Skeletal development in Pan paniscus with comparisons to Pan troglodytes

Fusion of skeletal elements provides markers for timing of growth and is one component of a chimpanzee's physical development. Epiphyseal closure defines bone growth and signals a mature skeleton. Most of what we know about timing of development in chimpanzees derives from dental studies on Pan troglodytes. Much less is known about the sister species, Pan paniscus, with few in captivity and a wild range restricted to central Africa. Here, we report on the timing of skeletal fusion for female captive P. paniscus (n = 5) whose known ages range from 0.83 to age 11.68 years. Observations on the skeletons were made after the individuals were dissected and bones cleaned. Comparisons with 10 female captive P. troglodytes confirm a generally uniform pattern in the sequence of skeletal fusion in the two captive species. We also compared the P. paniscus to a sample of three unknown‐aged female wild P. paniscus, and 10 female wild P. troglodytes of known age from the Taï National Park, Côte d'Ivoire. The sequence of teeth emergence to bone fusion is generally consistent between the two species, with slight variations in late juvenile and subadult stages. The direct‐age comparisons show that skeletal growth in captive P. paniscus is accelerated compared with both captive and wild P. troglodytes populations. The skeletal data combined with dental stages have implications for estimating the life stage of immature skeletal materials of wild P. paniscus and for more broadly comparing the skeletal growth rates among captive and wild chimpanzees (Pan), Homo sapiens, and fossil hominins. Am J Phys Anthropol 2012. © 2012 Wiley Periodicals, Inc.     

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.     

Female Coalitions Against Male Aggression in Wild Chimpanzees of the Budongo Forest

In the wild, female chimpanzees (Pan troglodytes) are subject to male aggression that at times can be prolonged or particularly violent. There are no reports of cooperative retaliation to such aggression, a strategy observed in the congeneric Pan paniscus, from the wild despite >4 decades of detailed behavioral study across a number of populations and its occurrence among captive female chimpanzees. If the reports from captivity represent an inherent capacity, then the absence of similar reports from wild populations suggests that females may be able to form coalitions only under appropriate ecological and demographic conditions. During a study of male and female aggressive interactions among chimpanzees of the Budongo Forest, Uganda, wild adult female chimpanzees sometimes formed coalitions with one another to retaliate against male aggression. This may be possible because these females tend to be more gregarious than in other populations of East African chimpanzees, as other studies of the same population have suggested; the extent and variation of female chimpanzee social strategies may, therefore, need reconsideration. Further, my observations strengthen the argument that at least some of the differences between chimpanzees and bonobos may be more of degree than of kind.     

Meat eating and ant dipping by wild chimpanzees in Sierra Leone

This report presents the first records of meat-eating and ant dipping by wild chimpanzees,Pan troglodytes, from Sierra Leone. The study was conducted in the proposed Outamba-Kilimi National Park, Northern Sierra Leone. Measurements of tools used to dip for driver ants, are compared with those from four other study sites in Africa. The results reveal some fundamentally common characteristics. From both faecal analysis and direct observation, evidence was found that the chimpanzees eat meat. These recordings indicate a varied choice of prey and add new species to those preyed upon by wild chimpanzees. These findings preliminarily support the idea that despite a wide geographical distribution throughout Africa, chimpanzees share some essential conventional behavioural patterns.     

Do bonobos copulate more frequently and promiscuously than chimpanzees?

The copulatory activities of bonobos (Pan paniscus) of Wamba, Zaire, were compared with those of chimpanzees (P. troglodytes schweinfurthii) of Mahale, Tanzania. The copulation rates of adult male bonobos were equal to or lower than those of adult male chimpanzees. The copulation rates of adult female bonobos were approximately equal to those of adult female chimpanzees who were in maximal genital swelling, but it should be much higher than those of the adult female chimpanzees throughout the birth interval. The copulation rates of adolescent male bonobos were lower than those of adolescent male chimpanzees, whereas the copulation rates of adolescent female bonobos were much higher than those of adolescent female chimpanzees. It was suggested that the bonobos of Wamba did not copulate more promiscuously than did the chimpanzees of Mahale. The female bonobos may show “receptivity”, whereas female chimpanzees may show rather “proceptivity”.     

Behavioral diversity in populations of free-ranging chimpanzees in Africa: is it culture?

Behavioral differences exist among populations of wild chimpanzees (Pan troglodytes, Hominoidea) across Africa. Deciding if these are cross-cultural differences demands careful interpretation and rigorous scrutiny. Even standard patterns like social grooming may show variation in detail between neighboring populations. Some patterns of tool use, such as using hammers to crack nuts, also vary across far western Africa. At least 37 populations of free-ranging chimpanzees show tool use, and 14 show at least one habitual pattern of tool use. Regional differences exist among the three subspecies or geographical races of chimpanzees. Convincing empirical demonstration of social customs and traditions in non-human species is problematical, and even something so simple in principle as innovation is hard to show in practice. However, culture need not depend on imitation, teaching, or language, either in humans or in other species.     

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.     

Using the Tools at Hand: Manual Laterality and Elementary Technology in Cebus spp. and Pan spp.

Cebus and Pan appear to be a remarkable example of evolutionary convergence in behavioral ecology. We examine their apparently analogous solutions to problems posed by laterality of hand function and elementary technology. We scrutinize appropriate published data in a meta-analysis, focusing on Cebus apella and C. capucinus and on Pan paniscus and P. troglodytes. We compare behavioral data in terms of captive versus wild, and tool use versus non-tool use, but notable gaps exist in the data, especially for bonobos. Cebus and Pan spp. are equivalent tool users in captivity, but chimpanzees are notably more extensively so in nature. For hand preference, captive bonobos and wild and captive chimpanzees show ambipreference for non-tool-use patterns. For both Cebus spp. and Pan spp., there is a tendency for individuals to be committed exclusively to one hand or the other for tool use. The data for laterality of hand function fit consistently into the five-level model proposed by McGrew and Marchant (1996).     

Leaf-swallowing in Nigerian chimpanzees: evidence for assumed self-medication

A field study in Gashaka, Nigeria, adds the fourth subspecies of chimpanzee, Pan troglodytes vellerosus, to the list of African ape populations in which leaf-swallowing occurs. Unchewed herbaceous leaves of Desmodium gangeticum (Leguminosae-Papilionoideae) were recovered in 4% of 299 faecal samples of wild chimpanzees and clumps of sharp-edged grass leaves in 2%. The ingestion is believed to serve self-medicatory purposes because the leaves had a rough surface or were sharp-edged (which could be related to parasite control through a self-induced increase of gut motility), were not chewed, were excreted whole (indicating that they were not ingested for nutritional purposes), leaf-swallowing was restricted to the rainy season (during which time parasite re-infections are more common), and parasitic worms (Oesophagostomum stephanostomum) were found together with the leaves. Submitted to: Primates, May 2005; revision: 26 Oct 2005     

On the nomenclature ofPan paniscus

In 1929 a subspecies of chimpanzee was classified asPan satyrus paniscus, a subspecies of theeastern chimpanzee, and elevated to species level,Pan paniscus, in 1933. Review of the literature indicates that this ape type was known since 1881 from several locations throughout the Congo Basin and first scientifically described in 1887 asTroglodytes niger var.marungensis, a subspecies of thewestern chimpanzee. The evidence presented here demonstrates that the synonymmarungensis was known and used as an earlier name. According to the International Code of Zoological Nomenclature, the earliest name awarded to a species is the one which has to be recognized in use. However, maintaining the emphasis on stability and assuming that to change the name would cause considerable confusion in the literature, it is this author's recommendation that the earlier namemarungensis be suppressed and the later synonympaniscus be conserved while an application is being considered for ruling by the International Commission on Zoological Nomenclature.     

Skeletal and dental growth and development in chimpanzees of the Taï National Park, Côte D'Ivoire

An extraordinary collection of 22 immature skeletons from Taï National Park, Côte d'Ivoire, has provided a rare opportunity to establish the timing of dental eruption and its correlation with skeletal fusion and morphometrics in wild chimpanzees of known chronological ages. Comparison of the immature Taï chimpanzees Pan troglodytes verus with adults from the same population show that sex differences in skeletal maturation apparently appear during the Juvenile II stage, about age 8. A few skeletons from other chimpanzee field sites conform to the dental and skeletal growth in Taï chimpanzees. The tempo of wild chimpanzee growth contrasts sharply with the rate demonstrated for captive individuals. Captive chimpanzees may mature as much as 3 years earlier. The ability to link physical development with field observations of immature chimpanzees increases our understanding of their life-history stages. These data provide an improved dataset for comparing the rates of growth among chimpanzees, Homo sapiens and fossil hominids.     

Body size and proportions in chimpanzees,with special reference toPan troglodytes schweinfurthii from Gombe National Park,Tanzania

Body weight, cranial capacity, linear and joint area data from ten free-ranging adult chimpanzees from Gombe National Park, Tanzania with known life histories allow study of variation in a local population and comparison to other populations ofPan troglodytes and toPan paniscus. Because individuals in the Gombe population are small compared to other common chimpanzees, they provide a useful comparison toPan paniscus. Body weight and some linear dimensions overlap withPan paniscus. However, cranial capacity, tooth size, and body proportions of Gombe individuals lie within the range of otherPan troglodytes and are distinct fromPan paniscus.     

Development of epiphyseal union in Japanese macaques of known chronological age

Forty epiphyseal unions were studied in the two subspecies of the Japanese macaque at known chronological ages. The age standards of the beginning and completion of epiphyseal union were estimated. The total score of the ratings of the unions revealed significant correlations with chronological age before 9 years of age. The linear regressions were calculated in each group of different sex and different subspecies in order to enable predictions to be made of the chronological age from the total score. Although males and females generally showed the same pattern of sequences, the unions of the females united earlier than those of the males in both subspecies before 9 years of age. The Yaku subspecies demonstrated an earlier union than the common Japanese macaque in both sexes before the age of 9 years old. The epiphyseal union of the Japanese macaque usually developed earlier than the reported union in the rhesus macaque. A large number of epiphyseal unions united at least partially and the total score deviated widely during the range from around 4 to 6 years of age. This period was in accordance with the adolescent growth period, especially in males, with rapid growth of body size as observed based on by somatometrical measurements. The skeletal growth of the trunk was generally late compared with that of the limbs. During the range after 8 years of age, some unions of the trunk united earlier in males than in females. The epiphyseal union could allow a more precise age estimation than the body mass or dental eruption during a certain range of ages. However, developmental estimations obtained from animals fed artificially, as the present samples were, must be applied with caution to wild animals.     

Interspecific interactions between wild pygmy chimpanzees (Pan paniscus) and red colobus (Colobus badius)

Interspecific interactions accompanied by physical contacts between wild pygmy chimpanzees (Pan paniscus) and red colobus (Colobus badius) were observed on three occasions at Wamba, Republic of Zaire. In all cases, the red colobus initiated the interactions by approaching the pygmy chimpanzees. Most of the pygmy chimpanzees, which were within 5 m of the red colobus, were juveniles or infants but the adult male pygmy chimpanzees never showed any interest in the red colobus. The red colobus groomed the chimpanzees in two cases, but the latter never groomed the former. No true aggressive interactions were observed between the two species. The lack of any evidence of hunting of red colobus through longitudinal studies of the pygmy chimpanzees of Wamba, together with the present observations, suggests that red colobus are probably not targets of hunting by the pygmy chimpanzees.     

External body dimensions ofPan paniscus andPan troglodytes chimpanzees

Postcranial skeletal studies have demonstrated thatPan paniscus is a more gracile animal thanPan troglodytes, with different arm to leg proportions. Published data on external body dimensions are extremely rare forPan paniscus, however. We present here a series of such measures for a sample ofpaniscus, and we compare these to similar measures forPan troglodytes. This comparison further clarifies the morphological distinctions between the two chimpanzee species, and indicates that bonobos have longer legs and smaller chest girths relative to overall body height than doPan troglodytes chimpanzees.     

Observations on the meat-eating behavior of wild bonobos (Pan paniscus) at Wamba,Republic of Zaire

Meat-eating behavior of wild bonobos (Pan paniscus) was witnessed on two occasions at Wamba, Republic of Zaire. Only flying squirrels were observed to be eaten by the bonobos. Several bonobos gathered around the possessor of the meat and showed interest in the meat on all occasions. Begging behavior was noted on one of the two occasions, but the possessor of the meat ignored it. No sharing of meat was seen on either occasion. The exclusive targets of hunting by bonobos are apparently small mammals, such as flying squirrels and infant duikers, since evidence of meat eating by wild bonobos, which have been studied for more than fifteen years, has been restricted to these mammals. The bonobos at Wamba may have a specialized “prey image”, as in the case of the chimpanzees (Pan troglodytes) of the Tai forest, and certain medium-sized or small mammals may not conform to this image.     

Comparison of behavioral sequence of copulation between chimpanzees and bonobos

We compared sex differences in behaviors leading to copulation of chimpanzees (Pan troglodytes) in the Kalinzu Forest, Uganda with those of bonobos (Pan paniscus) at Wamba, D.R. Congo, using the same definition. Female chimpanzees were more likely to initiate copulation than female bonobos. While most of copulations (96%) were initiated by males in bonobos, among chimpanzees only 63% of copulations were initiated by males. Female bonobos initiated an interaction leading to copulation when males approached them within a short distance. On the other hand, both male and female chimpanzees initiated behavior at a longer distance. Higher proceptivity and a higher copulation rate during the maximal swelling period of female chimpanzees might suggest that they gain greater benefits from a high frequency of copulations than do female bonobos.     

Chimpanzee microsatellite PCR primers applied to paternity testing in a captive colony

Previously designed primers for the polymerase chain reaction (PCR) amplifying microsatellite DNA segments containing GT/AC dinucleotide repeats in the chimpanzee (Pan troglodytes) genome were used for paternity testing in a breeding colony in captivity. Combinations of three PCR primers identified the fathers of all the tested 40 chimpanzees born in an eight-year period. The results suggested: (1) a positive (though not conclusive) correlation between male rank and number of offspring; (2) choice of mating partners by the female rather than by the male; and (3) absence of stable mating pairs over the years. For studies of chimpanzees in captivity and in the wild, these primers should be useful for paternity testing, for investigating genetic variations, and for improving genetic maintenance of breeding colonies.     

Vertebrate Predation and Food-Sharing in Cebus and Pan

Capuchins and chimpanzees are the only nonhuman primates apart from baboons known to prey systematically upon relatively large vertebrates. Vertebrate predation is common and well documented in Pan troglodytes, rare in Pan paniscus, and commonly reported but infrequently studied in Cebus. Food-sharing is common in both Pan species but rarely reported for wild capuchins. I present data on vertebrate predation and food-sharing by white-faced capuchins (Cebus capucinus) from ongoing field studies at Santa Rosa National Park, Costa Rica. We have observed 106 successful predation events resulting in the capture of 156 prey items during 2929 observation hr (5.35 prey per 100 hr). Squirrels and nestling coatis comprised half of the prey taken; the remainder were mainly nestling birds and eggs. Adult males took 52% of all prey and 67% of squirrels. Squirrels are actively hunted and about 65% of them are adults. I estimated that the average capuchin group kills 43–50 squirrels annually, mostly during the dry season. Capuchins hunt squirrels in groups 81% of the time, and 17% of hunts are successful. There is no evidence for cooperative hunting, but occasional collaboration is suggested. Rates of food-sharing were low (1.7 per 100 hr), and meat was the only food shared between adults. I compare predation and food-sharing in C. capucinus with published data for Pan troglodytes, primarily in Gombe and Taï National Parks. I discuss sex differences, hunting strategies, the relationship between hunting and food-sharing, and various ecological and social factors that may promote vertebrate predation in Pan and Cebus.     

Behavioral Ecology of Sympatric Chimpanzees and Gorillas in Bwindi Impenetrable National Park,Uganda: Diet

Via a field study of chimpanzees (Pan troglodytes schweinfurthii) and gorillas (Gorilla gorilla beringei) in Bwindi Impenetrable National Park, Uganda, we found that their diets are seasonally similar, but diverge during lean seasons. Bwindi chimpanzees fed heavily on fruits of Ficus sp., which were largely ignored by the gorillas. Bwindi gorilla diet was overall more folivorous than chimpanzee diet, but was markedly more frugivorous than that of gorillas in the nearby Virunga Volcanoes. During 4 mo of the year Bwindi gorilla diet included more food species than that of the chimpanzees. Three factors in particular—seasonal consumption of fibrous foods by gorillas, interspecific differences in preferred fruit species, and meat consumption by chimpanzees—contributed to dietary divergence between the two species. When feeding on fruits, gorillas ate Myrianthus holstii more frequently than chimpanzees did, while chimpanzees included more figs in their annual diet. Chimpanzee diet included meat of duikers and monkeys; gorilla frequently consumed decaying wood.