Sexual swelling,receptivity, and grouping of wild pygmy chimpanzee females at Wamba,Zaïre

The sexual swelling and copulatory behavior of ten pygmy chimpanzee (Pan paniscus) females in a wild group were studied at Wamba, Republic of Zaïre. Since the maximum size of the sexual skin revealed great individual variations depending on age and adolescent females showed little cyclic fluctuation in size, the sexual swelling was measured according to its firmness which periodically fluctuated in all age classes. The duration of maximum swelling and the cycle length were longer inP. paniscus than inP. troglodytes. Although pregnant females and those with newborn infants were sexually inactive, females with infants older than 3 years copulated as frequently as those without dependent infants. Contrary to previous reports on the sexuality ofP. paniscus, copulation was mostly restricted to the maximum swelling phase. All females were usually found in a large mixed party containing both sexes and offspring, regardless of their sexual receptivity.     

Party composition and dynamics inPan paniscus

The pygmy chimpanzee, or bonobo, Pan paniscus,diplays a fission-fusion social organization in which individuals associate in parties that vary in size and composition. Data from a 2-year field study of nonprovisioned P. paniscusshow that party composition varies with party size. Although females, on average, outnumber males, the proportion of males in the party increases in larger parties. This effect was not due to the greater number of known females. Both females and males will join and leave a party in the company of others, but only males appear frequently to join or leave as lone individuals. All-male parties were not observed, but all-female (nonnursery) parties were relatively common. These trends reflect greater cohesion among females than observed in P. troglodytes schweinfurthii.Cohesion between males and female P. paniscusmay increase with party size.     

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.     

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.     

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.     

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.     

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.     

Relative orbitonasal overlap in african great apes and humans quantified by the automatic determination of horizontal and vertical lines of reference

The relative positions of the orbital and nasal openings in African apes and humans were studied by a new methodological approach based on the automatic determination, by image analysis techniques, of horizontal and vertical lines of reference. The material used consisted ofGorilla gorilla (38 males and 20 females),Pan troglodytes (19 males and 13 females), and modernHomo spaiens (51 males and 41 females). This allowed the relative positions of the orbital and nasal openings to be quantified by the determination of medio-lateral and vertical orbitonasal indices of overlap. In all the species studied, a medio-lateral orbitonasal overlap was systematically observed. This indicates that nasal breadth is always larger than interorbital distance. Medio-lateral overalp was greatest inGorilla, reduced inHomo, and intermediate inPan. By contrast, onlyHomo presents systematically a vertical overlap: a vertical overlap was sometimes observed inPan, but never inGorilla. Homo presented the greatest vertical overlap, andGorilla the least; the disposition inPan was intermediate. The interspectific study of the relationships between medio-lateral and vertical overlap inGorilla, Pan, andHomo demonstrated that an increase in veritical overlap was correlated with a decrease of medio-lateral overlap. Sexual dimorphism in orbitonasal relationships was systematically greatest inGorilla, and reduced inPan andHomo, this is also the case for the orbital, nasal, and orbitonasal parameters measured in this study. All these results provide interesting elements for understanding the morphological evolution of the middle face in hominoids.     

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.     

Contribution of genetic distances studies to the taxonomy ofAteles,particularlyAteles paniscus paniscus andAteles paniscus chamek

We studied 20 electrophoretic loci in two populations ofAteles (Ateles paniscus paniscus andAteles paniscus chamek). We observed intrapopulational variation at the following loci: esterase D, glyoxalase 1, adenosine deaminase (A. p. chamek) and carbonic anhydrase 2 (A. p. paniscus). The two populations share the most frequent alleles at 17 loci, but we noted great differences in glyoxalase 1, adenosine deaminase and phosphoglucomutase 1.A. p. paniscus is monomorphic for theGLO1 ^*1 allele, which has a frequency of 6% inA. p.chamek. They did not share alleles in relation to the ADA and PGM1 loci. We found a CA2 allele, named hereCA2 ^*1, which has not been described previously in other neotropical primates (Sampaio et al., 1991a), inA. p. paniscus. The present results suggest that the geographical isolation represented by the Rio Amazonas has lasted long enough to support this level of divergence. These observations taken together with chromosomal findings, led us to endorse the proposal of two distinct species:Ateles paniscus andAteles chamek.     

Redescription of Enterobius anthropopitheci (Gedoelst, 1916) (Nematoda,Oxyurida), a parasite of chimpanzees

Enterobius anthropopitheci (Gedoelst, 1916), a parasite of the chimpanzees Pan troglodytes and P. paniscus, is redescribed. E. anthropopitheci can be distinguished from the two closely related species parasitic in man, E. vermicularis (L., 1758) and E. gregorii Hugot, 1983, by the following characters: in the males, the cuticular pericloacal ornamentation, and the size and shape of the spicule; in the females, the lateral alae, which are simple in the pinworms of man, are simple only anteriorly and divided into two crests at the mid-oesophageal level in the parasite of chimpanzees. Enterobius anthropopitheci (Gedoelst, 1916), parasite des chimpanzés, Pan troglodytes et P. paniscus, dans toute leur aire de répartition est redécrite. E. anthropopitheci est très proche par sa morphologie des deux oxyures de l'Homme, E. vermicularis (L., 1758) et E. gregorii Hugot, 1983, dont il diffère toutefois par les caractères suivants: chez le mâle, ornementation cuticulaire péricloacale, taille et forme du spicule; chez la femelle, aile latérale simple sur toute sa longuer chez les oxyures de l'Homme, simple dans la région antérieure se dédoublant en deux crêtes au milieu de l'oesophage, chez l'oxyure parasite des chimpanzés.     

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.     

Population systematics of chimpanzees using molar morphometrics

When dental morphological variation within extant species is used as a guideline to partition variation within fossil samples into species, the underlying assumption is that fossil species are equivalent to extant species. This is the case despite the fact that dental morphology, which is commonly used to differentiate fossil species, is rarely used to differentiate extant species. Aspects of external morphology, ecology, behavior, breeding patterns, and molecular structure that are used to delineate living species are generally not available for fossils. In this paper, the utility of dental evidence for sorting fossil samples into species is evaluated by testing whether molar occlusal morphology is capable of sorting populations of Pan into the species and subspecies already well-established by nondental evidence. The dentitions of 341 chimpanzee individuals, sampled from regions throughout equatorial Africa, were sorted into 16 populations using rivers to demarcate the boundaries between populations. Digital-imaging software was used to measure 15 traits on the occlusal surface of each upper molar and 19 on each lower molar. After applying size adjustments, size-transformed and untransformed variables were subjected to discriminant analysis, with separate analyses carried out for each molar type. Results indicate that populations of Pan troglodytes and Pan paniscus are well differentiated at all molar positions. Populations of P. t. verus are distinct from other populations of P. troglodytes. Populations of P. t. troglodytes and P. t. schweinfurthii show close dental similarity. A distinct population is recognized at the Nigeria-Cameroon border, indicating the presence of P. t. vellerosus. The concordance between the patterns of diversity recognized by this study and other molecular and nonmolecular studies indicates that paleontological species that are similar to species of Pan in terms of size and patterns of diversification may be differentiated using molar morphology.     

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.     

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.     

Mobility of short interspersed repeats within the chimpanzee lineage

The PV subfamily of Alu repeats in human DNA is largely composed of recently inserted members. Here we document additional members of the PV subfamily that are found in chimpanzee but not in the orthologous loci of human and gorilla, confirming the relatively recent and independent expansion of this Alu subfamily in the chimpanzee lineage. As further evidence for the youth of this Alu subfamily, one PV Alu repeat is specific to Pan troglodytes, whereas others are present in Pan paniscus as well. The A-rich tails of these Alu repeats have different lengths in Pan paniscus and Pan troglodytes. The dimorphisms caused by the presence and absence of PV Alu repeats and the length polymorphisms attributed to their A-rich tails should provide valuable genetic markers for molecular-based studies of chimpanzee relationships. The existence of lineage-specific Alu repeats is a major sequence difference between human and chimpanzee DNAs. Correspondence to: C.W. Schmid     

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).     

A model of the biogeographical journey from<Emphasis Type="Italic"> Proto-pan</Emphasis> to<Emphasis Type="Italic"> Pan paniscus</Emphasis>

Pan paniscus is unique in the group of African apes because of its range south of the Congo River. Examination of the bio-geographical journey of the genus Pan to the species P. paniscus is important when discussing the evolution of African apes. This paper is a review of the paleo-geographic events, the zoogeography, and faunal sorting which influenced P. paniscus divergence from the Proto-pan ancestor within the recent Miocene through Pliocene Epochs, approximately 10–2 MYA. Finally, by elucidating modern day evidence of food plant forms in the southern periphery exploited by P. paniscus in the forest/savanna mosaic habitat, we are able to conclude with those extrinsic events that most influenced the occurrence and distribution of P. paniscus. Electronic Publication     

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.     

What Role Do Mothers Play in the Gestural Acquisition of Bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes)?

Contemporary research hypothesizes that biological inheritance and ontogenetic factors shape the development of gestural communication in nonhuman great apes. However, little is known about the specific role that mothers play in the acquisition of their infants’ gestures. We observed 6 bonobo (Pan paniscus) and 4 chimpanzee (Pan troglodytes) mother–infant dyads and recorded their gesture types and frequency. We analyzed all behavioral contexts in which gestures occurred as well as the play context alone. Infants of both species were unlikely to share gestures with their mother or unrelated adult females. However, gestural sharing was prevalent within age groups. Within and across species, infant–infant and mother–mother groups were homogeneous regarding the types of gestures they shared, although there was individual variation in the frequency of gesture use. Our findings provide limited evidence that infants learned their gestures by imitating their mothers. Phylogenetic influences seem to be vital in gestural acquisition but, we suggest, repertoire development cannot be disentangled from individual social encounters during life.