Trabecular architecture and joint loading of the proximal humerus in extant hominoids,Ateles, and Australopithecus africanus

Objectives

Several studies have investigated potential functional signals in the trabecular structure of the primate proximal humerus but with varied success. Here, we apply for the first time a “whole‐epiphyses” approach to analysing trabecular bone in the humeral head with the aim of providing a more holistic interpretation of trabecular variation in relation to habitual locomotor or manipulative behaviors in several extant primates and Australopithecus africanus.

Materials and methods

We use a “whole‐epiphysis” methodology in comparison to the traditional volume of interest (VOI) approach to investigate variation in trabecular structure and joint loading in the proximal humerus of extant hominoids, Ateles and A. africanus (StW 328).

Results

There are important differences in the quantification of trabecular parameters using a “whole‐epiphysis” versus a VOI‐based approach. Variation in trabecular structure across knuckle‐walking African apes, suspensory taxa, and modern humans was generally consistent with predictions of load magnitude and inferred joint posture during habitual behaviors. Higher relative trabecular bone volume and more isotropic trabeculae in StW 328 suggest A. africanus may have still used its forelimbs for arboreal locomotion.

Discussion

A whole‐epiphysis approach to analysing trabecular structure of the proximal humerus can help distinguish functional signals of joint loading across extant primates and can provide novel insight into habitual behaviors of fossil hominins.

     

Trabecular bone structure in the mandibular condyles of gouging and nongouging platyrrhine primates

The relationship between mandibular form and biomechanical function is a topic of significant interest to morphologists and paleontologists alike. Several previous studies have examined the morphology of the mandible in gouging and nongouging primates as a means of understanding the anatomical correlates of this feeding behavior. The goal of the current study was to quantify the trabecular bone structure of the mandibular condyle of gouging and nongouging primates to assess the functional morphology of the jaw in these animals. High‐resolution computed tomography scan data were collected from the mandibles of five adult common marmosets (Callithrix jacchus), saddle‐back tamarins (Saguinus fuscicollis), and squirrel monkeys (Saimiri sciureus), respectively, and various three‐dimensional morphometric parameters were measured from the condylar trabecular bone. No significant differences were found among the taxa for most trabecular bone structural features. Importantly, no mechanically significant parameters, such as bone volume fraction and degree of anisotropy, were found to vary significantly between gouging and nongouging primates. The lack of significant differences in mechanically relevant structural parameters among these three platyrrhine taxa may suggest that gouging as a habitual dietary behavior does not involve significantly higher loads on the mandibular condyle than other masticatory behaviors. Alternatively, the similarities in trabecular architecture across these three taxa may indicate that trabecular bone is relatively unimportant mechanically in the condyle of these primates and therefore is functionally uninformative. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Long bone articular and diaphyseal structure in old world monkeys and apes. I: locomotor effects

The relationship between locomotor behavior and long bone structural proportions is examined in 179 individuals and 13 species of hominoids and cercopithecoids. Articular surface areas, estimated from linear caliper measurements, and diaphyseal section moduli (strengths), determined from CT scans, were obtained for the femur, tibia, humerus, radius, and ulna. Both within-bone (articular to shaft) and between-bone (forelimb to hindlimb) proportions were calculated and compared between taxa. It was hypothesized that: 1) species emphasizing slow, cautious movement and/or more varied limb positioning (i.e., greater joint excursion) would exhibit larger articular to cross-sectional shaft proportions, and 2) species with more forelimb suspensory behavior would have relatively stronger/larger forelimbs, while those with more leaping would have relatively stronger/larger hindlimbs. The results of the analysis generally confirm both hypotheses. Several partial exceptions can be explained on the basis of more detailed structural-functional considerations. Associations between locomotion and structural proportions can be demonstrated both across major groupings (hominoids and cercopithecoids) and between relatively closely related taxa, e.g., mountain and lowland gorillas, siamangs and gibbons, and Trachypithecus and other colobines. Furthermore, structure and function do not always covary with taxonomy. For example, compared to cercopithecoids, mountain gorillas have relatively larger joints, like other hominoids, but do not have relatively stronger forelimbs, unlike other hominoids. This is consistent with a locomotor repertoire emphasizing relatively slow movement but with very little forelimb suspension. Proportions of Proconsul nyanzae, Proconsul heseloni, Morotopithecus bishopi, and Theropithecus oswaldi are compared with modern distributions to illustrate the application of the techniques to fossil taxa.     

From the ground up: Integrative research in primate locomotion

Primate locomotor adaptation and evolution is a principal and thriving area of research by biological anthropologists. Research in this field generally targets hypotheses regarding locomotor kinetics and kinematics, form–function associations in both the soft and hard tissue components of the musculoskeletal system, and reconstructing locomotor behavior in fossil primates. A wide array of methodological approaches is used to address adaptive hypotheses in all of these realms. Recent advances in three-dimensional shape capture, musculoskeletal physiological measurements, and analytical processing technologies (e.g., laser and CT-scans, 3D motion analysis systems, finite element analysis) have facilitated the collection and analysis of larger and more complex locomotor datasets than previously possible. With these advances in technology, new methods of form–function analyses can be developed to produce a more thorough understanding of how form reflects an organism's mechanical requirements, how shape is influenced by external environmental factors, and how these investigations of living taxa can inform questions of primate paleobiology. The papers in this special section of the American Journal of Physical Anthropology present research that builds on that foundation, by combining new data on living primates and new methodologies and approaches to answer a range of questions on extant and extinct primates. Am J Phys Anthropol 156:495–497, 2015. © 2015 Wiley Periodicals, Inc.     

Ontogeny of the hominoid scapula: The influence of locomotion on morphology

Primate shoulder morphology has been linked with locomotor habits, oftentimes irrespective of phylogenetic heritage. Among hominoids, juvenile African apes are known to climb more frequently than adults, while orangutans and gibbons maintain an arboreal lifestyle throughout ontogeny. This study examined if these ontogenetic locomotor differences carry a morphological signal, which should be evident in the scapulae of chimpanzees and gorillas but absent in taxa that do not display ontogenetic behavioral shifts. The scapular morphology of five hominoid primates and one catarrhine outgroup was examined throughout ontogeny to evaluate if scapular traits linked with arboreal activities are modified in response to ontogenetic behavioral shifts away from climbing. Specifically, the following questions were addressed: 1) which scapular characteristics distinguish taxa with different locomotor habits; and 2) do these traits show associated changes during development in taxa known to modify their behavioral patterns? Several traits characterized suspensory taxa from nonsuspensory forms, such as cranially oriented glenohumeral joints, obliquely oriented scapular spines, relatively narrow infraspinous fossae, and inferolaterally expanded subscapularis fossae. The relative shape of the dorsal scapular fossae changed in Pan, Gorilla, and also Macaca in line with predictions based on reported ontogenetic changes in locomotor behavior. These morphological changes were mostly distinct from those seen in Pongo, Hylobates, and Homo and imply a unique developmental pattern, possibly related to ontogenetic locomotor shifts. Accordingly, features that sorted taxa by locomotor habits and changed in concert with ontogenetic behavioral patterns should be particularly useful for reconstructing the locomotor habits of fossil forms. Am J Phys Anthropol 152:239–260, 2013. © 2013 Wiley Periodicals, Inc.     

Cortical bone distribution in the femoral neck of hominoids: Implications for the locomotion of Australopithecus afarensis

Contiguous high resolution computed tomography images were obtained at a 1.5 mm slice thickness perpendicular to the neck axis from the base of the femoral head to the trochanteric line in a sample of 10 specimens each of Homo sapiens, Pan troglodytes, and Gorilla gorilla, plus five specimens of Pan paniscus. Superior, inferior, anterior, and posterior cortical thicknesses were automatically measured directly from these digital images. Throughout the femoral neck H. sapiens displays thin superior cortical bone and inferior cortical bone that thickens distally. In marked contrast, cortical bone in the femoral neck of African apes is more uniformly thick in all directions, with even greater thickening of the superior cortical bone distally. Because the femoral neck acts as a cantilevered beam, its anchorage at the neck-shaft junction is subjected to the highest bending stresses and is the most biomechanically relevant region to inspect for response to strain. As evinced by A.L. 128-1, A.L. 211-1 and MAK-VP-1/1, Australopithecus afarensis is indistinguishable from H. sapiens, but markedly different from African apes in cortical bone distribution at the femoral neck-shaft junction. Cortical distribution in the African ape indicates much greater variation in loading conditions consistent with their more varied locomotor repertoire. Cortical distribution in hominids is a response to the more stereotypic loading pattern imposed by habitual bipedality, and thin superior cortex in A. afarensis confirms the absence of a significant arboreal component in its locomotor repertoire. Am J Phys Anthropol 104:117–131, 1997. © 1997 Wiley-Liss, Inc.     

A Three-Dimensional Histological Method for Direct Determination of the Number of Trabecular Termini in Cancellous Bone

Osteoporotic fractures occur frequently in aging populations. Established methods for analyzing microarchitecture indicate that cancellous bone loss in the elderly is associated with progressive reduction in the connectivity of the trabecular network. This disconnection may explain the increased skeletal fragility that is sometimes out of proportion to the amount of bone lost. Connectivity, however, is difficult to measure and usually requires indirect methods. We describe development of a simple, inexpensive and direct procedure for counting sites of trabecular disconnection. The method is based upon preparation of 300-500 fjim thick slices of methylmethacrylate embedded material rather than the more usual thin 8 μm. histological sections. The marrow tissue is retained within the thick slice; this is essential for conservation of any detached bone fragments. In such preparations differential superficial staining of the upper and lower surfaces with alizarin red and light green, respectively, allows the two-dimensional image to be viewed at the same time as its three-dimensional counterpart. In this way, “real” (i. e., unstained) trabecular termini can be distinguished from “apparent” (i. e., stained red or green) termini that are artifacts of the plane of section. Partly polarized light enhances the microscope image. The method does not destroy the material for subsequent bone histomorphom-etry and, therefore, may be a useful adjunct to iliac bone biopsy analysis in studies of metabolic bone disease.     

Histologic examination of bone development in juvenile chimpanzees

The purpose of this study is to determine whether histologic skeletal development in chimpanzees (Pan troglodytes) differs from that in humans. Currently, minimal quantitative data are available on the bone histology of great apes. In addition to providing baseline data on juvenile chimpanzee bone histology, the data generated by this study have potential applications for studying the comparative development between chimpanzees and humans and other primates, as well as investigating the evolution of human bone development, differences in development among limb elements, and differences in histology related to locomotor function. The study sample includes thin sections from the femoral, tibial, and fibular midshafts of 13 chimpanzees originally prepared by Kerley ([1966] Tulane Stud. Zool. 13:71-82) as part of a study on skeletal age changes in the chimpanzee. Twelve juveniles, ranging in known age from 2-15.3 years, and one adult, with a known age of 35 years, are represented. For each specimen, numbers of osteons, osteon fragments, and non-Haversian canals were counted, and percent lamellar bone was estimated. Results were compared with data extracted from Kerley ([1965] Am. J. Phys. Anthropol. 23:149-164) on a juvenile human sample. Results indicate that juvenile chimpanzees and humans exhibit similar age-related changes in histologic variables. However, age is not as strong a predictor of variation in microstructural variables in chimpanzees as it is in humans.     

Trabecular bone scales allometrically in mammals and birds

Many bones are supported internally by a latticework of trabeculae. Scaling of whole bone length and diameter has been extensively investigated, but scaling of the trabecular network is not well characterized. We analysed trabecular geometry in the femora of 90 terrestrial mammalian and avian species with body masses ranging from 3 g to 3400 kg. We found that bone volume fraction does not scale substantially with animal size, while trabeculae in larger animals' femora are thicker, further apart and fewer per unit volume than in smaller animals. Finite element modelling indicates that trabecular scaling does not alter the bulk stiffness of trabecular bone, but does alter strain within trabeculae under equal applied loads. Allometry of bone's trabecular tissue may contribute to the skeleton's ability to withstand load, without incurring the physiological or mechanical costs of increasing bone mass.     

A new bone banking technique to maintain osteoblast viability in frozen human iliac cancellous bone

The aim of this study was to develop a new cryopreservation technique to maintain the osteoblast viability in frozen iliac bone and to prove cell viability using cell culture techniques.Human iliac cancellous bones were frozen with and without 10% Me(2)SO at -80 degrees C. The tubes were kept in a -80 degrees C freezer for at least 2 days. After the storage period, the frozen bone was thawed by placing the tube in a 37 degrees C water bath. A serial enzymatic digestion technique using 0.2% collagenase was employed to isolate osteoblast-like cells from the bone. The cells that were released were inoculated into tissue culture flasks containing DMEM supplemented with 10% FCS. They were incubated at 37 degrees C in a humidified atmosphere of 95% air and 5% CO(2). Cells of the second passage were plated at a density of 5 x 10(3)cells/cm(2) in a 24-well plate and used for characterization. For characterization, WST-1 assay, determination of alkaline phosphatase, Type I collagen assay, osteocalcin assay, and von Kossa staining were used. The assays were performed at 3, 6, 9, and 12 days after plating the cells. Based on the results of this study, we conclude that the osteoblast-like cells in the frozen bone can survive, only when the bone is frozen with cryoprotectants to prevent injury during freezing and thawing.     

Diversity of pectoral fin structure and function in fishes with labriform propulsion

Aquatic propulsion generated by the pectoral fins occurs in many groups of perciform fishes, including numerous coral reef families. This study presents a detailed survey of pectoral fin musculoskeletal structure in fishes that use labriform propulsion as the primary mode of swimming over a wide range of speeds. Pectoral fin morphological diversity was surveyed in 12 species that are primarily pectoral swimmers, including members of all labroid families (Labridae, Scaridae, Cichlidae, Pomacentridae, and Embiotocidae) and five additional coral reef fish families. The anatomy of the pectoral fin musculature is described, including muscle origins, insertions, tendons, and muscle masses. Skeletal structures are also described, including fin shape, fin ray morphology, and the structure of the radials and pectoral girdle. Three novel muscle subdivisions, including subdivisions of the abductor superficialis, abductor profundus, and adductor medialis were discovered and are described here. Specific functional roles in fin control are proposed for each of the novel muscle subdivisions. Pectoral muscle masses show broad variation among species, particularly in the adductor profundus, abductor profundus, arrector dorsalis, and abductor superficialis. A previously undescribed system of intraradial ligaments was also discovered in all taxa studied. The morphology of these ligaments and functional ramifications of variation in this connective tissue system are described. Musculoskeletal patterns are interpreted in light of recent analyses of fin behavior and motor control during labriform swimming. Labriform propulsion has apparently evolved independently multiple times in coral reef fishes, providing an excellent system in which to study the evolution of pectoral fin propulsion.     

There is no trade-off between speed and force in a dynamic lever system

Lever systems within a skeleton transmit force with a capacity determined by the mechanical advantage, A. A is the distance from input force to a joint, divided by the distance from the joint to the output force. A lever with a relatively high A in static equilibrium has a great capacity to generate force but moves a load over a small distance. Therefore, the geometry of a skeletal lever presents a trade-off between force and speed under quasi-static conditions. The present study considers skeletal dynamics that do not assume static equilibrium by modelling kicking by a locust leg, which is powered by stored elastic energy. This model predicts that the output force of this lever is proportional to A, but its maximum speed is independent of A. Therefore, no trade-off between force and velocity exists in a lever system with spring-mass dynamics. This demonstrates that the motion of a skeleton depends on the major forces that govern its dynamics and cannot be inferred from skeletal geometry alone.