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Longitudinal study of dental development in chimpanzees of known chronological age: implications for understanding the age at death of Plio-Pleistocene hominids.

Reconstruction of life history variables of fossil hominids on the basis of dental development requires understanding of and comparison with the pattern and timing of dental development among both living humans and pongids. Whether dental development among living apes or humans provides a better model for comparison with that of Plio-Pleistocene hominids of the genus Australopithecus remains a contentious point. This paper presents new data on chimpanzees documenting developmental differences in the dentitions of modern humans and apes and discusses their significance in light of recent controversies over the human or pongid nature of australopithecine dental development. Longitudinal analysis of 299 lateral head radiographs from 33 lab-reared chimpanzees (Pan troglodytes) of known chronological age allows estimation of means and standard deviations for the age at first appearance of 8 developmental stages in the mandibular molar dentition. Results are compared with published studies of dental development among apes and with published standards for humans. Chimpanzees are distinctly different from humans in two important aspects of dental development. Relative to humans, chimpanzees show advanced molar development vis a vis anterior tooth development, and chimpanzees are characterized by temporal overlap in the calcification of adjacent molar crowns, while humans show moderate to long temporal gaps between the calcification of adjacent molar crowns. In combination with recent work on enamel incremental markers and CAT scans of developing dentitions of Plio-Pleistocene hominids, this evidence supports an interpretation of a rapid, essentially "apelike" ontogeny among australopithecines.

Aging↗

Permanent tooth calcification in chimpanzees (Pan troglodytes): patterns and polymorphisms.

Tooth calcification is an important developmental marker for use in constructing models for early hominid life history, particularly for its application to the fossil record. As chimpanzees are commonly utilized in interspecific comparisons in such research, this study aims to improve available baseline data for tooth calcification patterns in chimpanzees (Pan troglodytes), and to quantify basic patterns and polymorphisms. We present an analysis of developmental patterns for the left mandibular dentition (I1-M3) based on intraoral radiographs obtained from a cross-sectional sample of chimpanzees (58 males, 60 females) housed at LEMSIP (NYU Medical Center) and Yerkes (Emory University). No significant differences with previous descriptions of the basic sequences of tooth calcification in chimpanzees were found, but variation in such patterns was documented for the first time. In the overall sequence, polymorphisms between the canine and the group (M2 P4 P3) reached significant levels. This is due to the relative delay in canine crown formation compared to other teeth. Differences in the basic sequence between males and females were recorded, but are due to minor shifts in the percentages of occurrence for polymorphic sequences which are common to both genders. Perhaps our most important findings are that a) different polymorphic sequences occur in tooth calcification and tooth emergence in chimpanzees, and b) developmental relationships among teeth fluctuate throughout tooth calcification. Thus, characterizations of dental developmental patterns based on particular stages of development cannot necessarily be extrapolated to other stages without supporting data.

Animals↗

Identifying conservation units within captive chimpanzee populations.

One of the primary objectives in the captive management of any endangered primate is to preserve as much as possible the genetic diversity that has evolved and still exists in wild gene pools. The rationale for this is based on the theoretical understanding of the relationship between genetic diversity and fitness in response to selection. There remains little consensus, however, as to the type of genetic data that should be used to monitor captive populations. In order to develop a deeper understanding of the degree and nature of genetic diversity among "wild" chimpanzee gene pools, as well as to determine if one type of genetic data is more useful than others, DNA sequence data were generated at three unlinked, nonrepetitive nuclear loci, one polymorphic microsatellite, and the mitochondrial D-loop for 59 unrelated common and pygmy chimpanzees. The results suggest that: 1) data from nuclear loci can be used to differentiate common chimpanzee subspecies; 2) pygmy chimpanzees may have less genetic diversity than common chimpanzees; 3) shared microsatellite alleles do not always indicate identity by descent; and 4) nonrepetitive loci provide unique insights into evolutionary relationships and provide useful information for captive management programs.

Animals↗

"Stepping-sticks" and "seat-sticks": new types of tools used by wild chimpanzees (Pan troglodytes) in Sierra Leone.

In Tenkere, Sierra Leone, a community of wild chimpanzees (Pan troglodytes verus) spent long hours eating the fruits and flowers of the Kapok (Ceiba pentandra) tree. The branches of this species are covered in sharp thorns which make movement in their high canopies problematic for the chimpanzees. In an apparent attempt to increase their mobility and to ease the discomfort of lengthy bouts of eating in these trees, some of the Tenkere chimpanzees have been observed using stick tools as foot ("stepping-sticks") and body ("seat-sticks") protection against the painful thorns. This form of tool-using is culturally unique to the Tenkere chimpanzees, as at other sites where these apes have been observed eating parts of kapok trees, there are no published records of this tool technology. In three of the stepping-stick tool use incidents, the chimpanzee used the tool(s), held between their greater and lesser toes, in locomotion. This form of tool use is the first recorded case of habitually used tools that can be justifiably categorized as being "worn" by any known wild population of Pan troglodytes.

Animals↗

Use of leaves as cushions to sit on wet ground by wild chimpanzees.

A new type of tool use, leaf cushion, by wild chimpanzees (Pan troglodytes verus) at Bossou, Guinea, was found. We report two cases: one is indirect evidence; the other is direct observation of a chimpanzee who used the tool. Both cases indicate that chimpanzees used a set of leaves as a cushion while sitting on wet ground. Chimpanzees at Bossou show various kinds of tool use, some of which are unique to the community. Most of these behavioral patterns are substance tool use for obtaining food, as at other study sites. The use of leaves as a cushion adds to the few instances of nonsubstance, elementary technology seen used by wild chimpanzees.

Animals↗

Recognizing hominoid-modified bones: the taphonomy of colobus bones partially digested by free-ranging chimpanzees in the Kibale Forest, Uganda.

We present a taphonomic study of bones that have passed though the digestive tracts of free-ranging chimpanzees from the Kibale Forest in Uganda. The bone assemblage can be characterized as having a very low species diversity; low number of identifiable specimens (NISP) per scat; bones extremely broken up (very small size range); skeletal part frequencies similar in some ways to those resulting from carnivore partial digestion; and sometimes articulated specimens. Modifications to the bones include corrosion, tiny tooth scores and pits, cracking, and fraying of bone edges. Together, these characteristics suggest that hominoid bone digestion may be recognizable, despite some similarities with leopard-, canid-, and eagle-modified bone. Chimpanzees are well-documented hunters of medium-sized vertebrates such as monkeys. This is significant in the study of human evolution if, as it seems, the last common ancestor of chimpanzees and humans was chimpanzee-like. It suggests there was a pre-stone-tool-using hunting phase in human evolution, perhaps by australopiths or the last common ancestor. Taphonomically, pre-stone tool meat eating has been very difficult to detect in the fossil record. However, if chimpanzees leave a recognizable taphonomic signature on the bones of their prey, we will be able to look for analogous signatures in fossil bones associated with fossil hominoids and hominids.

Animals↗

Ant-dipping among the chimpanzees of Bossou, Guinea, and some comparisons with other sites.

We present a detailed study of ant-dipping among the wild chimpanzees (Pan troglodytes verus) of Bossou, in southeastern Guinea, West Africa. Observations suggest a strong influence of prey (Dorylusspp.) characteristics, including aggressiveness and/or gregariousness, on tool length and technique employed by the chimpanzees. Bossou chimpanzees exhibit two ant-dipping techniques: 1) direct mouthing, and 2) pull-through. In addition, they were observed dipping for several species of Dorylus ants, classed into two categories: Red and Black. Tool length was longer when dipping in higher-risk contexts, i.e., at the ants' nest site or on Black ants. The pull-through technique was almost exclusively associated with dipping at the nest site. This latter technique was associated with tools over 50 cm long, whereas direct mouthing was the only technique observed with tools < 50 cm long. Our experimental findings, together with our observations on the behavior of the chimpanzees, suggest that at the nest, the pull-through technique was a more efficient technique than direct mouthing. We review our results in the context of ant-dipping observed at two other long-term chimpanzee study sites, i.e., Gombe (Tanzania) and Taï (Côte d'Ivoire), where differences in tool length, technique used, and focal Dorylus ant species have been reported. Finally, we urge similar detailed studies of this tool-use behavior in both Gombe and Taï to shed further light upon our results and their implications.

Aggression↗

Dominance rank and fecal testosterone levels in adult male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda.

In an attempt to describe hormone-behavior interactions in a sample of wild male chimpanzees, we quantified testosterone in 67 fecal samples obtained from 22 adult male chimpanzees at Ngogo, Kibale National Park, Uganda. A mixed-model methodology that controlled for age-class identified a significant positive association between testosterone levels and dominance rank. The results are consistent with those reported from a separate, smaller chimpanzee community in the same population in a study that analyzed testosterone levels in urine [Muller & Wrangham, 2004]. As in that earlier study, our results held during a period of social stability, which is not consistent with predictions of the "challenge hypothesis." We concur with Muller and Wrangham [2004] that the challenge hypothesis requires modification to explain the chimpanzee data, because fission-fusion sociality in chimpanzees makes challenges unpredictable. We also discuss the utility of fecal samples and a mixed-model statistical method for behavioral endocrinology studies.

Androgens↗

Nutritional significance of the selective ingestion of Albizia zygia gum exudate by wild chimpanzees in Bossou, Guinea.

The selective ingestion of plant gum exudates by chimpanzees has been frequently observed at various study sites. At Bossou, Guinea, chimpanzees also frequently ingest Albizia zygia gum exudate. A functional explanation for this behavior is lacking, so we evaluated its possible contribution of energy in the form of short-chain fatty acids (SCFA) as well as minerals. An in vitro fermentation study of A. zygia gum using the fecal bacteria of a Bossou chimpanzee showed that carboxylic acids were produced with a 6-hr lag phase up to 44 mmol/l by 18 hr of incubation. Acetate was the most abundant acid produced, followed by lactate and propionate. The energy supplied from the fermentation of a piece of gum exudate (20-30 g) was negligible in comparison with the estimated daily energy requirements of chimpanzees in the wild. However, A. zygia gum exudate (20-30 g) can supply sufficient amounts of calcium, manganese, magnesium, and potassium to fulfill the daily requirements for these minerals in chimpanzees.

Albizzia↗

Molecular analyses of the intestinal microbiota of chimpanzees in the wild and in captivity.

Little information is available regarding the intestinal bacteria of chimpanzees in the wild, due to the technical difficulties of studying intestinal bacteria in the field. In this study, molecular-based bacterial analyses were performed to overcome this difficulty because polymerase chain reaction (PCR)-based methods, such as temperature gradient gel electrophoresis (TGGE) and amplified ribosomal DNA restriction analysis (ARDRA), of the bacterial 16S rRNA gene can be applied to ethanol-fixed fecal samples. The common presence of bacteria belonging to the Clostridium rRNA sub-group XIVa, such as Ruminococcus obeum and Eubacterium sp., was indicated for Bossou wild chimpanzees by ARDRA. TGGE on partial 16S rDNA followed by hierarchical clustering analysis showed a systematic difference in the composition of intestinal microbiota between wild and captive chimpanzees. However, several TGGE bands commonly shared by wild and captured chimpanzees were excised, and their sequences were obtained. They were suggested to be the Clostridium leptum subgroup bacteria, Lactobacillus gasseri-like bacterium, and Bifidobacterium pseudocatenulatum- or B. catenulatum-like bacterium. These may be considered as common intestinal bacteria for chimpanzees, and may be transmitted vertically over generations.

Animals↗

Longitudinal analysis of length growth in the chimpanzee (Pan troglodytes).

The adolescent growth spurt in linear dimension in humans is considered to be unique among mammals, but few comparative studies have been done, even on chimpanzees. Growth of the summed length of crown to rump, thigh, and leg was studied longitudinally in 12 chimpanzees. We took body weight growth and reproductive maturation into consideration. Reproductive maturation was monitored by the swelling of sexual skin and menarche in females, and by testicular development in males. We applied two relationships found in humans between body length growth and the environment to the chimpanzees. The first relationship was the robustness of the growth spurt, meaning that the spurt is absent only in individuals under the most severe environmental pressure. Subjects maturing in a favorable or even mediocre environment are anticipated to show the growth spurt. The second relationship was catch-up growth, where, when the environment is ameliorated, growth may be accelerated to attain the target size. Catch-up growth at the end of the juvenile period may mimic the adolescent growth spurt. Results showed that subjects living under favorable conditions did not exhibit a growth spurt, and that it was only the subjects who had delayed growth in the juvenile period that showed a spurt in adolescence, the period when reproductive maturation occurred. Although we have concluded that chimpanzees do not have an adolescent growth spurt, except in cases of catch-up growth, this does not mean that they have a different growth pattern from that of humans. The absence of a growth spurt may be associated with adaptations to chimpanzee patrilineal society, where adolescent males are incorporated into the adult hierarchy at a low rank.

Animals↗

Developmental changes in the shape of the supralaryngeal vocal tract in chimpanzees.

The hyoid bone and larynx in human neonates are positioned as high as in other mammals. However, during postnatal life, they descend relative to the hard palate more rapidly compared with the horizontal growth of the oral cavity. This process is completed through the descent of the laryngeal skeleton relative to the hyoid, and through the descent of the hyoid relative to the cranial base. Thus, the human supralaryngeal vocal tract (SVT) develops to form a two-tube configuration with equally long horizontal and vertical parts. Longitudinal studies on living chimpanzee infants show that the descent of the larynx is more rapid than the horizontal growth of the oral cavity. This is primarily attributed to the descent of their larynges relative to the hyoid bone, but this is not accompanied by the descent of the hyoid. The present study, using embalmed specimens of chimpanzees, also shows that the horizontal and vertical parts of the SVT grow in chimpanzees similarly to humans during infancy. However, in chimpanzees, the horizontal part of the SVT grows greatly, whereas the vertical part of the SVT grows only slightly during the juvenile period. As a result, the chimpanzee larynx does not descend rapidly relative to the oral elongation during that period. Such differences may be related to the structural and morphological development of the facial skeleton and mandible, which affects prognathism and hyoid descent. These results support the hypothesis that the descent of the larynx evolved in at least two steps during hominoid evolution.

Animals↗

Social play in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): Implications for natural social systems and interindividual relationships.

This study compares adult play behavior in the two Pan species in order to test the effects of phylogenetic closeness and the nature of social systems on play distribution. The social play (both with fertile and immature subjects) performed by adults did not differ between the two species. In contrast, in bonobos, play levels among fertile subjects were higher than in chimpanzees. Findings regarding levels of undecided conflicts (more frequent in bonobos) and formal submission displays (lacking in bonobos) confirm, in the two colonies under study, that bonobos exhibit "egalitarianism" more than chimpanzees. Some authors emphasized the importance of play-fighting for social assessment when relationships among individuals are not codified and structured according to rank-rules. Indeed, adult bonobos played more roughly than chimpanzees. Moreover, adult bonobos displayed the full play-face at a high frequency especially during rough play sessions, whereas in chimpanzees, the frequency of play signals was not affected by roughness of play. The frequency of social play among bonobo females was higher than in any other sex combinations, whereas no difference was found for chimpanzees. As a matter of fact, social play can be viewed as a balance between cooperation and competition. Among bonobo females, characterized by social competence and affiliation, social play might enhance their behavioral flexibility and increase their socially symmetrical relationships which, after all, are the basis for their egalitarian society.

Age Factors↗

A map of the common chimpanzee genome.

The completion of the chimpanzee genome will greatly help us determine which genetic changes are unique to humanity. Chimpanzees are our closest living relative, and a recent study has made considerable progress towards decoding the genome of our sister taxon.1 Over 75,000 common chimpanzee (Pan troglodytes) bacterial artificial chromosome end sequences were aligned and mapped to the human genome. This study shows the remarkable genetic similarity (98.77%) between humans and chimpanzees, while highlighting intriguing areas of potential difference. If we wish to understand the genetic basis of humankind, the completion of the chimpanzee genome deserves high priority.

Animals↗

The perihypoglossal nuclei in the macaque monkey and the chimpanzee.

The topography of the perihypoglossal nuclei (nucleus intercalatus, nucleus prepositus, and nucleus of Roller) of the macaque and the chimpanzee was studied in serial Nissl-stained sections through the brainstem. Maps of the nuclei in the two species are presented. Although in both species the perihypoglossal nuclei are organized according to the general mammalian pattern, they show some particular features, reflecting in part, an increasing phylogenetic differentiation. In the chimpanzee the nucleus prepositus is relatively larger, the nucleus of Roller is more of a separate unit, and its cellular composition is more uniform than is the case in the macaque. A cellular connection between the two nuclei is present in the macaque (even more conspicuous in the cat, apparently absent in man), but is barely discernible in the chimpanzee. A conspicuous difference between the chimpanzee and the macaque concerns the nucleus supragenualis nervi facialis, forming a rostral continuation of the prepositus. In the chimpanzee it is a loosely structured region of small cells (as in the cat and in man). In the macaque, however, it appears as a rather well-delimited column of chiefly medium-sized cells. Some comparative anatomical and functional aspects are discussed. Many contingents of afferents to--and efferents from--the nucleus prepositus have their preferential sites of termination or origin in the nucleus, although with considerable overlapping. This indicates the presence of topical patterns in the prepositus. In general the caudal parts appear to be more related to the cooperation with the cerebellum than the rostral part, whereas the latter appears to be more particularly linked with the oculomotor apparatus.

Animals↗

Subcortical projections to the occipital and parietal lobes of the chimpanzee brain.

The subcortical sources of afferents to occipital and parietal cortex were studied in two chimpanzees with the aid of retrogradely transported horseradish peroxidase (HRP). In chimpanzee 1, HRP was injected into right cortical areas 17 and 18; chimpanzee 2 received HRP into right areas 17, 18, 19, and 39. The following subcortical structures were found to project to area 17 and/or area 18: locus coeruleus, dorsal raphe nucleus, nucleus annularis, nucleus centralis superior, pontine reticular formation, mesencephalic reticular formation, dorsal hypothalamus, lateral hypothalamus, nucleus basalis of Meynert, nucleus of the diagonal band of Broca, claustrum, nucleus basalis lateralis amygdalae, lateral geniculate nucleus, inferior pulvinar, lateral pulvinar, nucleus limitans, medial magnocellular part of the nucleus ventralis anterior, nucleus paracentralis, and nucleus centralis medialis thalami. Some of these structures may also project to area 19 and/or area 39. The following thalamic nuclei were found to project to area 19 and/or area 39 but not to areas 17 and 18: nucleus lateralis posterior, nucleus centralis lateralis, nucleus medialis dorsalis, nucleus ventralis lateralis, nucleus ventralis anterior nucleus lateralis dorsalis, and nucleus anterior ventralis. In several Instances, the HRP-labeled cells traversed specific nuclear borders, extending uninterruptedly from one classically defined nucleus into another. These results in the chimpanzee largely confirm data from a number of other mammalian taxa on the subcortical sources of afferents to the posterior cortex. Because of the close biological relationship between chimpanzee and man, we feel confident that such projections are also features of the human brain.

Amygdala↗

Cytoplasmic tubular structures in liver of HBsAg carrier chimpanzees infected with delta agent and comparison with cytoplasmic structures in non-A, non-B hepatitis.

Electron microscopic observations were carried out on five HBsAg carrier chimpanzees infected with delta (delta) agent and two chimpanzees infected with human non-A, non-B hepatitis. The cytoplasmic tubular structures, which have been recognized in the liver of chimpanzees infected with human non-A, non-B hepatitis, were found also in the liver of HBsAg carrier chimpanzees infected with delta agent. The quantity of the cytoplasmic structures in serial studies was associated with SGPT elevation rather than with expression of delta antigen in sera and liver tissues. This indicates that the cytoplasmic structures reflect a pathologic change of the hepatocytes in chimpanzees infected with delta agent or human non-A, non-B hepatitis. These and other similarities between the two agents suggest a similar nature.

Animals↗

Breakpoint analysis of the pericentric inversion distinguishing human chromosome 4 from the homologous chromosome in the chimpanzee (Pan troglodytes).

The study of breakpoints that occurred during primate evolution promises to yield valuable insights into the mechanisms underlying chromosome rearrangements in both evolution and pathology. Karyotypic differences between humans and chimpanzees include nine pericentric inversions, which may have potentiated the parapatric speciation of hominids and chimpanzees 5-6 million years ago. Detailed analysis of the respective chromosomal breakpoints is a prerequisite for any assessment of the genetic consequences of these inversions. The breakpoints of the inversion that distinguishes human chromosome 4 (HSA4) from its chimpanzee counterpart were identified by fluorescence in situ hybridization (FISH) and comparative sequence analysis. These breakpoints, at HSA4p14 and 4q21.3, do not disrupt the protein coding region of a gene, although they occur in regions with an abundance of LINE and LTR-elements. At 30 kb proximal to the breakpoint in 4q21.3, we identified an as yet unannotated gene, C4orf12, that lacks an homologous counterpart in rodents and is expressed at a 33-fold higher level in human fibroblasts as compared to chimpanzee. Seven out of 11 genes that mapped to the breakpoint regions have been previously analyzed using oligonucleotide-microarrays. One of these genes, WDFY3, exhibits a three-fold difference in expression between human and chimpanzee. To investigate whether the genomic architecture might have facilitated the inversion, comparative sequence analysis was used to identify an approximately 5-kb inverted repeat in the breakpoint regions. This inverted repeat is inexact and comprises six subrepeats with 78 to 98% complementarity. (TA)-rich repeats were also noted at the breakpoints. These findings imply that genomic architecture, and specifically high-copy repetitive elements, may have made a significant contribution to hominoid karyotype evolution, predisposing specific genomic regions to rearrangements.

Animals↗