of diaphyseal robusticity based upon moulding of sub-periosteal contours is proposed. This method maximizes correlation with cross-sectional geometry (r(2) = .998) and minimizes prediction errors in all cases. The results underscore the importance of accurate periosteal measurement in the quantification of bone strength, and suggest that, regardless of theoretical scaling predictions, external area based robusticity estimates involving the product of diaphyseal diameters are most directly comparable to cross-sectional geometric properties when they are standardized using the product of body mass and bone length.     

Primate limb bones and locomotor types in arboreal or terrestrial environments

Postcranial limb bones were compared among primates of different locomotor types. Seventy-one primate species, in which all families of primates were included, were grouped into nine locomotor types. Osteometrical data on long bones and data on the cross-sectional geometry of the humerus and the femur were studied by means of allometric analysis and principal component analysis. Relatively robust forelimb bones were observed in the primate group which adopted the relatively terrestrial locomotor type compared with the group that adopted the arboreal locomotor type. The difference resembled the previously reported comparison between terrestrial and arboreal groups among all quadrupedal mammals. The degree of arboreality in daily life is connected with the degree of hindlimb dominance, or the ratio of force applied to the fore- and hindlimb in positional behaviour and also with the shape, size and robusticity of limb bones.     

Functional differentiation of long bones in lorises

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.     

Estrogen, exercise, and the skeleton

Patterns of variation in bone size and shape provide crucial data for reconstructing hominin paleobiology, including ecogeographic adaptation, life history, and functional morphology. Measures of bone strength, including robusticity (diaphyseal thickness relative to length) and cross-sectional geometric properties such as moments of area, are particularly useful for inferring behavior because bone tissue adapts to its mechanical environment. Particularly during skeletal growth, exercise-induced strains can stimulate periosteal modeling so that, to some extent, bone thickness reflects individual behavior. Thus, patterns of skeletal robusticity have been used to identify gender-based activity differences, temporal shifts in mobility, and changing subsistence strategies. Although there is no doubt that mechanical loading leaves its mark on the skeleton, less is known about whether individuals differ in their skeletal responses to exercise. For example, the potential effects of hormones or growth factors on bone-strain interactions are largely unexplored. If the hormonal background can increase or decrease the effects of exercise on skeletal robusticity, then the same mechanical loads might cause different degrees of bone response in different individuals. Here I focus on the role of the hormone estrogen in modulating exercise-induced changes in human bone thickness.     

Biomechanical approach to the reconstruction of activity patterns in Neolithic Western Liguria, Italy

This paper investigates the changes in upper and lower limb robusticity and activity patterns that accompanied the transition to a Neolithic subsistence in western Liguria (Italy). Diaphyseal robusticity measures were obtained from cross-sectional geometric properties of the humerus and femur in a sample of 16 individuals (eight males and eight females) dated to about 6,000-5,500 BP. Comparisons with European Late Upper Paleolithics (LUP) indicate increased humeral robusticity in Neolithic Ligurian (NEOL) males, but not in females, with a significant reduction in right-left differences in both sexes. Sexual dimorphism in robusticity increases in upper and lower limb bones. Regarding the femur, while all female indicators of bending strength decrease steadily through time, values for NEOL males approach those of LUP. This suggests high, and unexpected, levels of mechanical stress for NEOL males, probably reflecting the effects of the mountainous terrain on lower limb remodeling. Comparisons between NEOL males and a small sample of LUP hunter-gatherers from the same area support this interpretation. In conclusion, cross-sectional geometry data indicate that the transition to Neolithic economies in western Liguria did not reduce functional requirements in males, and suggest a marked sexual division of labor involving a more symmetrical use of the upper limb, and different male-female levels of locomotory stress. When articulated with archaeological, faunal, paleopathological, and ethnographic evidence, these results support the hypothesis of repetitive, bimanual use of axes tied to pastoral activities in males, and of more sedentary tasks linked to agriculture in females.     

The mandibular corpus of female primates: taxonomic, dietary, and allometric correlates of interspecific variations in size and shape

Measurements were taken on skulls of 253 adult female anthropoid primates from 32 species, in order to determine patterns and possible causes for variation among species in the cross-sectional size and shape of the mandibular corpus under M1. When all 32 species are considered as a group, there is a tendency for corpus shape to become more robust with increasing body size. However, this does not hold for colobines or cercopithecines evaluated separately. When diets are classified into the general categories of folivory or frugivory, neither size-adjusted measurements of mandibular corpus breadth and height, nor estimates of the second moments of inertia or the polar moment of inertia of the mandibular cross section, show any relationship to dietary variation among species. Species reported to include hard nuts in their diets have larger mandibular cross sections than other species, and the size of the corpus is significantly correlated with size of the dentition and molar enamel thickness. A biomechanical model taking into account frictional effects of tooth-to-tooth contact indicates that mandibular corpus robusticity may not be related to a large horizontal component of force during mastication.     

Allometric patterning in the limb skeleton of bats: Implications for the mechanics and energetics of powered flight

Allometric analysis was employed to compare linear dimensions of forelimb and hindlimb bones (humeri, radii, third and fifth metacarpals, third and fifth manual phalanges, femora, and tibiae) of 227 species of bats and 105 species of nonvolant mammals of varying degrees of phylogenetic affinity to bats. After accounting for body size, all forelimb bones are longer in bats than in nonvolant species, with the exception of humeri and radii of a few highly arboreal primates. Hindlimb bones are generally, but not uniformly, shorter in bats than in other mammals. For the humerus, radius, and metacarpals, midshaft diameters are greater in bats than in their comparably sized relatives. Proximal phalangeal midshaft diameters are statistically indistinguishable from those of other mammals, and distal phalanges show significantly reduced outer diameters. The pattern of relative reduction in wing bone diameters along the wing's proximodistal axis parallels the reduction in bone mineralization along the same axis, and a similar pattern of change in cortical thickness from the smallest wall thicknesses among mammals in the humerus and radius to the greatest wall thicknesses among mammals in the phalanges. The combination of altered cross-sectional geometry and mineralization appears significantly to reduce the mass moment of inertia of the bat wing relative to a theoretical condition in which elongated bones preserve primitive mammalian mineralization levels and patterns of scaling of long bone diameters. This intercorrelated suite of skeletal specializations may significantly reduce the inertial power of flight, contributing significant energetic savings to the total energy budgets of the only flying mammals. J. Morphol. 234: 277–294, 1997. © 1997 Wiley-Liss, Inc.     

Differentiation between fore- and hindlimb bones and locomotor behaviour in primates

Primate appendicular limb bones were measured on the cross-sectional geometry at the mid-length of the humerus and femur and on the external dimensions of long bones of the same individuals. Cross sections were directly measured by means of computer tomography or direct sectioning. The morphometry of bones and locomotor behaviour is discussed from the viewpoint of the functional differentiation between the fore- and hindlimbs. The primate group which daily adopted a relatively terrestrial locomotor type demonstrates robust forelimb bones compared with the group which adopted a fully arboreal locomotor type. In contrast, the arboreal group showed relatively large and long hindlimb bones. The difference resembled the previously reported comparison between terrestrial and arboreal groups among wholly quadrupedal mammals. Humans were more similar to the arboreal group than to the terrestrial group. Parameters of the cross-sectional geometry showed a slightly positive allometry in total primate species. Slopes of the parameters were explained by the influence of muscle force.     

Cranial muscle markers: A preliminary examination of size, sex, and age effects

Most muscle marker research consists of post-cranial analyses, but some researchers examine crania to reconstruct activities. Regardless of bones examined, anthropologists know of some of the complexities surrounding muscle marker development. Here, posterior cranial muscle markers are analyzed to determine whether they are useful in reconstructing activities by examining effects that may hinder reconstructions. Additionally, upper limb muscle markers and humeral cross-sectional robusticity variables are correlated with cranial muscle markers to determine if robust individuals are generally robust due to the synergistic effects of muscle use.Cranial muscle markers of 65 prehistoric California Amerinds are scored using a five-point observer rating scale. Body mass is calculated from femoral head size; maximum cranial length and breadth are measured with a spreading caliper; and age and sex are determined through standard procedures. Upper limb muscle markers are scored on seven sites using two dimensions within a seven-point scale. Cross-sectional properties are calculated from biplanar humeral radiographs. Aggregates are created for cranial muscle markers, upper limb muscle markers, and cross-sectional robusticity.Cranial muscle markers correlate significantly with cranial length, r=0.25 and cross-sectional robusticity of humerus, r=0.29; P’s<0.05. All variables differed between sexes (Mann-Whitney=31.00-307.50, P’s<0.01). Results imply that some differences in cranial muscle markers are related to size; however, individuals with well-developed cranial muscle markers have greater upper limb robusticity possibly due to activity patterns. Sex differences remained after size controls and may relate to activity differences.     

The variation of the cross-sectional shape in the long bones of birds and mammals

The transverse and sagittal diameters of the long bones were measured in a sample of 53 species of eutherian mammals and 36 species of birds. The scaling of the transverse and sagittal diameters of each bone to body mass was calculated. For each bone the ratio of sagittal/transverse diameter was calculated, as an expression of the cross-sectional shape of the bones. The distributions of the ratios were not significantly different from normality in all the avian bones and in the mammalian femur and tibia. In most cases, the mean of the distribution was significantly different from 1 (circular shape). The analysis shows that changes in the ratio can be caused by selective factors, considering the correlation predicted between the breaking moments and the radii, but at the same time the cross-sectional shape of mammalian and avian long bones may have a phylogenetic basis. Finally, the previous assumption of relationship between bone curvature and stress predictability, is also discussed.     

辽宁建平古人类肱骨形态结构分析

1957年,在辽宁省建平县发现了一根古人类肱骨化石,编号PA103。通过同一批龙骨中筛选的哺乳动物化石,吴汝康推断PA103应该为更新世晚期古人类,并对该化石进行了表面形态特征观察和描述。为了对PA103化石的内外结构进行更全面的了解,除了线性测量数据的对比,本文还通过计算机断层扫描技术,结合生物力学和形态示量图分析对建平古人类右侧肱骨化石PA103进行了分析。通过本研究发现,PA103骨干横断面的生物力学粗壮度和力学形状指数明显小于尼安德特人,而与同时期欧亚大陆古人类不利手侧最为接近,这说明建平人右侧肱骨可能不是惯用手,同时,建平人的行为活动应该与同时期同地区的古人类处于同一水平,而小于尼安德特人。整体来看,PA103骨干骨密质厚度和截面惯性矩与近现代人的分布模式较为接近,除局部数值增大外,其整体数值小于近现代人的平均水平,这可能与遗传或行为活动有关,由于缺少古人类化石对比数据,更详细的了解还需后期开展更多相关的研究。     

Postcranial robusticity in Homo. I: Temporal trends and mechanical interpretation

Temporal trends in postcranial robusticity within the genus Homo are explored by comparing cross-sectional diaphyseal and articular properties of the femur, and to a more limited extent, the humerus, in samples of Recent and earlier Homo. Using both theoretical mechanical models and empirical observations within Recent humans, scaling relationships between structural properties and bone length are developed. The influence of body shape on these relationships is considered. These scaling factors are then used to standardize structural properties for comparisons with pre-Recent Homo (Homo sp. and H. erectus, archaic H. sapiens, and early modern H. sapiens). Results of the comparisons lead to the following conclusions: 1) There has been a consistent, exponentially increasing decline in diaphyseal robusticity within Homo that has continued from the early Pleistocene through living humans. Early modern H. sapiens are closer in shaft robusticity to archaic H. sapiens than they are to Recent humans. The increase in diaphyseal robusticity in earlier Homo is a result of both medullary contraction and periosteal expansion relative to Recent humans. 2) There has been no similar temporal decline in articular robusticity within Homo–relative femoral head size is similar in all groups and time periods. Thus, articular to shaft proportions are different in pre-Recent and Recent Homo. 3) These findings are most consistent with a mechanical explanation (declining mechanical loading of the postcranium), that acted primarily through developmental rather than genetic means. The environmental (behavioral) factors that brought about the decline in postcranial robusticity in Homo are ultimately linked to increases in brain size and cultural-technological advances, although changes in robusticity lag behind changes in cognitive capabilities. © 1993 Wiley-Liss, Inc.     

Microstructure and Cross-Sectional Shape of Limb Bones in Great Horned Owls and Red-Tailed Hawks: How Do These Features Relate to Differences in Flight and Hunting Behavior?

The Red-tailed Hawk and Great Horned Owl are two species of raptor that are similar in body size, diet, and habitat. Both species use their hindlimbs during hunting, but differ in foot morphology, how they approach and immobilize prey, and the average size of prey captured. They also differ in primary flight style: the Red-tailed Hawk uses static soaring and the Great Horned Owl uses flap-gliding. The objectives of this study were to characterize the microstructure and cross-sectional shape of limb bones of these species and examine the relationship with flight and hunting behaviors. The mid-shaft of six limb bones from six individuals of each species was sampled. The degree of bone laminarity (proportion of circular primary vascular canals) and cross-sectional geometric parameters were calculated. In both species, the humerus and femur exhibited features that suggest high resistance to torsional loading, whereas the tibiotarsus and phalanges had a shape more likely to resist compression and bending in a specific plane. The femur of the Red-tailed Hawk exhibited higher laminarity and larger polar moment of area than that of the Great Horned Owl. The tibiotarsus was more elliptical than that of the Great Horned Owl. The hawk approaches prey from a more horizontal axis, takes prey of greater mass, and is more likely to pursue prey on the ground, which could potentially be causing more torsional loads on the femur and bending loads on the tibiotarsus. In addition, differences in polar moment of area of the phalanges between the species could relate to differences in foot morphology or digit length. The humerus and ulna of the flap-gliding Great Horned Owl are more elliptical than the static soaring Red-tailed Hawk, a shape that may better resist the bending loads associated with a larger amount of flapping.     

Biomechanics of cross-sectional size and shape in the hominoid mandibular corpus

Mandibular cross sections of Pan, Pongo, Gorilla, Homo, and two fossil specimens of Paranthropus were examined by computed tomography (CT) to determine the biomechanical properties of the hominoid mandibular corpus. Images obtained by CT reveal that while the fossil hominids do not differ significantly from extant hominoids in the relative contribution of compact bone to total subperiosteal area, the shape of the Paranthropus corpora indicates that the mechanical design of the robust australopithecine mandible is fundamentally distinct from that of modern hominoids in terms of its ability to resist transverse bending and torsion. It is also apparent that, among the modern hominoids, interspecific and sexual differences in corpus shape are not significant from a biomechanical perspective. While ellipse models have been used previously to describe the size, shape, and subsequent biomechanical properties of the corpus, the present study shows that such models do not predict the biomechanical properties of corpus cross-sectional geometry in an accurate or reliable manner. The traditional "robusticity" index of the mandibular corpus is of limited utility for biomechanical interpretations. The relationship of compact bone distribution in the corpus to dimensions such as mandibular length and arch width may provide a more functionally meaningful definition of mandibular robusticity.     

The anomalous archaic Homo femur from Berg Aukas, Namibia: a biomechanical assessment.

The probably Middle Pleistocene human femur from Berg Aukas, Namibia, when oriented anatomically and analyzed biomechanically, presents an unusual combination of morphological features compared to other Pleistocene Homo femora. Its midshaft diaphyseal shape is similar to most other archaic Homo, but its subtrochanteric shape aligns it most closely with earlier equatorial Homo femora. It has an unusually low neck shaft angle. Its relative femoral head size is matched only by Neandertals with stocky hyperarctic body proportions. Its diaphyseal robusticity is modest for a Neandertal, but reasonable compared to equatorial archaic Homo femora. Its gluteal tuberosity is relatively small. Given its derivation from a warm climatic region, it is best interpreted as having had relatively linear body proportions (affecting proximal diaphyseal proportions, shaft robusticity, and gluteal tuberosity size) combined with an elevated level of lower limb loading during development (affecting femoral head size and neck shaft angle).     

A modern human humerus from the early aurignacian of Vogelherdhöhle (Stetten, Germany)

Implicit in much of the discussion of the cultural and population biological dynamics of modern human origins in Europe is the assumption that the Aurignacian, from its very start, was made by fully modern humans. The veracity of this assumption has been challenged in recent years by the association of Neandertal skeletal remains with a possibly Aurignacian assemblage at Vindija Cave (Croatia) and the association of Neandertals with distinctly Upper Paleolithic (but non-Aurignacian) assemblages at Arcy-sur-Cure and St. C?esaire (France). Ideally we need human fossil material that can be confidently assigned to the early Aurignacian to resolve this issue, yet in reality there is a paucity of well-provenanced human fossils from early Upper Paleolithic contexts. One specimen, a right humerus from the site of Vogelherd (Germany), has been argued, based on its size, robusticity, and muscularity, to possibly represent a Neandertal in an Aurignacian context. The morphological affinities of the Vogelherd humerus were explored by univariate and multivariate comparisons of humeral epiphyseal and diaphyseal shape and strength measures relative to humeri of Neandertals and Early Upper Paleolithic (later Aurignacian and Gravettian) modern humans. On the basis of diaphyseal cross-sectional geometry, deltoid tuberosity morphology, and distal epiphyseal morphology, the specimen falls clearly and consistently with European early modern humans and not with Neandertals. Along with the other Vogelherd human remains, the Vogelherd humerus represents an unequivocal association between the Aurignacian and modern human morphology in Europe.     

Gender-specific growth patterns of transversal body dimensions in Croatian children and youth (2 to 18 years of age)

In a cross-sectional study of growth, 5,260 healthy children of both sexes from Zagreb (Croatia) aged 2 to 18 years were measured. Six transversal body dimensions were studied: biacromial, transverse chest, antero-posterior chest, biiliocristal, bicondylar humerus and bicondylar femur diamters. A significant increase in body diameters has been observed until the age of 14 to 15 in girls and until the age of 16 in boys, showing that girls have a 1 to 2 years shorter period of growth. Compared to boys of the same age, they achieved larger amounts of final transversal bone size throughout the whole growth period. The most pronounced example was the knee diameter that in girls attained 95% of adult size as early as the age of 10. In both genders, the adult size is achieved earlier in widths of the extremities than in those of the trunk. The studied transversal body segments showed different growth dynamics, which is gender-specific. While sexual dimorphism in pelvic and shoulder diameters emerged with pubertal spurt, gender differences in chest and extremities' diameters started early in life. In all ages, boys had larger chest, elbow and knee diameters. In pubertal age boys gained a significantly larger biacromial diameter (from the age of 13 onwards), while girls exceeded them in biiliocristal diameter (from 10 to 14 years). The findings of gender differences were compared to those reported for other European populations and their growth patters were discussed comparing viewpoints.     

Incidence and mechanical significance of pneumatization in the long bones of birds

The incidence of pneumatization in avian long bones was studied, by direct observation, in a large sample of species. Only proximal bones (humerus and femur) presented pneumatization in the sample studied. The incidence obtained was related to the variation of the maximum cortical thickness and mechanical properties, such as bending strength and flexural Young's modulus. Cortical thickness, bending strength and flexural Young's modulus were significantly lower in pneumatized bones than in marrow-filled bones. Furthermore, some congruence was found between pneumatization and systematic groups when compared. In this sense, Charadriformes was the only order studied with total absence of long bone pneumatization. Results on cortical thickness appear to be in agreement with modelling predictions previously made and with results obtained on other groups of flying vertebrates. The possible selective advantage of reduction in cortical thickness in relation to flying is suggested.