Specimens as individuals: Four interventions and recommendations for great ape skeletal collections research and curation.

Extensive discourse surrounds the ethics of human skeletal research and curation, but there has yet to be a similar discussion of the treatment of great ape skeletal remains, despite the clear interest in their ethical treatment when alive. Here we trace the history of apes who were killed and collected for natural history museums during the early 20th century and showcase how the guiding research questions of the colonial era continue to influence scholarship. We discuss best practices for improving industry and academic standards of research on, and the curation of, ape remains. The suggested interventions involve restoring individual identity and narrative to great apes while engaging with contextual reflexivity and decolonial theory. The resulting recommendations include contextualizing the individual, piecing individuals back together, challenging/questioning the captive-wild dichotomy, and collaborative international conversations. Our objective is to encourage a conversation regarding ethical and theoretical considerations in great ape skeletal remains research.

In vivo deciduous dental eruption in LuiKotale bonobos and Gombe chimpanzees.

OBJECTIVES: Existing data on bonobo and chimpanzee dental eruption timing are derived predominantly from captive individuals or deceased wild individuals. However, recent advances in noninvasive photographic monitoring of living, wild apes have enabled researchers to characterize dental eruption in relatively healthy individuals under naturalistic conditions. At present, such data are available for only one population of wild chimpanzees. We report data for an additional population of wild chimpanzees and the first dental eruption data for wild bonobos. MATERIALS AND METHODS: We collected photographs and video footage of teeth from the open mouths of wild bonobos and East African chimpanzees of known age from LuiKotale, Democratic Republic of the Congo, and Gombe National Park, Tanzania, respectively. We scored the presence and absence of deciduous teeth from photographs and video footage to characterize deciduous dental eruption timing in these two populations. RESULTS: Deciduous dental eruption ages in our sample fall within the range of variation previously documented for captive chimpanzees, but eruption ages are later in wild than in captive contexts. We found substantial variation in deciduous canine eruption timing, particularly among bonobos. One bonobo had a deciduous canine present by 227 days old while another did not have a deciduous canine present at 477 days old. DISCUSSION: Our data indicate that deciduous teeth erupt later in wild individuals than in captive individuals. We also found that deciduous dental eruption timing varies considerably between individuals within our study populations, a pattern that is consistent with previous studies. Future studies should consider sources of variation in deciduous canine eruption timing and relationships with other aspects of life history as additional data become available.

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.

Investigating factors of metabolic bone disease in baboons (Papio spp.) using museum collections.

OBJECTIVES: To assess manifestations of metabolic bone disease (MBD) and their potential environmental and phenotypic factors in captive and non-captive baboon (Papio spp.) specimens. MATERIALS AND METHODS: Our sample consisted of 160 baboon specimens at the Smithsonian's National Museum of Natural History accessioned from 1890 to 1971. Combining cranial indicators of MBD and the museum's historical data, we examined factors contributing to likely instances of MBD. We used binomial-family generalized linear models to assess differences in MBD frequency by environment (captive, non-captive), specimen accession year, and skin color (light, medium, dark). RESULTS: Indicators of MBD were most frequently observed in captive baboons, with a decrease in MBD frequency over time. Fifteen non-captive individuals showed indicators of MBD, which are the first published cases of MBD in non-captive nonhuman primates (NHPs) to our knowledge. The most common MBD indicators were bone porosity (n = 35) and bone thickening/enlargement (n = 35). Fibrous osteodystrophy was observed frequently in our sample, likely relating to nutritional deficiencies. We found no association between exposed facial skin color variation and MBD. CONCLUSIONS: Our findings are consistent with historical accounts of MBD prevalence in captive facilities, especially earlier in the 20th century. A decrease in MBD prevalence later in the 20th century likely reflects improvements in housing, diet, and veterinary care in captive settings. Causes of MBD development in non-captive baboons should be further explored, as understanding the potential health impacts that anthropogenic environments impose on NHPs is imperative as humans increasingly alter the natural world in the 21st century.

Body proportions and environmental adaptation in gorillas.

OBJECTIVES: Limb length and trunk proportions are determined in a large, taxonomically and environmentally diverse sample of gorillas and related to variation in locomotion, climate, altitude, and diet. MATERIALS AND METHODS: The sample includes 299 gorilla skeletons, 115 of which are infants and juveniles, distributed between western lowland (G. gorilla gorilla), low and high elevation grauer (G. beringei graueri), and Virunga mountain gorillas (G. b. beringei). Limb bone and vertebral column lengths scaled to body mass are compared between subgroups by age group. RESULTS: All G. beringei have relatively short 3rd metapodials and manual proximal phalanges compared to G. gorilla, and this difference is apparent in infancy. All G. beringei also have shortened total limb lengths relative to either body mass or vertebral column length, although patterns of variation in individual skeletal elements are more complex, and infants do not display the same patterns as adults. Mountain gorillas have relatively long clavicles, present in infancy, and a relatively long thoracic (but not lumbosacral) vertebral column. DISCUSSION: A variety of environmental factors likely contributed to observed patterns of morphological variation among extant gorillas. We interpret the short hand and foot bones of all G. beringei as genetic adaptations to greater terrestriality in the last common ancestor of G. beringei; variation in other limb lengths to climatic adaptation, both genetic and developmental; and the larger thorax of G. b. beringei to adaptation to reduced oxygen pressure at high altitudes, again as a product of both genetic differences and environmental influences during development.

What does it mean to be wild? Assessing human influence on the environments of nonhuman primate specimens in museum collections.

OBJECTIVES: Natural history collections are often thought to represent environments in a pristine natural state-free from human intervention-the so-called "wild." In this study, we aim to assess the level of human influence represented by natural history collections of wild-collected primates over 120 years at the Smithsonian Institution's National Museum of Natural History (NMNH). MATERIALS AND METHODS: Our sample consisted of 875 catarrhine primate specimens in NMNH collections, representing 13 genera collected in 39 countries from 1882 to 2004. Using archival and accession information we determined the approximate locations from which specimens were collected. We then plotted location coordinates onto publicly available anthrome maps created by Ellis et al. (Global Ecology and Biogeography, 2010, 19, 589), which delineate terrestrial biomes of human population density and land use worldwide since the 1700s. RESULTS: We found that among primates collected from their native ranges, 92% were from an environment that had some level of human impact, suggesting that the majority of presumed wild-collected primate specimens lived in an environment influenced by humans during their lifetimes. DISCUSSION: The degree to which human-modified environments may have impacted the lives of primates currently held in museum collections has been historically ignored, implicating unforeseen consequences for collection-based research. While unique effects related to commensalism with humans remain understudied, effects currently attributed to natural phenomena may, in fact, be related to anthropogenic pressures on unmanaged populations of primates.

Rapid development of secondary hyperparathyroidism and fibrous osteodystrophy in a juvenile orangutan.

This study presents a probable case of rapidly-developed fibrous osteodystrophy and secondary hyperparathyroidism in a juvenile wild-caught zoo orangutan, Pongo pygmaeus. Cases of this metabolic disease, associated with captivity in primates, are underreported in non-human Hominidae, and none to the extent of postcranial afflictions. We present the first described case of these metabolic pathologies of a great ape at both the cranial and skeletal levels.