Sexual Dimorphism and Facial Growth Beyond Dental Maturity in Great Apes and Gibbons

The great apes and gibbons are characterized by extensive variation in degree of body size and cranial dimorphism, but although some studies have investigated how sexual dimorphism in body mass is attained in these species, for the majority of taxa concerned, no corresponding work has explored the full extent of how sexual dimorphism is attained in the facial skeleton. In addition, most studies of sexual dimorphism combine dentally mature individuals into a single “adult” category, thereby assuming that no substantial changes in size or dimorphism take place after dental maturity. We investigated degree and pattern of male and female facial growth in Pan troglodytes troglodytes, Pan paniscus, Gorilla gorilla gorilla, Pongo pygmaeus, and Hylobates lar after dental maturity through cross-sectional analyses of linear measurements and geometric mean values of the facial skeleton and age-ranking of individuals based on molar occlusal wear. Results show that overall facial size continues to increase after dental maturity is reached in males and females of Gorilla gorilla gorilla and Pongo pygmaeus, as well as in the females of Hylobates lar. In male Pongo pygmaeus, adult growth patterns imply the presence of a secondary growth spurt in craniofacial dimensions. There is suggestive evidence of growth beyond dental maturity in the females of Pan troglodytes troglodytes and Pan paniscus, but not in the males of those species. The results show the presence of statistically significant facial size dimorphism in young adults of Pan paniscus and Hylobates lar, and of near statistical significance in Pan troglodytes troglodytes, but not in older adults of those species; adults of Gorilla gorilla gorilla and Pongo pygmaeus are sexually dimorphic at all ages after dental maturity. The presence of sex-specific growth patterns in these hominoid taxa indicates a complex relationship between socioecological selective pressures and growth of the facial skeleton.     

Sexual dimorphism in relative sacral breadth among catarrhine primates

As the sacrum contributes to the size and shape of the birth canal, the sexually dimorphic sacrum of humans is frequently interpreted within obstetric contexts. However, while the human sacrum has been extensively studied, comparatively little is known about sacral morphology in nonhuman primates. Thus, it remains unclear whether sacral sexual dimorphism exists in other primates, and whether potential dimorphism is primarily related to obstetrics or other factors such as body size dimorphism. In this study, sacra of Homo sapiens, Hylobates lar, Nasalis larvatus, Gorilla gorilla, Pongo pygmaeus, Pan troglodytes, and Pan paniscus were evaluated for sexual dimorphism in relative sacral breadth (i.e., the ratio of overall sacral breadth to first sacral vertebral body breadth). Homo sapiens, H. lar, N. larvatus, and G. gorilla exhibit dimorphism in this ratio. Of these, the first three species have large cephalopelvic proportions, whereas G. gorilla has small cephalopelvic proportions. P. pygmaeus, P. troglodytes, and P. paniscus, which all have small cephalopelvic proportions, were not dimorphic for relative sacral breadth. We argue that among species with large cephalopelvic proportions, wide sacral alae in females facilitate birth by increasing the pelvic inlet's transverse diameter. However, given the small cephalopelvic proportions among gorillas, an obstetric basis for dimorphism in relative sacral breadth appears unlikely. This raises the possibility that sacral dimorphism in gorillas is attributable to selection for relatively narrow sacra in males rather than relatively broad sacra in females. Accordingly, these results have implications for interpreting pelvic dimorphism among fossil primates, including hominins. Am J Phys Anthropol 152:435–446, 2013. © 2013 Wiley Periodicals, Inc.     

Food washing and placer mining in captive great apes

Sweet potato washing and wheat placer mining in Japanese macaques (Macaca fuscata) are among the most well known examples of local traditions in non-human animals. The functions of these behaviors and the mechanisms of acquisition and spread of these behaviors have been debated frequently. Prompted by animal caretaker reports that great apes [chimpanzees (Pan troglodytes), bonobos (Pan paniscus), gorillas (Gorilla gorilla), and orangutans (Pongo abelii)] at Leipzig Zoo occasionally wash their food, we conducted a study of food washing behaviors that consisted of two parts. In the first part we assessed the current distribution of the behavior on the basis of caretaker reports. In the second (experimental) part, we provided subjects individually with a water basin and two types of food (apples and cereal) that was either clean or covered/mixed with sand. We found that subjects of all species (except gorillas) placed apples in the water before consumption, and that they did so more often when the apples were dirty than when they were clean. Several chimpanzees and orangutans also engaged in behaviors resembling wheat placer mining.     

Immunoglobulin Gm allotypes in apes: Comparison with man

Serum samples from 245 apes (184 Pan troglodytes, five Pan paniscus, 28 Gorilla gorilla, 23 Pongo pygmaeus abelei, and five Pongo pygmaeus pygmaeus) were tested for G1m (1,2,3,17), G2m (23), and G3m (5,6,10,11,13,14,15,16,21,24,28) immunoglobulin allotypes by the classical method of inhibition of hemagglutination. Some phenotypes are species specific while a few are shared by man and African apes.     

Food-Associated Calling in Gorillas (Gorilla g. gorilla) in the Wild

Many nonhuman primates produce food-associated vocalizations upon encountering or ingesting particular food. Concerning the great apes, only food-associated vocalizations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) have been studied in detail, providing evidence that these vocalizations can be produced flexibly in relation to a variety of factors, such as the quantity and quality of food and/or the type of audience. Only anecdotal evidence exists of eastern (Gorilla beringei) and western gorillas (Gorilla gorilla) producing food-associated vocalizations, termed singing or humming. To enable a better understanding of the context in which these calls are produced, we investigated and compared the vocal behavior of two free-ranging groups of western lowland gorillas (Gorilla g. gorilla) at Mondika, Republic of Congo. Our results show that (a) food-associated call production occurs only during feeding and not in other contexts; (b) calling is not uniformly distributed across age and sex classes; (c) calls are only produced during feeding on specific foods; and (d) normally just one individual gives calls during group feeding sessions, however, certain food types elicit simultaneous calling of two or more individuals. Our findings provide new insight into the vocal abilities of gorillas but also carry larger implications for questions concerning vocal variability among the great apes. Food-associated calls of nonhuman primates have been shown to be flexible in terms of when they are used and who they are directed at, making them interesting vocalizations from the viewpoint of language evolution. Food-associated vocalizations in great apes can offer new opportunities to investigate the phylogenetic development of vocal communication within the primate lineage and can possibly contribute novel insights into the origins of human language.     

Epidermal patterns of the hands and feet of the pygmy chimpanzee (Pan paniscus)

The characteristics of the epidermal ridge system were studied in a series of eighteen lesser or pygmy chimpanzees (Pan paniscus). The general ridge alignments are very similar to those of the chimpanzee (Pan troglodytes); Biegert ('61). On the average the pattern intensity (P.I.) of the palm configurations is considerably higher in the pygmy chimpanzee than in the chimpanzee, thus representing the highest total palm pattern intensity of all species of the Hominoidea. The sole configurations show parallel main results to those of the palm; however, the decreased sole pattern frequency of the pygmy chimpanzee is of a smaller predominance only as compared to the values of the other species of this superfamily. The preliminary data on the finger tip patterns, translated into P.I. values, are much higher than in chimpanzees and within the range of the mean values of gorillas (Brehme, '73), while those of the toes of pygmy chimpanzees seem to possess the lowest P.I. values of the African apes.     

The role of taste in food selection by African apes: implications for niche separation and overlap in tropical forests

Ripe fruit eating shapes the behavior of most of the apes. Gorillas (Gorilla gorilla) and chimpanzees (Pan troglodytes) are very different sizes and, consequently, have been traditionally viewed as ecologically distinct, but few studies have explored the behavioral and physiological foundations of their diets. Debate continues on the extent that large-bodied gorillas may be less selective and more opportunistic fruit eaters than chimpanzees. Taste responses have been predicted to relate to body size and digestive strategies. This study employs laboratory research on taste perception and discrimination among captive zoo-housed chimpanzees and relates it to previous work on gorillas to better characterize diets and niche separation among these apes. During the captive trials, differences were recorded in consumption patterns of water and varying concentrations of dilute aqueous fructose (sweet) and tannic acid solutions (astringent), compounds commonly found in wild foods. The chimpanzees exhibited similar preference thresholds for fructose (50 mM) to other primates studied. They exhibited slightly lower inhibition thresholds for tannic acid solutions than gorillas, but higher than smaller primates studied to date. These preliminary findings suggest that tannin tolerance may well be mediated by body size, though possible species differences in salivary proteins or other sensory differences remain to be explored. This research furthers our efforts to understand the roles of body size and physiological adaptations in shaping diet and niche separation of chimpanzees and gorillas.     

Review of medical literature of great apes in the 1980s

The medical problems of great apes including gorillas (Gorilla gorilla), orangutans (Pongo pymaeus), and chimpanzees (Pan sp.) published during the last decade are reviewed. Anesthetic techniques, diseases or organ systems, neoplasia, infectious diseases, and reproductive problems are reviewed. Gonadal tumors and atherosclerosis in great apes appear frequently in the literature. Diseases with suspected viral etiology include papillomas in chimpanzees, retrovirus-associated lymphomas in gorillas, and various herpesvirus disease. Technology developed for human medicine has expanded the diagnostic opportunities for clinicians working with great apes.     

Great apes track hidden objects after changes in the objects' position and in subject's orientation

Eight chimpanzees (Pan troglodytes), five bonobos (Pan paniscus), five gorillas (Gorilla gorilla), and seven orangutans (Pongo pygmaeus) were presented with two invisible object displacement tasks. In full view of the subject, a food item was hidden under one of three opaque cups resting on a platform and, after an experimental manipulation, the subject was allowed to select one of the cups. In the rotation task, the platform was rotated 180° while the subject remained stationary. In the translocation task, the platform remained stationary while the subject walked to the opposite side from where she saw the reward being hidden. The final position of the food relative to the subject was equivalent in both tasks. Single displacement trials consisted of only one manipulation, either a rotation or a translocation, whereas double displacement trials consisted of both a rotation and a translocation. We also included no displacement trials in which no displacements took place. No displacement trials were easier than single displacements which, in turn, were easier than double displacements. Unlike earlier studies with children, there was no difference in performance between rotation and translocation displacements. Overall, apes performed above chance in all conditions, but chimpanzees outperformed the other species. This study reinforces the notion that the great apes use an allocentric spatial coding. Am. J. Primatol. 72:349–359, 2010. © 2010 Wiley‐Liss, Inc.     

Apes in a changing world – the effects of global warming on the behaviour and distribution of African apes

Aim In this study we use a modelling approach to identify: (1) the factors responsible for the differences in ape biogeography, (2) the effects that global warming might have on distribution patterns of African apes, (3) the underlying mechanisms for these effects, and (4) the implications that behavioural flexibility might be expected to have for ape survival. All African apes are highly endangered, and the need for efficient conservation methods is a top priority. The expected changes in world climate are likely to further exacerbate the difficulties they face. Our study aims to further understand the mechanisms that link climatic conditions to the behaviour and biogeography of ape species. Location Africa. Method We use an existing validated time budgets model, derived from data on 20 natural populations of gorillas (Gorilla beringei and Gorilla gorilla) and chimpanzees (Pan troglodytes and Pan paniscus), which specifies the relationship between climate, group size, body weight and time available for various activities, to predict ape distribution across Africa under a uniform worst‐case climate change scenario. Results We demonstrate that a worst‐case global warming scenario is likely to alter the delicate balance between different time budget components. Our model points to the importance of annual temperature variation, which was found to have the strongest impact on ape biogeography. Our simulation indicates that rising temperatures and changes in rainfall patterns are likely to have strong effects on ape survival and distribution, particularly for gorillas. Even if they behaved with maximum flexibility, gorillas may not be able to survive in most of their present habitats if the climate was to undergo extreme changes. The survival of chimpanzees was found to be strongly dependent on the minimum viable group size required. Main conclusions Our model allows us to explore how climatic conditions, individual behaviour and morphological traits may interact to limit the biogeographical distributions of these species, thereby allowing us to predict the effects of climate change on African ape distributions under different climate change regimes. The model suggests that climate variability (i.e. seasonality) plays a more important role than the absolute magnitude of the change, but these data are not normally provided by climate models.     

A chimpanzee-derived chromosome-specific alpha satellite DNA sequence conserved between chimpanzee and human

We describe a cloned 2.7 kb alpha satellite sequence, Pan-3, from the pygmy chimpanzee (Pan paniscus) that specifically hybridizes in situ to chromosome 19 in the pygmy chimpanzee and to the homeologous human chromosome, no. 17. Using high stringency conditions of hybridization on Southern blots, this sequence hybridized to DNA from both species of chimpanzee (P. paniscus and P. troglodytes) and from human but not to DNA from gorilla (Gorilla gorilla) or orangutan (Pongo pygmaeus). Partial sequence analysis showed that Pan-3 and a previously described human chromosome 17-specific clone have up to 91% sequence identity. To our knowledge this is the highest sequence similarity reported between alphoid subsets from human and any other primate.by T.C. Hsu     

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.     

Estimation of African apes’ body size from postcranial dimensions

We examine how African apes’ postcranial skeletal dimensions and their combinations are related to body size, as represented by trunk volume, within sex-specific samples of a total of 39 central chimpanzees (Pan troglodytes troglodytes) and 34 western gorillas (Gorilla gorilla gorilla). We examine this relationship by determining the strength of the correlation between selected skeletal dimensions and trunk volume. The findings indicate that sex should be taken into account when possible. Most two-predictor models perform better than most single-predictor models. Interspecific regressions based on log-transformed variables and sex/species-specific regression based on raw variables perform about equally well.     

Scapula form and locomotion in chimpanzee evolution

A number of primatologists have followed Coolidge (Am. J. Phys. Anthropol. 18:1–57, 1933) in suggesting that 1) there are significant shape differences in scapula form between pygmy and common chimpanzees, 2) scapulae of P. paniscus resemble those of hylobatids more than do those of P. troglodytes, and 3) therefore pygmy chimpanzees may exhibit a greater component of arm-swinging and other arboreal behaviors than common chimpanzees. In this paper I utilize a comparative analysis of ontogenetic allometries of linear dimensions to determine shape differences in the scapulae of adult pygmy and common chimpanzees and to clarify size-related changes in shape resulting from ontogenetic scaling, i.e., the differential extension of common patterns of growth allometry. Results demonstrate that the scapulae of adult P. paniscus are relatively narrower (in a direction approximately perpendicular to the scapula spine) than those of P. troglodytes, supporting Coolidge's original claim. The allometric analysis further demonstrates, however, that the two chimpanzee species exhibit ontogenetic scaling for all proportions of the scapula examined. Thus, adult pygmy chimpanzees have the scapula proportions observed in small adult and subadult P. troglodytes of comparable scapula size. The implications of this finding for past claims concerning differences in locomotor behavior between the species are discussed. This work lends additional support to previous studies that have demonstrated a high frequency of ontogenetic scaling within the genus Pan and a pedomorphic or juvenilized morphology in the pygmy chimpanzee.     

Population Density of Chimpanzees and Gorillas in the Petit Loango Reserve,Gabon: Employing a New Method to Distinguish Between Nests of the Two Species

We studied the vegetation and population density of chimpanzees (Pan troglodytes troglodytes) and gorillas (Gorilla gorilla gorilla) in the Petit Loango Reserve, Gabon. The study site consists mainly of primary and secondary forest, and it also includes patches of savanna, inundated forest, and coastal scrub. The density of herbaceous plants of Marantaceae and Zingiberaceae, which serve as important foods for great apes at other study sites, is extremely low. It was very difficult to distinguish between the nests of chimpanzees and gorillas because most gorilla nests were made in trees. We developed a new method to identify the builder of nests via a combination of field observation of nests and fecal samples, and examination of hair samples under a scanning electron microscope. Nests of chimpanzees were mainly in primary forest, and the estimated density (0.78 individual per km ² ) is higher than the average density in Gabon and comparable to the nest density in the Lopé Reserve, Gabon. Nests of gorillas were mainly in secondary forest, and their estimated density (0.21) is similar to the average next density in Gabon but lower than the gorilla nest density in the Lopé Reserve. The low density of herbaceous foods seemed to influence the density of gorillas but not the density of chimpanzees.     

Food Preferences Among Captive Western Gorillas (Gorilla gorilla gorilla) and Chimpanzees (Pan troglodytes)

I used a zoological park setting to address food preferences among gorillas (Gorilla gorilla gorill) and chimpanzees (Pan troglodytes). Gorillas and chimpanzees are different sizes, and consequently, have been traditionally viewed as ecologically distinct. Sympatric western gorillas and chimpanzees have proved difficult to study in the wild. Limited field data have provided conflicting information about whether gorillas are fundamentally different from chimpanzees in diet and behavior. Fruit eating shapes the behavior of most apes, but it is unclear whether the large-bodied gorillas are an exception to this rule, specifically whether they are less selective and more opportunistic fruit eaters than chimpanzees are. My research provides experimental observational data to complement field data and to better characterize the diets and food preferences of the African apes. During laboratory research at the San Francisco Zoological Gardens, I examined individual and specific differences in food preferences of captive gorillas and chimpanzees via experimental paired-choice food trials with foods that varied in nutritional content. During the study, I offered 2500 paired-food choices to 6 individual gorillas and 2000 additional pairs to them as a group. I also proffered 600 food pairs to 4 individual chimpanzees. Despite expectations of the implications of body size differences for diet, gorillas and chimpanzees exhibited similar food preferences. Both species preferred foods high in non-starch sugars and sugar-to-fiber ratios, and low in total dietary fiber. Neither species avoided foods containing tannins. These data support other suggestions of African apes sharing a frugivorous adaptation.     

A Legacy of Low-Impact Logging does not Elevate Prevalence of Potentially Pathogenic Protozoa in Free-Ranging Gorillas and Chimpanzees in the Republic of Congo: Logging and Parasitism in African Apes

Many studies have examined the long-term effects of selective logging on the abundance and diversity of free-ranging primates. Logging is known to reduce the abundance of some primate species through associated hunting and the loss of food trees for frugivores; however, the potential role of pathogens in such primate population declines is largely unexplored. Selective logging results in a suite of alterations in host ecology and forest structure that may alter pathogen dynamics in resident wildlife populations. In addition, environmental pollution with human fecal material may present a risk for wildlife infections with zoonotic protozoa, such as Cryptosporidium and Giardia. To better understand this interplay, we compared patterns of infection with these potentially pathogenic protozoa in sympatric western lowland gorillas (Gorilla gorilla gorilla) and chimpanzees (Pan troglodytes troglodytes) in the undisturbed Goualougo Triangle of Nouabalé-Ndoki National Park and the adjacent previously logged Kabo Concession in northern Republic of Congo. No Cryptosporidium infections were detected in any of the apes examined and prevalence of infection with Giardia was low (3.73% overall) and did not differ between logged and undisturbed forest for chimpanzees or gorillas. These results provide a baseline for prevalence of these protozoa in forest-dwelling African apes and suggest that low-intensity logging may not result in long-term elevated prevalence of potentially pathogenic protozoa.     

Skeletal evidence of trauma in African apes, with special reference to the gombe chimpanzees

Incidence of cranial and postcranial skeletal trauma was investigated in samples of chimpanzees (Pan troglodytes troglodytes, P. troglodytes schweinfurthii), lowland gorillas (Gorilla gorilla gorilla), and bonobos (P. paniscus). The larger (adult) samples of chimpanzees (N=127 crania, 92 postcrania) and gorillas (N=136 crania, 62 postcrania) are curated at the Powell-Cotton Museum, Birchington, U.K. The bonobo collection (N=71 crania, 15 postcrania) is housed the Musée Royal de l'Afrique Centrale in Tervuren, Belgium. In addition, data were collected on the small but extremely well-documented skeletal sample from Gombe National Park (N=14 crania, 13 postcrania — including adults and adolescents). Cranial injuries, including healed fractures and bite wounds, were fairly frequent in the museum collection of chimpanzees (5.5% of individuals), but were twice as frequent in gorillas (11.0%). In the Gombe sample an even higher incidence was observed (28.6% of individuals). Bonobos, however, showed the lowest incidence of cranial trauma found among any of the African ape samples (1.4% of individuals). Postcranial trauma, documented most clearly by healed fractures, was seen in 21.7% of the Powell-Cotton chimpanzees, 30.8% of Gombe chimpanzees, 17.7% of gorillas, and in 13.3% of bonobos. Most of these lesions were found in the upper appendage. Nevertheless, highly debilitating healed fractures of the femur were also noted, most frequently and severe in female gorillas. The pattern of injuries suggests serious risks of falling in all free-ranging African apes, but also (in chimpanzees and gorillas) considerable risk from interindividual aggression, especially for males.     

Food Neophobia and Social Learning Opportunities in Great Apes

Finding food resources and maintaining a balanced diet are major concerns for all animals. A compromise between neophobia and neophilia is hypothesised to enable animals to enlarge their diet while limiting the risk of poisoning. However, little is known about how primates respond to novel food items and whether their use is socially transmitted. By comparing how four different species of great apes respond to novel food items, we investigated how differences in physiology (digestive tract size and microbial content), habitats (predictability of food availability), and social systems (group size and composition) affect their response toward novelty. We presented two familiar foods, one novel fruit, four novel aromatic plants from herbal medicine, and kaolin to captive chimpanzees (Pan troglodytes), western gorillas (Gorilla gorilla), Bornean orangutans (Pongo pygmaeus) and Sumatran orangutans (Pongo abelii). We recorded smelling, approach-taste delays, ingestion, interindividual observations, and food transfers with continuous sampling. We found that behaviors differed between the apes: chimpanzees were the most cautious species and observed their conspecifics handling the items more frequently than the other apes. Close observations and food transfers were extremely rare in gorillas in comparison to orangutans and chimpanzees. We suggest that a low neophobia level reflects an adaptive response to digestive physiological features in gorillas and to unpredictable food availability in orangutans. Social interactions appeared to be predominant in chimpanzees and in both orangutan species to overcome food neophobia. They reflect higher social tolerance and more opportunities for social learning and cultural transmission in a feeding context.