M. Loring Burgess

Ontogenetic changes in limb bone structural proportions in mountain gorillas (Gorilla beringei beringei)

Behavioral studies indicate that adult mountain gorillas (Gorilla beringei) are the most terrestrial of all nonhuman hominoids, but that infant mountain gorillas are much more arboreal. Here we examine ontogenetic changes in diaphyseal strength and length of the femur, tibia, humerus, radius, and ulna in 30 Virunga mountain gorillas, including 18 immature specimens and 12 adults. Comparisons are also made with 14 adult western lowland gorillas (Gorilla gorilla gorilla), which are known to be more arboreal than adult mountain gorillas. Infant mountain gorillas have significantly stronger forelimbs relative to hind limbs than older juveniles and adults, but are nonsignificantly different from western lowland gorilla adults. The change in inter-limb strength proportions is abrupt at about two years of age, corresponding to the documented transition to committed terrestrial quadrupedalism in mountain gorillas. The one exception is the ulna, which shows a gradual increase in strength relative to the radius and other long bones during development, possibly corresponding to the gradual adoption of stereotypical fully pronated knuckle-walking in older juvenile gorillas. Inter-limb bone length proportions show a contrasting developmental pattern, with hind limb/forelimb length declining rapidly from birth to five months of age, and then showing no consistent change through adulthood. The very early change in length proportions, prior to significant independent locomotion, may be related to the need for relatively long forelimbs for climbing in a large-bodied hominoid. Virunga mountain gorilla older juveniles and adults have equal or longer forelimb relative to hind limb bones than western lowland adults. These findings indicate that both ontogenetically and among closely related species of Gorilla, long bone strength proportions better reflect actual locomotor behavior than bone length proportions.

Body mass estimation in hominoids: Age and locomotor effects

While there are a number of methods available for estimation of body mass in adult nonhuman primates, very few are available for juveniles, despite the potential utility of such estimations in both analyses of fossils and in museum collection based research. Furthermore, because of possible scaling differences, adult based body mass estimation equations may not be appropriate for non-adults. In this study, we present new body mass estimation equations for both adult and immature nonhuman hominoids based on joint and metaphyseal dimensions. Articular breadths of the proximal and distal femur, distal humerus and tibial plateau, and metaphyseal breadths of the distal femur and humerus were collected on a reference sample of 159 wild Pan, Gorilla, Pongo, Hylobates, and Symphalangus specimens of known body mass from museum and research collections. Scaling of dimensions with body weight was assessed in both the adult and the ontogenetic sample at several taxonomic levels using reduced major axis regression, followed by regression of each dimension against body mass to generate body mass estimation equations. Joint dimensions were found to be good predictors of body mass in both adult and immature hominoids, with percent prediction errors of 10-20%. However, subtle scaling differences between taxa impacted body mass estimation, suggesting that phylogeny and locomotor effects should be considered when selecting reference samples. Unlike patterns of joint growth in humans, there was little conclusive evidence for consistently larger joints relative to body mass in the non-adult sample. Metaphyseal breadths were strong predictors of body mass and, with some exceptions, gave more precise body mass estimates for non-adults than epiphyseal breadths.

Articular scaling and body mass estimation in platyrrhines and catarrhines: Modern variation and application to fossil anthropoids

Body mass is an important component of any paleobiological reconstruction. Reliable skeletal dimensions for making estimates are desirable but extant primate reference samples with known body masses are rare. We estimated body mass in a sample of extinct platyrrhines and Fayum anthropoids based on four measurements of the articular surfaces of the humerus and femur. Estimates were based on a large extant reference sample of wild-collected individuals with associated body masses, including previously published and new data from extant platyrrhines, cercopithecoids, and hominoids. In general, scaling of joint dimensions is positively allometric relative to expectations of geometric isometry, but negatively allometric relative to expectations of maintaining equivalent joint surface areas. Body mass prediction equations based on articular breadths are reasonably precise, with %SEEs of 17-25%. The breadth of the distal femoral articulation yields the most reliable estimates of body mass because it scales similarly in all major anthropoid taxa. Other joints scale differently in different taxa; therefore, locomotor style and phylogenetic affinity must be considered when calculating body mass estimates from the proximal femur, proximal humerus, and distal humerus. The body mass prediction equations were applied to 36 Old World and New World fossil anthropoid specimens representing 11 taxa, plus two Haitian specimens of uncertain taxonomic affinity. Among the extinct platyrrhines studied, only Cebupithecia is similar to large, extant platyrrhines in having large humeral (especially distal) joints. Our body mass estimates differ from each other and from published estimates based on teeth in ways that reflect known differences in relative sizes of the joints and teeth. We prefer body mass estimators that are biomechanically linked to weight-bearing, and especially those that are relatively insensitive to differences in locomotor style and phylogenetic history. Whenever possible, extant reference samples should be chosen to match target fossils in joint proportionality.

A radiographic study of permanent molar development in wild Virunga mountain gorillas of known chronological age from Rwanda

OBJECTIVES While dental development is important to life history investigations, data from wild known-aged great apes are scarce. We report on the first radiographic examination of dental development in wild Virunga mountain gorillas, using known-age skeletal samples recovered in Rwanda. MATERIALS AND METHODS In 43 individuals (0.0-14.94 years), we collected radiographs of mandibular molars, and where possible, cone beam CT scans. Molar crown and root calcification status was assessed using two established staging systems, and age prediction equations generated using polynomial regression. Results were compared to available data from known-age captive and wild chimpanzees. RESULTS Mountain gorillas generally fell within reported captive chimpanzee distributions or exceeded them, exhibiting older ages at equivalent radiographic stages of development. Differences reflect delayed initiation and/or an extended duration of second molar crown development, and extended first and second molar root development, in mountain gorillas compared to captive chimpanzees. However, differences in the duration of molar root development were less evident compared to wild chimpanzees. DISCUSSION Despite sample limitations, our findings extend the known range of variation in radiographic estimates of molar formation timing in great apes, and provide a new age prediction technique based on wild specimens. However, mountain gorillas do not appear accelerated in radiographic assessment of molar formation compared to chimpanzees, as they are for other life history traits. Future studies should aim to resolve the influence of species differences, wild versus captive environments, and/or sampling phenomena on patterns observed here, and more generally, how they relate to variation in tooth size, eruption timing, and developmental life history.

Ontogenetic scaling of fore limb and hind limb joint posture and limb bone cross-sectional geometry in vervets and baboons

OBJECTIVES Previous studies suggest that the postures habitually adopted by an animal influence the mechanical loading of its long bones. Relatively extended limb postures in larger animals should preferentially reduce anteroposterior (A-P) relative to mediolateral (M-L) bending of the limb bones and therefore decrease A-P/M-L rigidity. We test this hypothesis by examining growth-related changes in limb bone structure in two primate taxa that differ in ontogenetic patterns of joint posture. MATERIALS AND METHODS Knee and elbow angles of adult and immature vervets (Chlorocebus aethiops, n = 16) were compared to published data for baboons (Papio hamadryas ursinus, n = 33, Patel et al., ). Ontogenetic changes in ratios of A-P/M-L bending rigidity in the femur and humerus were compared in skeletal samples (C. aethiops, n = 28; P. cynocephalus, n = 39). Size changes were assessed with linear regression, and age group differences tested with ANOVA. RESULTS Only the knee of baboons shows significant postural change, becoming more extended with age and mass. A-P/M-L bending rigidity of the femur decreases during ontogeny in immature and adult female baboons only. Trends in the humerus are less marked. Adult male baboons have higher A-P/M-L bending rigidity of the femur than females. CONCLUSIONS The hypothesized relationship between more extended joints and reduced A-P/M-L bending rigidity is supported by our results for immature and adult female baboon hind limbs, and the lack of significant age changes in either parameter in forelimbs and vervets. Adult males of both species depart from general ontogenetic trends, possibly due to socially mediated behavioral differences between sexes. Am J Phys Anthropol 161:72-83, 2016.

Phylogenetic and environmental effects on limb bone structure in gorillas

OBJECTIVES The effects of phylogeny and locomotor behavior on long bone structural proportions are assessed through comparisons between adult and ontogenetic samples of extant gorillas. MATERIALS AND METHODS A total of 281 wild-collected individuals were included in the study, divided into four groups that vary taxonomically and ecologically: western lowland gorillas (G. g. gorilla), lowland and highland grauer gorillas (G. b. graueri), and Virunga mountain gorillas (G. b. beringei). Lengths and articular breadths of the major long bones (except the fibula) were measured, and diaphyseal cross-sectional geometric properties determined using computed tomography. Ages of immature specimens (n = 145) were known or estimated from dental development. Differences between groups in hind limb to forelimb proportions were assessed in both adults and during development. RESULTS Diaphyseal strength proportions among adults vary in parallel with behavioral/ecological differences, and not phylogeny. The more arboreal western lowland and lowland grauer gorillas have relatively stronger forelimbs than the more terrestrial Virunga mountain gorillas, while the behaviorally intermediate highland grauer gorillas have intermediate proportions. Diaphyseal strength proportions are similar in young infants but diverge after 2 years of age in western lowland and mountain gorillas, at the same time that changes in locomotor behavior occur. There are no differences between groups in length or articular proportions among either adults or immature individuals. CONCLUSION Long bone diaphyseal strength proportions in gorillas are developmentally plastic, reflecting behavior, while length and articular proportions are much more genetically canalized. These findings have implications for interpreting morphological variation among fossil taxa.

Long bone diaphyseal shape follows different ontogenetic trajectories in captive and wild gorillas

OBJECTIVES A number of studies have demonstrated the ontogenetic plasticity of long bone diaphyseal structure in response to mechanical loading. Captivity should affect mechanical loading of the limbs, but whether captive apes grow differently than wild apes has been debated. Here, we compare captive and wild juvenile and adult Gorilla to ascertain whether growth trajectories in cross-sectional diaphyseal shape are similar in the two environments. MATERIALS AND METHODS A sample of young juvenile (n = 4) and adult (n = 10) captive Gorilla gorilla gorilla specimens, with known life histories, were compared with age-matched wild G.g. gorilla (n = 62) and G. beringei beringei (n = 75) in relative anteroposterior to mediolateral bending strength of the femur, tibia, and humerus. Cross sections were obtained using peripheral quantitative CT. RESULTS Captive and wild adult G.g. gorilla differed in bending strength ratios for all three bones, but these differences were not present in young juvenile G.g. gorilla. In comparisons across taxa, captive juvenile G.g. gorilla were more similar to wild G.g. gorilla than to G.b. beringei, while captive adult G.g. gorilla were more similar in shape to G.b. beringei in the hind limb. DISCUSSION Captive and wild G. gorilla follow different ontogenetic trajectories in long bone diaphyseal shape, corresponding to environmental differences and subsequent modified locomotor behaviors. Differences related to phylogeny are most evident early in development.