Articular to diaphyseal proportions of human and great ape metatarsals

This study proposes a new way to use metatarsals to identify locomotor behavior of fossil hominins. Metatarsal head articular dimensions and diaphyseal strength in a sample of chimpanzees, gorillas, orangutans, and humans (n = 76) are used to explore the relationships of these parameters with different locomotor modes. Results show that ratios between metatarsal head articular proportions and diaphyseal strength of the hallucal and fifth metatarsal discriminate among extant great apes and humans based on their different locomotor modes. In particular, the hallucal and fifth metatarsal characteristics of humans are functionally related to the different ranges of motion and load patterns during stance phase in the forefoot of humans in bipedal locomotion. This method may be applicable to isolated fossil hominin metatarsals to provide new information relevant to debates regarding the evolution of human bipedal locomotion. The second to fourth metatarsals are not useful in distinguishing among hominoids. Further studies should concentrate on measuring other important qualitative and quantitative differences in the shape of the metatarsal head of hominoids that are not reflected in simple geometric reconstructions of the articulation, and gathering more forefoot kinematic data on great apes to better understand differences in range of motion and loading patterns of the metatarsals. Am J Phys Anthropol 143:198–207, 2010. © 2010 Wiley‐Liss, Inc.     

The locomotion of Babakotia radofilai inferred from epiphyseal and diaphyseal morphology of the humerus and femur

Palaeopropithecids, or “sloth lemurs,” are a diverse clade of large‐bodied Malagasy subfossil primates characterized by their inferred suspensory positional behavior. The most recently discovered genus of the palaeopropithecids is Babakotia, and it has been described as more arboreal than Mesopropithecus, but less than Palaeopropithecus. In this article, the within‐bone and between‐bones articular and cross‐sectional diaphyseal proportions of the humerus and femur of Babakotia were compared to extant lemurs, Mesopropithecus and Palaeopropithecus in order to further understand its arboreal adaptations. Additionally, a sample of apes and sloths (Choloepus and Bradypus) are included as functional outgroups composed of suspensory adapted primates and non‐primates. Results show that Babakotia and Mesopropithecus both have high humeral/femoral shaft strength proportions, similar to extant great apes and sloths and indicative of forelimb suspensory behavior, with Babakotia more extreme in this regard. All three subfossil taxa have relatively large femoral heads, also associated with suspension in modern taxa. However, Babakotia and Mesopropithecus (but not Palaeopropithecus) have relatively small femoral head surface area to shaft strength proportions suggesting that hind‐limb positioning in these taxa during climbing and other behaviors was different than in extant great apes, involving less mobility. Knee and humeral articular dimensions relative to shaft strengths are small in Babakotia and Mesopropithecus, similar to those found in modern sloths and divergent from those in extant great apes and lemurs, suggesting more sloth‐like use of these joints during locomotion. Mesopropithecus and Babakotia are more similar to Choloepus in humerofemoral head and length proportions while Palaeopropithecus is more similar to Bradypus. These results provide further evidence of the suspensory adaptations of Babakotia and further highlight similarities to both extant suspensory primates and non‐primate slow arboreal climbers and hangers. J. Morphol. 277:1199–1218, 2016. © 2016 Wiley Periodicals, Inc.     

Modeling and remodeling responses to normal loading in the human lower limb

Limb bones are designed to be strong enough to support the body and yet be energetically conservative during locomotion. Bones of the distal segment, which are relatively costly to move, are often more slender than bones of the proximal segments, even though they must sustain proportionally greater loads. As a result, they are expected to experience a higher incidence of microdamage. With this constraint in mind, Lieberman and Crompton (1998 Principles of Animal Design, Cambridge: Cambridge University Press, p. 78-86) proposed that bones response to strain varies along the proximo-distal axis of the limb. In order to avoid fatigue fractures due to the accumulation of microdamage, the distal segment, in comparison to the proximal segment, will have an increase in remodeling events to replace damaged bone. In this paper, we test the hypothesis of Lieberman and Crompton (1998) with respect to the human lower limb. With a sample of adult individuals, we compare tibiae and femora for mid-diaphyseal cross-sectional geometry and Haversian remodeling differences. Our results indicate that the human limb is not designed like that of quadrupedal cursorial animals. The tibia is not less resistant in bending and torsion, and does not remodel more than the femur. Our findings fail to support the hypothesis of Lieberman and Crompton (1998) and suggest, instead, that the human lower limb is not designed like a cursorial animal limb. In addition, our results support previous observations that remodeling is not uniform within the cross section of a bone, probably a reflection of different loading histories within the different regions of the cross section.     

In vivo bone strain and bone functional adaptation

Mechanistic interpretations of bone cross-sectional shapes are based on the paradigm of shape optimization such that bone offers maximum mechanical resistance with a minimum of material. Recent in vivo strain studies (Demes et al., Am J Phys Anthropol 106 (1998) 87-100, Am J Phys Anthropol 116 (2001) 257-265; Lieberman et al., Am J Phys Anthropol 123 (2004) 156-171) have questioned these interpretations by demonstrating that long bones diaphyses are not necessarily bent in planes in which they offer maximum resistance to bending. Potential limitations of these in vivo studies have been pointed out by Ruff et al. (Am J Phys Anthropol 129 (2006) 484-498). It is demonstrated here that two loading scenarios, asymmetric bending and buckling, would indeed not lead to correct predictions of loads from strain. It is also shown that buckling is of limited relevance for many primate long bones. This challenges a widely held view that circular bone cross sections make loading directions unpredictable for bones which is based on a buckling load model. Asymmetric bending is a potentially confounding factor for bones with directional differences in principal area moments (I(max) > I(min)). Mathematical corrections are available and should be applied to determine the bending axis in such cases. It is concluded that loads can be reliably extrapolated from strains. More strain studies are needed to improve our understanding of the relationships between activities, bone loading regimes associated with them, and the cross-sectional geometry of bones.     

Hunter-gatherer postcranial robusticity relative to patterns of mobility, climatic adaptation, and selection for tissue economy

Human skeletal robusticity is influenced by a number of factors, including habitual behavior, climate, and physique. Conflicting evidence as to the relative importance of these factors complicates our ability to interpret variation in robusticity in the past. It remains unclear how the pattern of robusticity in the skeleton relates to adaptive constraints on skeletal morphology. This study investigates variation in robusticity in claviculae, humeri, ulnae, femora, and tibiae among human foragers, relative to climate and habitual behavior. Cross-sectional geometric properties of the diaphyses are compared among hunter-gatherers from southern Africa (n = 83), the Andaman Islands (n = 32), Tierra del Fuego (n = 34), and the Great Lakes region (n = 15). The robusticity of both proximal and distal limb segments correlates negatively with climate and positively with patterns of terrestrial and marine mobility among these groups. However, the relative correspondence between robusticity and these factors varies throughout the body. In the lower limb, partial correlations between polar second moment of area (J(0.73)) and climate decrease from proximal to distal section locations, while this relationship increases from proximal to distal in the upper limb. Patterns of correlation between robusticity and mobility, either terrestrial or marine, generally increase from proximal to distal in the lower and upper limbs, respectively. This suggests that there may be a stronger relationship between observed patterns of diaphyseal hypertrophy and behavioral differences between populations in distal elements. Despite this trend, strength circularity indices at the femoral midshaft show the strongest correspondence with terrestrial mobility, particularly among males.     

Regional variation in the postcranial robusticity of late Upper Paleolithic humans

Early modern humans from the European Upper Paleolithic (UP) demonstrate trends in postcranial biomechanical features that coincide with the last glacial maximum (LGM). These features have been interpreted as evidence that ecological changes of the LGM played a critical role in cultural and biological adaptation in European UP populations. In areas outside of Europe, similar environmental changes occurred with the LGM. This analysis introduces postcranial material from the Late Upper Paleolithic (LUP) of North Africa and Southeast Asia and tests two related hypotheses: 1) LUP samples across the Old World had similar patterns of postcranial robusticity and 2) relative to an available Early Upper Paleolithic (EUP) sample, regional LUP samples demonstrate similar trends in robusticity that may be attributable to climatic effects of the LGM. Cross-sectional geometric data of the humeri and femora were obtained for 26 EUP and 100 LUP humans from Europe, Africa, and Asia. Despite regional differences, LUP samples are similar relative to the EUP sample. In the humerus, bilateral asymmetry decreases in all LUP samples relative to the EUP sample. In the femur, LUP samples demonstrate increasingly circular femoral midshaft sections, reflecting reduced anteroposterior bending strength relative to the EUP sample. These patterns suggest changes in subsistence behavior and mobility after the LGM across the Old World that are most consistent with reduced mobility and broad-spectrum resource exploitation.     

Predicting long bone loading from cross-sectional geometry

Long bone loading histories are commonly evaluated using a beam model by calculating cross-sectional second moments of areas (SMAs). Without in vivo strain data, SMA analyses commonly make two explicit or implicit assumptions. First, while it has long been known that axial compression superimposed on bending shifts neutral axes away from cross-sectional area centroids, most analyses assume that cross-sectional properties calculated through the area centroid approximate cross-sectional strength. Second, the orientation of maximum bending rigidity is often assumed to reflect the orientation of peak or habitual bending forces the bone experiences. These assumptions are tested in sheep in which rosette strain gauges mounted at three locations around the tibia and metatarsal midshafts measured in vivo strains during treadmill running at 1.5 m/sec. Calculated normal strain distributions confirm that the neutral axis of bending does not run through the midshaft centroid. In these animals, orientations of the principal centroidal axes around which maximum SMAs (Imax) are calculated are not in the same planes in which the bones experienced bending. Cross-sectional properties calculated using centroidal axes have substantial differences in magnitude (up to 55%) but high correlations in pattern compared to cross-sectional properties calculated around experimentally determined neutral axes. Thus interindividual comparisons of cross-sectional properties calculated from centroidal axes may be useful in terms of pattern, but are subject to high errors in terms of absolute values. In addition, cross-sectional properties do not necessarily provide reliable data on the orientations of loads to which bones are subjected.     

Mobility and subsistence economy: a diachronic comparison between two groups settled in the same geographical area (Liguria, Italy)

The purpose of this article is to investigate temporal shifts in skeletal robusticity to infer behavioral changes in two populations (Neolithic, NEOL and Medieval, MED) settled in the same geographic area but involved in different subsistence economies (pastoralism and coastal resources exploitation). This comparison allows us to test the hypothesis that occupational stress and mobility in the same environment produce predictable changes in the robusticity of both upper and lower limbs. Results show a lower degree of humeral robusticity and a similar degree of humeral asymmetry in the two sexes in the MED population. These results are consistent with the relatively less stressful subsistence economy documented in the MED population relative to that of the NEOL. Lower limb results suggest that femoral robusticity does not correlate directly with the level of logistical mobility, but is instead due to the summation of several diverse factors that place biomechanical loads on the hindlimb, particularly unevenness of the terrain. However, female femoral gracility seems to indicate that below a certain "threshold" of mobility, i.e., movement over the natural terrain, terrain conformation is no longer the main contributing factor to femoral robusticity. The femoral shape index I(x)/I(y) declines through time, particularly in males. This agrees with the expected mobility of the samples based on archaeological and historical data, providing further evidence on the reliability of this index in inferring terrestrial mobility.     

Brief communication: The effects of disuse on the mechanical properties of bone: What unloading tells us about the adaptive nature of skeletal tissue

The intricate link between load environment and skeletal health is exemplified by the severe osteopenia that accompanies prolonged periods of immobilization, frequently referred to as disuse osteoporosis. Investigating the effects disuse has on the structural properties of bone provides a unique opportunity to better understand how mechanical loads influence the adaptation and maintenance of skeletal tissue. Here, we report results from an examination of multiple indicators of bone metabolism (e.g., mean osteon density, mean osteon size, bone mass, and bone area distribution) within the major long bones of individuals with distinct activity level differences. Results are based on a sample comprising two subjects that suffered from long‐term quadriplegia and 28 individuals of comparable age that had full limb mobility. Although limited in sample size, our findings suggest bones associated with long‐term disuse have lower osteon densities and larger osteon areas compared to individuals of normal mobility, reflecting dramatically lower remodeling rates potentially related to reduced strain levels. Moreover, immobilized skeletal elements demonstrate a reduced percentage of cortical area present resulting from endosteal resorption. Differences between mobility groups in the percentage of cortical area present and bone distribution of all skeletal elements, suggests bone modeling activity is negligible in the unloaded adult skeleton. Additional histomorphometric comparisons reveal potential intraskeletal differences in bone turnover rates suggesting remodeling rates are highest within the humeri and femora. Addition of more immobilized individuals in the future will allow for quantitative statistical analyses and greater consideration of human variation within and between individuals. Am J Phys Anthropol 2012. © 2012 Wiley Periodicals, Inc.     

Activity patterns in the Sahara Desert: an interpretation based on cross-sectional geometric properties

The Garamantian civilization flourished in modern Fezzan, Libya, between 900 BC and 500 AD, during which the aridification of the Sahara was well established. Study of the archaeological remains suggests a population successful at coping with a harsh environment of high and fluctuating temperatures and reduced water and food resources. This study explores the activity patterns of the Garamantes by means of cross-sectional geometric properties. Long bone diaphyseal shape and rigidity are compared between the Garamantes and populations from Egypt and Sudan, namely from the sites of Kerma, el-Badari, and Jebel Moya, to determine whether the Garamantian daily activities were more strenuous than those of other North African populations. Moreover, sexual dimorphism and bilateral asymmetry are assessed at an intra- and inter-population level. The inter-population comparisons showed the Garamantes not to be more robust than the comparative populations, suggesting that the daily Garamantian activities necessary for survival in the Sahara Desert did not generally impose greater loads than those of other North African populations. Sexual dimorphism and bilateral asymmetry in almost all geometric properties of the long limbs were comparatively low among the Garamantes. Only the lower limbs were significantly stronger among males than females, possibly due to higher levels of mobility associated with herding. The lack of systematic bilateral asymmetry in cross-sectional geometric properties may relate to the involvement of the population in bilaterally intensive activities or the lack of regular repetition of unilateral activities.     

Cross sectional geometry of the forelimb skeleton and flight mode in pelecaniform birds

Avian wing elements have been shown to experience both dorsoventral bending and torsional loads during flapping flight. However, not all birds use continuous flapping as a primary flight strategy. The pelecaniforms exhibit extraordinary diversity in flight mode, utilizing flapping, flap‐gliding, and soaring. Here we (1) characterize the cross‐sectional geometry of the three main wing bone (humerus, ulna, carpometacarpus), (2) use elements of beam theory to estimate resistance to loading, and (3) examine patterns of variation in hypothesized loading resistance relative to flight and diving mode in 16 species of pelecaniform birds. Patterns emerge that are common to all species, as well as some characteristics that are flight‐ and diving‐mode specific. In all birds examined, the distal most wing segment (carpometacarpus) is the most elliptical (relatively high I_max/I_min) at mid‐shaft, suggesting a shape optimized to resist bending loads in a dorsoventral direction. As primary flight feathers attach at an oblique angle relative to the long axis of the carpometacarpus, they are likely responsible for inducing bending of this element during flight. Moreover, among flight modes examined the flapping group (cormorants) exhibits more elliptical humeri and carpometacarpi than other flight modes, perhaps pertaining to the higher frequency of bending loads in these elements. The soaring birds (pelicans and gannets) exhibit wing elements with near‐circular cross‐sections and higher polar moments of area than in the flap and flap‐gliding birds, suggesting shapes optimized to offer increased resistance to torsional loads. This analysis of cross‐sectional geometry has enhanced our interpretation of how the wing elements are being loaded and ultimately how they are being used during normal activities. J. Morphol., 2011. © 2011 Wiley‐Liss,Inc.     

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.     

Functional significance of variation in bryophyte canopy structure

In most bryophytes, the thickness of boundary layers (i.e., unstirred layers) that surrounds plant surfaces governs rates of water loss. Architectural features of canopies that influence boundary layer thickness affect the water balance of bryophytes. Using field samples (9.3 cm diameter cushions) from 12 populations (11 species) of mosses and liverworts, we evaluated the relationship between canopy structure and boundary layer properties. Canopy structure was characterized using a contact surface probe to measure canopy depth along perpendicular transects at spatial scales ranging from 0.8 to 30 mm on 186 points per sample. Semivariance in depth measurements at different spatial scales was used to estimate three architectural properties: surface roughness (L(r)), the scale of roughness elements (S(r)), and fine-scale surface texture, the latter characterized by the fractal dimension (D) of the canopy profile. Boundary layer properties were assessed by evaporation of ethanol from samples in a wind-tunnel at wind speeds from 0.6 to 4.2 m/s and applied to characterize mass transfer using principles of dynamic similarity (i.e., using dimensionless representations of conductance and flow). In addition, particle image velocimetry (PIV) was used to visualize and quantify flow over two species. All cushions exhibited the characteristics of turbulent as opposed to laminar boundary layers, and conductance increased with surface roughness. Bryophyte canopies with higher L(r) had greater conductances at all wind speeds. Particle image velocimetry analysis verified that roughness elements interacted with flow and caused turbulent eddies to enter canopies, enhancing evaporation. All three morphological features were significantly associated with evaporation. When L(r), S(r), and D were incorporated with a flow parameter into a conductance model using multiple linear regression, the model accounted for 91% of the variation in mass transfer.     

Periosteal versus true cross‐sectional geometry: A comparison along humeral,femoral, and tibial diaphyses

Cross‐sectional geometric (CSG) properties of human long bone diaphyses are typically calculated from both periosteal and endosteal contours. Though quantification of both is desirable, periosteal contours alone have provided accurate predictions of CSG properties at the midshaft in previous studies. The relationship between CSG properties calculated from external contours and “true” (endosteal and periosteal) CSG properties, however, has yet to be examined along the whole diaphysis. Cross‐sectional computed tomography scans were taken from 21 locations along humeral, femoral, and tibial diaphyses in 20 adults from a late prehistoric central Illinois Valley cemetery. Mechanical properties calculated from images with (a) artificially filled medullary cavities (“solid”) and (b) true unaltered cross‐sections were compared at each section location using least squares regression. Results indicate that, in this sample, polar second moments of area (J), polar section moduli (Z_p), and cross‐sectional shape (I_max/I_min) calculated from periosteal contours correspond strongly with those calculated from cross‐sections that include the medullary cavity. Correlations are high throughout most of the humeral diaphysis and throughout large portions of femoral and tibial diaphyses (R² = 0.855–0.998, all P < 0.001, %SEE ≤ 8.0, %PE ≤ 5.0), the major exception being the proximal quarter of the tibial diaphysis for J and Z_p. The main source of error was identified as variation in %CA. Results reveal that CSG properties quantified from periosteal contours provide comparable results to (and are likely to detect the same differences among individuals as) true CSG properties along large portions of long bone diaphyses. Am J Phys Anthropol, 2013. © 2013 Wiley Periodicals, Inc.     

Linking structural variability in long bone diaphyses to habitual behaviors: foragers from the southern African Later Stone Age and the Andaman Islands

The cross-sectional distribution of cortical bone in long bone diaphyses is highly responsive to mechanical loading during life, yet the relationship between systemic and localized influences on skeletal structure remains unclear. This study investigates postcranial robustness throughout the body among adults from two groups of foragers with different patterns and modes of mobility, to determine whether there is evidence for upper vs. lower body localization of skeletal robustness. The samples used for this comparison are from the southern African Later Stone Age (LSA; n = 65, male = 33, female = 28) dating from ca. 10,000 to 2,000 B.P., and 19th century indigenous Andaman Islanders (AI; n = 36, male = 17, female = 16). The LSA were highly mobile foragers who did not exploit offshore marine resources. In contrast, the AI had tightly constrained terrestrial, but significant marine, mobility. Geometric properties of cortical bone distribution in the diaphyses of the clavicle, humerus, femur, tibia, and first metatarsal are compared between the samples, providing a representation of skeletal robustness throughout the body. Multivariate ANOVA shows the AI to have significantly stronger clavicles and humeri, while the LSA femora, tibiae, and first metatarsals are stronger than those of the AI. These patterns, in which upper and lower limbs show biomechanical properties that are consistent with habitual behaviors, suggest localized osteogenic response. Although postcranial robustness appears to be correlated with overall limb function, the results suggest that more proximal elements within the limb may be more responsive to mechanical loading.