Permanent tooth mineralization in bonobos (Pan paniscus) and chimpanzees (P. troglodytes)

The timing of tooth mineralization in bonobos (Pan paniscus) is virtually uncharacterized. Analysis of these developmental features in bonobos and the possible differences with its sister species, the chimpanzee (P. troglodytes), is important to properly quantify the normal ranges of dental growth variation in closely related primate species. Understanding this variation among bonobo, chimpanzee and modern human dental development is necessary to better contextualize the life histories of extinct hominins. This study tests whether bonobos and chimpanzees are distinguished from each other by covariance among the relative timing and sequences of tooth crown initiation, mineralization, root extension, and completion. Using multivariate statistical analyses, we compared the relative timing of permanent tooth crypt formation, crown mineralization, and root extension between 34 P. paniscus and 80 P. troglodytes mandibles radiographed in lateral and occlusal views. Covariance among our 12 assigned dental scores failed to statistically distinguish between bonobos and chimpanzees. Rather than clustering by species, individuals clustered by age group (infant, younger or older juvenile, and adult). Dental scores covaried similarly between the incisors, as well as between both premolars. Conversely, covariance among dental scores distinguished the canine and each of the three molars not only from each other, but also from the rest of the anterior teeth. Our study showed no significant differences in the relative timing of permanent tooth crown and root formation between bonobos and chimpanzees. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.     

The behavior of a group of captive pygmy chimpanzees (Pan paniscus)

A group of captive pygmy chimpanzees (Pan paniscus) was studied in the San Diego Zoological Gardens. The behavior patterns that these animals exhibit are described. Each of these behavior patterns is compared to those described for wild and captive common chimpanzees (P. troglodytes). Differences in behavior between these two species are attributed to specialization of the pygmy chimpanzee to a rain forest habitat and to a monogamous social system.     

Mandibular Shape, Ontogeny and Dental Development in Bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes)

The postnatal ontogenetic patterns and processes that underlie species differences in African ape adult mandibular morphology are not well understood and there is ongoing debate about whether African ape faces and mandibles develop via divergent or parallel trajectories of shape change. Using three-dimensional (3D) morphometric data, we first tested when in postnatal development differences in mandibular shape are initially evident between sister species Pan troglodytes and P. paniscus. Next, we tested whether each species has a distinct and non-parallel trajectory of mandibular development. Mandibles sampled across a broad developmental range of wildshot bonobos (n = 44) and chimpanzees (n = 59) were radiographed and aged from their dental development. We then collected 3D landmark surface data from all the mandibles. A geometric morphometric analysis of size-corrected 3D data found that bonobos and chimpanzees had parallel and linear ontogenetic trajectories of mandibular shape change. In contrast, mandibular shape was statistically different between P. paniscus and P. troglodytes as early as infancy, suggesting that species shape differences are already established near or before birth. A linear and stable trajectory of shape change suggests that mandibular ontogeny in these apes is unimpacted by non-linear variation in tooth developmental timing.     

Body mass and growth rates in captive chimpanzees (Pan troglodytes) cared for in African wildlife sanctuaries,zoological institutions,and research facilities

Captive chimpanzees (Pan troglodytes) mature earlier in body mass and have a greater growth rate compared to wild individuals. However, relatively little is known about how growth parameters compare between chimpanzees living in different captive environments. To investigate, body mass was measured in 298 African sanctuary chimpanzees and was acquired from 1030 zoological and 442 research chimpanzees, using data repositories. An analysis of covariance, adjusting for age, was performed to assess same-sex body mass differences between adult sanctuary, zoological, and research populations. Piecewise linear regression was performed to estimate sex-specific growth rates and the age at maturation, which were compared between sexes and across populations using extra-sum-of-squares F tests. Adult body mass was greater in the zoological and resarch populations compared to the sanctuary chimpanzees, in both sexes. Male and female sanctuary chimpanzees were estimated to have a slower rate of growth compared with their zoological and research counterparts. Additionally, male sanctuary chimpanzees were estimated to have an older age at maturation for body mass compared with zoological and research males, whereas the age at maturation was similar across female populations. For both the zoological and research populations, the estimated growth rate was greater in males compared to females. Together, these data contribute to current understanding of growth and maturation in this species and suggest marked differences between the growth patterns of chimpanzees living in different captive environments.     

Inter-menstrual intervals in captive bonobosPan paniscus

In this study we provide new data on the duration of the inter-menstrual intervals of six captive female bonobos (Pan paniscus). We found that the mean duration of the inter-menstrual interval was about 34 days. This lies close to the average value of 37 days that has been reported for common chimpanzees (Pan troglodytes).     

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.     

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.     

A quantitative comparison of terrestrial herbaceous food consumption by Pan paniscus in the Lomako Forest,Zaire, and Pan troglodytes in the Kibale Forest,Uganda

Differences in the social organization and dental morphology of Pan paniscus (bonobos) and Pan troglodytes (chimpanzees) have been related to differences in the spatiotemporal availability of food and its exploitation. The presence of abundant terrestrial herbaceous vegetation (THV) in the bonobo's habitat and the apparent greater reliance on herbs for food has been used to explain differences in party size and, by extension, social organization. Using fecal analysis, we assess quantitatively the amount of herbaceous foods consumed by Pan paniscus in the Lomako Forest, Zaire, compared to similar data for Pan troglodytes in the Kibale Forest, Uganda. We examine this data in the context of spatiotemporal patterns of availability of herbaceous foods and fruit, as well as their nutritional content. The results support the suggestion that bonobos consume more herbaceous food than do the Kibale chimpanzees and that these foods are more prevalent in the bonobo's habitat than in the Kibale Forest. However, temporal changes in fruit availability and herb consumption, along with nutritional analyses, suggest that chimpanzees consume herbs as a fallback source of carbohydrates, whereas bonobos consume herbs as a source of protein regardless of season or fruit abundance. Available data suggest that party size while feeding on terrestrial herbs is restricted at both sites, but a determination of the relative strength of this constraint is not possible at this time. Difficulties in methods used for data collection are discussed and areas where more information is needed are highlighted. © 1994 Wiley-Liss, Inc.     

Growth of wild and laboratory born chimpanzees

The skeletal remains of a wild juvenile chimpanzee,Pan troglodytes verus, of known chronological age are measured and found to be smaller than laboratory born and fed juveniles of the same age. Other wild born immature skeletal materials of all the three subspecies ofPan troglodytes, including both known and estimated chronological ages, are also smaller than laboratory born chimpanzees when comparisons are made on corresponding age groups. Differences between wild and laboratory born chimpanzees are larger in the limb bones than in the cranium. Limb bones of laboratory individuals grow earlier than those of wild ones regardless of subspecies. Small limb bone size of wild chimpanzees is discussed in terms of life processes.     

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.     

Ontogeny and the evolution of adult body size dimorphism in apes

This analysis investigates the ontogeny of body size dimorphism in apes. The processes that lead to adult body size dimorphism are illustrated and described. Potential covariation between ontogenetic processes and socioecological variables is evaluated. Mixed-longitudinal growth data from 395 captive individuals (representing Hylobates lar [gibbon], Hylobates syndactylus [siamang], Pongo pygmaeus [orangutan], Gorilla gorilla [gorilla], Pan paniscus [pygmy chimpanzee], and Pan troglodytes [“common” chimpanzee]) form the basis of this study. Results illustrate heterogeneity in the growth processes that produce ape dimorphism. Hylobatids show no sexual differentiation in body weight growth. Adult body size dimorphism in Pongo can be largely attributed to indeterminate male growth. Dimorphism in African apes is produced by two different ontogenetic processes. Both pygmy chimpanzees (Pan paniscus) and gorillas (Gorilla gorilla) become dimorphic primarily through bimaturism (sex differences in duration of growth). In contrast, sex differences in rate of growth account for the majority of dimorphism in common chimpanzees (Pan troglodytes). Diversity in the ontogenetic pathways that produce adult body size dimorphism may be related to multiple evolutionary causes of dimorphism. The lack of sex differences in hylobatid growth is consistent with a monogamous social organization. Adult dimorphism in Pongo can be attributed to sexual selection for indeterminate male growth. Interpretation of dimorphism in African apes is complicated because factors that influence female ontogeny have a substantial effect on the resultant adult dimorphism. Sexual selection for prolonged male growth in gorillas may also increase bimaturism relative to common chimpanzees. Variation in female growth is hypothesized to covary with foraging adaptations and with differences in female competition that result from these foraging adaptations. Variation in male growth probably corresponds to variation in level of sexual selection. © 1995 Wiley-Liss, Inc.     

Ultrasonographic monitoring of fetal development in unrestrained bonobos (Pan paniscus) at the Milwaukee County Zoo

The bonobo, Pan paniscus, is one of the most endangered primate species. In the context of the Bonobo Species Survival Plan^®, the Milwaukee County Zoo established a successful breeding group. Although the bonobo serves as a model species for human evolution, no prenatal growth curves are available. To develop growth graphs, the animals at the Milwaukee County Zoo were trained by positive reinforcement to allow for ultrasound exams without restraint. With this method, the well being of mother and fetus were maintained and ultrasound exams could be performed frequently. The ovulation date of the four animals in the study was determined exactly so that gestational age was known for each examination. Measurements of biparietal diameter (BPD), head circumference (HC), abdominal circumference (AC), and femur length (FL) were used to create growth curves. Prenatal growth of P. paniscus was compared with the data of humans and the common chimpanzee, P. troglodytes. With respect to cranial structures, such as BPD and HC, humans have significant acceleration of growth compared with P. paniscus and P. troglodytes. In P. paniscus, growth of AC was similar to HC throughout pregnancy, whereas in humans AC only reaches the level of HC close to term. Growth rate of FL was similar in humans and the two Pan species until near day 180 post‐ovulation. After that, the Pan species FL growth slowed compared with human FL. The newly developed fetal growth curves of P. paniscus will assist in monitoring prenatal development and predicting birth dates of this highly endangered species. Zoo Biol 30:241–253, 2011. © 2010 Wiley‐Liss, Inc.     

Periparturitional behavior of a bonobo (Pan paniscus)

Knowledge of periparturitional behaviors in captive primates may contribute to infant survival and is particularly important for endangered species, such as the bonobo, or pygmy chimpanzee (Pan paniscus). Given that the bonobo is considered to be closely related to humans, such knowledge also may offer insights about the evolutionary development of complex maternal patterns. To date, however, only one observation of a P. paniscus birth has been reported. The periparturitional behaviors of a mature bonobo (P. paniscus) female during the pregnancy and birth of two infants are described in detail. Information not previously reported for the species is included. Periparturitional behaviors were similar for both births.     

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.     

Seed dispersal by pygmy chimpanzees (Pan paniscus): A preliminary report

The role in seed dispersal played by the pygmy chimpanzees (Pan paniscus) inhabiting Wamba, Republic of Zaïre, was studied. Germination was tested for seeds of 17 plant species recovered from the feces of pygmy chimpanzees at Wamba. The fecal seeds of 13 species germinated, and in six of the species the germination rate for the fecal seeds was higher than that of control seeds. Although five other species showed a higher germination rate in the control seeds than in the fecal seeds, the remaining two species revealed no difference in germination rate between the fecal and control seeds. There was no great difference in germination velocity between the fecal and control seeds of the same species. For comparison, seeds of four plant species collected from the feces of common chimpanzees (Pan troglodytes) and gibbons (Hylobates lar) in captivity in Okinawa were tested for their germinability. In this test, although the seeds had passed through the digestive tract, their germinability demonstrated little change. Based on the behavioral characteristics of the pygmy chimpanzee at Wamba and observations of the captive primates on Okinawa, it seems that pygmy chimpanzees may play an important role in the seed dispersal of fruit plant species at Wamba.     

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.     

Reproductive aging in captive and wild common chimpanzees: factors influencing the rate of follicular depletion

We examine and discuss evidence of contrasting differences in fertility patterns between captive and wild female chimpanzees, Pan troglodytes, as they age; in the wild females reproduce in their 40s, but captive studies suggest that menopause occurs around that time. Thus, despite the increased longevity generally observed in captive populations reproductive life span is shortened. We outline a hypothesis to explain the apparent differential pace of reproductive decline observed between wild and captive populations. The breeding schedules of captive primates may contribute to accelerated reproductive senescence because continuous cycling in captive animals results in early depletion of the ovarian stock and premature senescence. Available evidence supports the hypothesis that women with patterns of high oocyte loss experience earlier menopause. Chimpanzees in captivity live longer, and thus, similar to humans, they may experience follicular depletion that precedes death by many years. In captivity, chimpanzees typically have an early age at menarche and first birth, shorter interbirth intervals associated with short lactational periods as young mature faster, and nursery rearing, which allows mothers to begin cycling earlier. Variables typical of wild chimpanzee populations, including late age at menarche and first birth, long interbirth intervals associated with prolonged lactational periods, and a long period of female infertility after immigration, spare ovulations and may be responsible for the later age at reproductive termination. Finally, we describe and discuss the timing of specific reproductive landmarks that occur as female chimpanzees age, distinguishing between functional menopause (age at last birth) and operational menopause (end of cycling). Am. J. Primatol. 71:271–282, 2009. © 2008 Wiley‐Liss, Inc.     

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.     

Co–Residence between Males and Their Mothers and Grandmothers Is More Frequent in Bonobos Than Chimpanzees

In long–lived social mammals such as primates, individuals can benefit from social bonds with close kin, including their mothers. In the patrilocal chimpanzee (Pan troglodytes spp.) and bonobo (Pan paniscus), sexually mature males reside and reproduce in their natal groups and can retain post-dependency bonds with their mothers, while immatures of both sexes might also have their paternal grandmothers available. However, quantitative information on the proportion of males and immatures that co-reside with both types of these close female relatives is limited for both species. Combining genetic parentage determination and group composition data from five communities of wild chimpanzees and three communities of wild bonobos, we estimated the frequency of co-residence between (1) mature males and their mothers, and (2) immature males and females and their paternal grandmothers. We found that adult males resided twice as frequently with their mothers in bonobos than in chimpanzees, and that immature bonobos were three times more likely to possess a living paternal grandmother than were immature chimpanzees. Patterns of female and male survivorship from studbook records of captive individuals of both species suggest that mature bonobo females survive longer than their chimpanzee counterparts, possibly contributing to the differences observed in mother–son and grandmother–immature co-residency levels. Taking into account reports of bonobo mothers supporting their sons'' mating efforts and females sharing food with immatures other than their own offspring, our findings suggest that life history traits may facilitate maternal and grandmaternal support more in bonobos than in chimpanzees.