Drug‐Resistant Human Staphylococcus Aureus in Sanctuary Apes Pose a Threat to Endangered Wild Ape Populations

Reintroduction of sanctuary apes to natural habitat is considered an important tool for conservation; however, reintroduction has the potential to endanger resident wild apes through the introduction of human pathogens. We found a high prevalence of drug‐resistant, human‐associated lineages of Staphylococcus aureus in sanctuary chimpanzees (Pan troglodytes) from Zambia and Uganda. This pathogen is associated with skin and soft tissue diseases and severe invasive infections (i.e. pneumonia and septicemia). Colonization by this bacterium is difficult to clear due to frequent recolonization. In addition to its pathogenic potential, human‐related S. aureus can serve as an indicator organism for the transmission of other potential pathogens like pneumococci or mycobacteria. Plans to reintroduce sanctuary apes should be reevaluated in light of the high risk of introducing human‐adapted S. aureus into wild ape populations where treatment is impossible. Am. J. Primatol. 74:1071‐1075, 2012. © 2012 Wiley Periodicals, Inc.     

Does Confirmed Pathogen Transfer between Sanctuary Workers and Great Apes Mean that Reintroduction Should not Occur?

This commentary discusses the findings and conclusions of the paper “Drug resistant human Staphylococcus aureus findings in sanctuary apes and its threat to wild ape populations.” This paper confirms the zoonotic transfer of Staphylococcus aureus in a sanctuary setting. The assertion that this in itself is enough to reconsider the conservation potential of ape reintroduction provides an opportunity to discuss risk analysis of pathogen transmission, following IUCN guidelines, using S. aureus as an example. It is concluded that ape reintroduction projects must have disease risk mitigation strategies that include effective biosecurity protocols and pathogen surveillance. These strategies will assist with creating a well planned and executed reintroduction. This provides one way to enforce habitat protection, to minimise human encroachment and the risks from the illegal wildlife trade. Thus reintroduction must remain a useful tool in the conservation toolbox. Am. J. Primatol. 74:1076‐1083, 2012. © 2012 Wiley Periodicals, Inc.     

Predicting body mass of bonobos (Pan paniscus) with human-based morphometric equations

A primate's body mass covaries with numerous ecological, physiological, and behavioral characteristics. This versatility and potential to provide insight into an animal's life has made body mass prediction a frequent and important objective in paleoanthropology. In hominin paleontology, the most commonly employed body mass prediction equations (BMPEs) are “mechanical” and “morphometric”: uni- or multivariate linear regressions incorporating dimensions of load-bearing skeletal elements and stature and living bi-iliac breadth as predictor variables, respectively. The precision and accuracy of BMPEs are contingent on multiple factors, however, one of the most notable and pervasive potential sources of error is extrapolation beyond the limits of the reference sample. In this study, we use a test sample requiring extrapolation—56 bonobos (Pan paniscus) from the Lola ya Bonobo sanctuary in Kinshasa, Democratic Republic of the Congo—to evaluate the predictive accuracy of human-based morphometric BMPEs. We first assess systemic differences in stature and bi-iliac breadth between humans and bonobos. Due to significant differences in the scaling relationships of body mass and stature between bonobos and humans, we use panel regression to generate a novel BMPE based on living bi-iliac breadth. We then compare the predictive accuracy of two previously published morphometric equations with the novel equation and find that the novel equation predicts bonobo body mass most accurately overall (41 of 56 bonobos predicted within 20% of their observed body mass). The novel BMPE is particularly accurate between 25 and 45 kg. Given differences in limb proportions, pelvic morphology, and body tissue composition between the human reference and bonobo test samples, we find these results promising and evaluate the novel BMPE's potential application to fossil hominins.     

Human Respiratory Syncytial Virus and <Emphasis Type="Italic">Streptococcus pneumoniae</Emphasis> Infection in Wild Bonobos

Despite being important conservation tools, tourism and research may cause transmission of pathogens to wild great apes. Investigating respiratory disease outbreaks in wild bonobos, we identified human respiratory syncytial virus and Streptococcus pneumoniae as causative agents. A One Health approach to disease control should become part of great ape programs.     

How did bonobos come to range south of the congo river? Reconsideration of the divergence of Pan paniscus from other Pan populations

While investigating the genetic structure in wild bonobos,¹ we realized that the widely accepted scenario positing that the Pleistocene appearance of the Congo River separated the common ancestor of chimpanzees (Pan troglodytes) and bonobos (P. paniscus) into two species is not supported by recent geographical knowledge about the formation of the Congo River. We explored the origin of bonobos using a broader biogeographical perspective by examining local faunas in the central African region. The submarine Congo River sediments and paleotopography of central Africa show that the Congo River has functioned as a geographical barrier for the last 34 million years. This evidence allows us to hypothesize that when the river was first formed, the ancestor of bonobos did not inhabit the current range of the species on the left bank of the Congo River but that, during rare times when the Congo River discharge decreased during the Pleistocene, one or more founder populations of ancestral Pan paniscus crossed the river to its left bank. The proposed scenario for formation of the Congo River and the corridor hypothesis for an ancestral bonobo population is key to understanding the distribution of great apes and their evolution.     

Preliminary bonobo and chimpanzee nesting by habitat type in the northern Lac Tumba Landscape,Democratic Republic of Congo

Knowing how habitat determines the distribution of great apes is essential for understanding their ecology and conservation requirements. Habitats in the northern Lac Tumba Landscape where this study was conducted are mostly swamp and flooded forests, which types have been overlooked in many great ape surveys. This study describes and discusses patterns of bonobo and chimpanzee nesting sites across these habitat types in the general scope of habitat use by great apes. Considerable efforts were deployed to survey forests of the Ngiri Triangle (186 km), Bomongo‐Lubengo (126 km) and Bolombo‐Losombo (112 km). Great ape nesting site encounter rates (r) were calculated for Bonobos (r = 0.21 nesting sites km^?1; Bolombo‐Losombo), chimpanzees (r = 0.11 nesting sites km^?1; Ngiri Triangle) and (r = 0.02 nesting sites km^?1; Bomongo‐Lubengo). Swamps and flooded forests dominated the three zones. Nesting sites were at the highest encounter rates in flooded forests; both great ape species were significantly associated with swampy and flood forests. Human signs did not influence the occurrence of nesting sites in these forests. These results confirm findings from other sites where great apes were observed using swamps; they suggest that future surveys include these types of habitat to avoid under‐estimating population sizes.     

Bonobos Respond to Distress in Others: Consolation across the Age Spectrum

How animals respond to conflict provides key insights into the evolution of socio-cognitive and emotional capacities. Evidence from apes has shown that, after social conflicts, bystanders approach victims of aggression to offer stress-alleviating contact behavior, a phenomenon known as consolation. This other-orientated behavior depends on sensitivity to the other''s emotional state, whereby the consoler acts to ameliorate the other''s situation. We examined post-conflict interactions in bonobos (Pan paniscus) to identify the determinants of consolation and reconciliation. Thirty-six semi-free bonobos of all ages were observed at the Lola ya Bonobo Sanctuary, DR Congo, using standardized Post-conflict/Matched Control methods. Across age and sex classes, bonobos consoled victims and reconciled after conflicts using a suite of affiliative and socio-sexual behaviors including embracing, touching, and mounting. Juveniles were more likely to console than adults, challenging the assumption that comfort-giving rests on advanced cognitive mechanisms that emerge only with age. Mother-reared individuals were more likely to console than orphans, highlighting the role of rearing in emotional development. Consistent with previous studies, bystanders were more likely to console relatives or closely bonded partners. Effects of kinship, affiliation and rearing were similarly indicated in patterns of reconciliation. Nearby bystanders were significantly more likely to contact victims than more distal ones, and consolation was more likely in non-food contexts than during feeding. The results did not provide convincing evidence that bystander contacts served for self-protection or as substitutes for reconciliation. Overall, results indicate that a suite of social, developmental and contextual factors underlie consolation and reconciliation in bonobos and that a sensitivity to the emotions of others and the ability to provide appropriate consolatory behaviors emerges early in development.     

Densities,Distributions, and Seasonal Movements of Gorillas and Chimpanzees in Swamp Forest in Northern Congo

The conservation of gorillas (Gorilla spp.) and chimpanzees (Pan troglodytes) depends upon knowledge of their densities and distribution throughout their ranges. However, information about ape populations in swamp forests is scarce. Here we build on current knowledge of ape populations by conducting line transect surveys of nests throughout a reserve dominated by swamp forest: the Lac Télé Community Reserve in northern Congo. We estimated gorilla and chimpanzee densities, distributions across habitats, and seasonal changes in abundance. Gorilla density was 2.9 gorillas km^–2, but densities varied by habitat (0.3–5.4 gorillas km^–2) with highest densities in swamp forest and terra firma mixed forest. Average chimpanzee density is 0.7 chimpanzees km^–2 (0.1–1.3 chimpanzees km^–2), with highest densities in swamp forest. Habitat was the best predictor of ape nest abundance, as neither the number of human indices nor the distance from the nearest village predicted nest abundance. We recorded significantly greater numbers of apes in terra firma forest during the high-water season than the low-water season, indicating that many gorillas and chimpanzees are at times concentrated in terra firma forest amid a matrix of swamp forest. Seasonally high numbers of apes on terra firma forest islands easily accessible to local people may expose them to substantial hunting pressure. Conversely, the nearly impenetrable nature of swamp forests and their low value for logging makes them promising sites for the conservation of apes.     

Origin of human chromosome 2 revisited

Similarities in chromosome banding patterns and hornologies in DNA sequence between chromosomes of the great apes and humans have suggested that human chromosome 2 originated through the fusion of two ancestral ape chromosomes. A lot of work has been directed at understanding the nature and mechanism of this fusion. The recent availability of the human chrornosome-2-specific alpha satellite DNA probe D2Z and the human chromosome-2p-specific subtelomeric DNA probe D2S445 prompted us to attempt cross-hybridization with chromosomes of the chimpanzee (Pan troglodytes), gorilla (Gorilla gorilla) and orangutan (Pongo pygmaeus) to search for equivalent locations in the great apes and to comment on the origin of human chromosome 2. The probes gave different results. No hybridization to the chromosome-2-specific alpha satellite DNA probe was observed on the presumed homologous great ape chromosomes using both high-stringency and low-stringency post-hybridization washes, whereas the subtelomeric-DNA probe specific for chromosome 2p hybridized to telomeric sites of the short arm of chromosome 12 of all three great apes. These observations suggest an evolutionary difference in the number of alpha satellite DNA repeat units in the equivalent ape chromosomes presumably involved in the chromosome fusion. Nevertheless, complete conservation of DNA sequence of the subtelomeric repeat sequence D2S445 in the ape chromosomes is demonstrated.     

Reproductive Parameters of Female<Emphasis Type="Italic">Pan paniscus</Emphasis> and <Emphasis Type="Italic">P. troglodytes</Emphasis>: Quality versus Quantity

We investigated intra- and interspecific differences in life history and reproductive parameters in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We compare the parameters of wild and captive females in order to shed light on the influence of habitat or specific differences or both on reproduction. We present new and additional information on reproductive parameters from captive bonobos and chimpanzees. Captive chimpanzees birth more live offspring and have a shorter interbirth interval, but experience higher infant mortality than captive bonobos. Although captive bonobo females tend to start reproduction at a younger age than chimpanzees, this is effectively only so for wild-born females of both species. Ultimately both species reach the same rate of production of offspring surviving to 5 yr. These results contrast with data from the wild. Wild bonobos tend to have higher reproductive success, a higher fertility rate and a shorter interbirth interval than wild chimpanzees. Reproduction is similar for wild and captive bonobos, which suggests that they are producing at their maximum under both conditions. Overall captive chimpanzees perform better than their wild conspecifics, probably because of lower feeding competition. Infant survival is the only specific difference not affected by captivity. Bonobo infants survive better, which suggests that chimpanzee infants are more at risk. We argue that the interspecific variation in reproductive parameters in captivity is related to the different influence of captivity on reproduction and different pressures of external sources of infant and juvenile mortality.     

Patterns of microsatellite polymorphism in the range-restricted bonobo (Pan paniscus): considerations for interspecific comparison with chimpanzees (P. troglodytes)

The endangered great ape, Pan paniscus (bonobo) has the smallest range of the African apes. Virtually nothing is known about the genetic diversity or genetic structure of this species, while substantial amounts of polymorphism have been reported for the bonobo’s widespread congener, the chimpanzee (P. troglodytes). Given its restricted range, what is the extent of genetic variation in the bonobo relative to the chimpanzee, and is the bonobo genetically depauperate? To investigate patterns of genetic polymorphism, bonobos of wild origin were genotyped for 28 microsatellite loci. The mean number of alleles per locus (5.2) and the mean observed heterozygosity (0.52) in bonobos were similar to variation observed in a wild chimpanzee community (P. t. schweinfurthii). The rarer bonobo is not genetically depauperate and may have genetic diversity comparable to the eastern chimpanzee subspecies. Bonobos have approximately 55% of the allelic diversity and 66% of the observed heterozygosity exhibited by all three chimpanzee subspecies sampled across equatorial Africa. Resampling techniques were used to quantify the effects of sample size differences and number and choice of loci between bonobos and chimpanzees. The examination of these variables underscores their importance in accurately interpreting interspecific comparisons of diversity estimates.     

Human proximity and habitat fragmentation are key drivers of the rangewide bonobo distribution

Habitat loss and hunting threaten bonobos (Pan paniscus), Endangered (IUCN) great apes endemic to lowland rainforests of the Democratic Republic of Congo. Conservation planning requires a current, data-driven, rangewide map of probable bonobo distribution and an understanding of key attributes of areas used by bonobos. We present a rangewide suitability model for bonobos based on a maximum entropy algorithm in which data associated with locations of bonobo nests helped predict suitable conditions across the species’ entire range. We systematically evaluated available biotic and abiotic factors, including a bonobo-specific forest fragmentation layer (forest edge density), and produced a final model revealing the importance of simple threat-based factors in a data poor environment. We confronted the issue of survey bias in presence-only models and devised a novel evaluation approach applicable to other taxa by comparing models built with data from geographically distinct sub-regions that had higher survey effort. The model’s classification accuracy was high (AUC = 0.82). Distance from agriculture and forest edge density best predicted bonobo occurrence with bonobo nests more likely to occur farther from agriculture and in areas of lower edge density. These results suggest that bonobos either avoid areas of higher human activity, fragmented forests, or both, and that humans reduce the effective habitat of bonobos. The model results contribute to an increased understanding of threats to bonobo populations, as well as help identify priority areas for future surveys and determine core bonobo protection areas.     

Comparative in vivo forefoot kinematics of Homo sapiens and Pan paniscus

The human metatarsophalangeal joints play a key role in weight transmission and propulsion during bipedal gait, but at present, the identification of when a habitual, human-like metatarsi-fulcrimating mechanism first appeared in the fossil record is debated. Part of this debate can be attributed to the absence of certain detailed quantitative data distinguishing human and great ape forefoot form and function.The aim of this study is to quantitatively test previous observations that human metatarsophalangeal joints exhibit greater amounts of dorsal excursion (i.e., dorsiflexion) than those of Pan at the terminal stance phase of terrestrial locomotion. Video recordings were made in order to measure sagittal excursions of the medial metatarsophalangeal joints in habitually shod/unshod adult humans and adult bonobos (Pan paniscus). Results indicate that the human first and second metatarsophalangeal joints usually dorsiflex more than those of bonobos. When timing of maximum excursion of the first metatarsophalangeal joint is coupled with existing plantar pressure data, the unique role of the human forefoot as a key site of leverage and weight transmission is highlighted. These results support hypotheses that significant joint functional differences between great apes and humans during gait underlie taxonomic distinctions in trabecular bone architecture of the forefoot.     

Comparative analyses of the Pan lineage reveal selection on gene pathways associated with diet and sociality in bonobos

Chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) diverged into distinct species approximately 1.7 million years ago when the ancestors of modern-day bonobo populations were separated by the Congo River. This geographic boundary separates the two species today and the associated ecological factors, including resource distribution and feeding competition, have likely shaped the divergent social behavior of both species. The most striking behavioral differences pertain to between group interactions in which chimpanzees behave aggressively towards unfamiliar conspecifics, while bonobos display remarkable tolerance. Several hypotheses attempt to explain how different patterns of social behavior have come to exist in the two species, some with specific genetic predictions, likening the evolution of bonobos to a process of domestication. Here, we utilize 73 ape genomes and apply linkage haplotype homozygosity and structure informed allele frequency differentiation methods to identify positively selected regions in bonobos since their split from a common pan ancestor to better understand the environment and processes that resulted in the behavioral differences observed today. We find novel evidence of selection in genetic regions that aid in starch digestion (AMY2) along with support for two genetic predictions related to self-domestication processes hypothesized to have occurred in the bonobo. We also find evidence for selection on neuroendocrine pathways associated with social behavior including the oxytocin, serotonin, and gonadotropin releasing hormone pathways.     

Comparative chemical analysis of body odor in great apes

Olfaction is important across the animal kingdom for transferring information on, for example, species, sex, group membership, or reproductive parameters. Its relevance has been established in primates including humans, yet research on great apes still is fragmentary. Observational evidence indicates that great apes use their sense of smell in various contexts, but the information content of their body odor has not been analyzed. Our aim was therefore to compare the chemical composition of body odor in great ape species, namely Sumatran orangutans (Pongo abelii (Lesson, 1827), one adult male, five adult females, four nonadults), Western lowland gorillas (Gorilla gorilla gorilla (Savage, 1847), one adult male, two adult females, one nonadult), common chimpanzees (Pan troglodytes (Blumenbach, 1775), four adult males, nine adult females, four nonadults), and bonobos (Pan paniscus (Schwarz, 1929), two adult males, four adult females, two nonadults). We collected 195 samples (five per individual) of 39 captive individuals using cotton swabs and analyzed them using gas chromatography mass spectrometry. We compared the sample richness and intensity, similarity of chemical composition, and relative abundance of compounds. Results show that species, age, and potentially sex have an impact on the variance between odor profiles. Richness and intensity varied significantly between species (gorillas having the highest, bonobos the lowest richness and intensity), and with age (both increasing with age). Richness and intensity did not vary between sexes. Odor samples of the same species were more similar to each other than samples of different species. Among all compounds identified some were associated with age (N = 7), sex (N = 6), and species‐related (N = 37) variance. Our study contributes to the basic understanding of olfactory communication in hominids by showing that the chemical composition of body odor varies across species and individuals, containing potentially important information for social communication.     

Large differences between LINE-1 amplification rates in the human and chimpanzee lineages

The genomic evolution and causes of phenotypic variation among humans and great apes remain largely unknown, although the phylogenetic relationships among them have been extensively explored. Previous studies that focus on differences at the amino acid and nucleotide sequence levels have revealed a high degree of similarity between humans and chimpanzees, suggesting that other types of genomic change may have contributed to the relatively large phenotypic differences between them. For example, the activity of long interspersed element 1 (LINE-1) retrotransposons may impose significant changes on genomic structure and function and, consequently, on phenotype. Here we investigate the relative rates of LINE-1 amplification in the lineages leading to humans, bonobos (Pan paniscus), and chimpanzees (P. troglodytes). Our data indicate that LINE-1 insertions have accumulated at significantly greater rates in bonobos and chimpanzees than in humans, provide insights into the timing of major LINE-1 amplification events during great ape evolution, and identify a Pan-specific LINE-1 subfamily.     

Prospects for Bonobo Insectivory: Lui Kotal, Democratic Republic of Congo

Chimpanzees (Pan troglodytes) are well-known to eat invertebrates, especially social insects, across Africa, but allopatric bonobos (P. paniscus) are not. Bonobo insectivory is sparsely documented and apparently sporadic. However, the availability to bonobos of social insect prey and raw materials with which to make tools to exploit them is unknown. Here, we test a set of hypotheses that relates to questions of presence, abundance, density, and distribution of taxa that Pan consume and of vegetation suitable for making extractive foraging tools. We worked at Lui Kotal, Democratic Republic of Congo, where unprovisioned bonobos live in intact forest, far from villages. We collected insect and fecal specimens, transected for prey and assessed raw materials, and monitored mounds of Macrotermes. All but 1 of the major taxa of relevant termites, ants, and (stinging) honey bees were present. The 3 main taxa of insects that chimpanzees elsewhere eat —Macrotermes (fungus-growing termites), Dorylus (Anomma; army or driver ants), and Apis (honey bees)— were abundant and widespread, and usually at densities exceeding those at well-known chimpanzee study-sites. Similarly, woody and nonwoody vegetation suitable for making fishing probes was common at mounds of Macrotermes. There is no obvious ecological reason why bonobos should not use elementary technology in extractive foraging, e.g., termite-fish, ant-fish, ant-dip, honey-dip, to obtain social insects.     

Comparing ape densities and habitats in northern Congo: surveys of sympatric gorillas and chimpanzees in the Odzala and Ndoki regions

The conservation status of western lowland gorillas and central chimpanzees in western equatorial Africa remains largely speculative because many remote areas have never been surveyed and the impact of emergent diseases in the region has not been well documented. In this study, we compared ape densities and habitats in the Lokoué study area in Odzala National Park and the Goualougo Triangle in Nouabalé-Ndoki National Park in northern Republic of Congo. Both of these sites have long been considered strongholds for the conservation of chimpanzees and gorillas, but supposedly differ in vegetative composition and relative ape abundance. We compared habitats between these sites using conventional ground surveys and classified Landsat-7 ETM+ satellite images. We present density estimates via both standing-crop and marked-nest methods for the first time for sympatric apes of the Congo Basin. The marked-nest method was effective in depicting chimpanzee densities, but underestimated gorilla densities at both sites. Marked-nest surveys also revealed a dramatic decline in the ape population of Lokoué which coincided with a local Ebola epidemic. Normal baseline fluctuations in ape nest encounter rates during the repeated passages of marked-nest surveys were clearly distinguishable from a 80% decline in ape nest encounter rates at Lokoué. Our results showed that ape densities, habitat composition, and population dynamics differed between these populations in northern Congo. We emphasize the importance of intensifying monitoring efforts and further refinement of ape survey methods, as our results indicated that even the largest remaining ape populations in intact and protected forests are susceptible to sudden and dramatic declines.