A contribution to tropical rain forest taphonomy: retrieval and documentation of chimpanzee remains from Kibale Forest, Uganda

The absence of Pan and Gorilla fossils from Africa has led some to suggest that African rain forests are not conducive to bone preservation. The absence of fossils is unfortunate as it hampers phylogenetic and socioecological interpretations on the divergence of the earliest hominids. For the most part, taphonomic studies have been restricted to cave and open country contexts. With this in mind, we have initiated a taphonomic project in a tropical rain forest, the Kibale Forest of western Uganda. In the course of bone gathering activities over the past 4 years, we have documented the retrieval of skeletal remains representing nine chimpanzees (Pan troglodytes schweinfurthii). Crania and mandibles are most commonly recovered, followed by elements of the axial skeleton, and finally, appendages. Vertical segregation of small compact bones can occur in areas with a soft substrate. Scavenging activity suggests the role of suids, but this has not been proven. Geochemical tests suggest that Kibale soils are neutral and may be conducive to bone preservation. Our independent preliminary data from bone weathering/survival experiments indicate that bones appear undamaged after several years and are able to accumulate on the forest floor. These results contrast with popular assumptions on the potential of African rain forests as potential fossil reservoirs.     

Observations on the illness and consumption of a possibly medicinal plantVernonia amygdalina (Del.), by a wild chimpanzee in the Mahale Mountains National Park,Tanzania

Detailed observations on the consumption ofVernonia amygdalina (Del.), a naturally occurring plant of known ethnomedicinal value, by an adult female chimpanzee (Pan troglodytes schweinfurthii) of M-group in the Mahale Mountains, Tanzania were made. Chewing the pith of several shoots, she sucked out and swallowed the astringent, bitter tasting juice; spitting out the fibrous remains. The female was followed during this period for 11 hr, over two consecutive days, and was recognized to be in irregular health at the time of consumption, exhibiting signs of lethargy, lack of appetite, and irregularity of bodily excretions. The low frequency and lack of seasonality in the usage of this plant suggest that it is sought after for reasons other than as a food source. These factors suggest that for chimpanzees, the consumption of this plant is primarily medicinal. The symptoms displayed by the female are the same as those experienced by people throughout tropical Africa who utilize this plant as a medicinal treatment for them. Interactions between the female and others suggest that they too were aware of her condition and coordinated their activities with the female and her infant.     

A new procedure to study the perceptual world of animals with sensory reinforcement: Recognition of humans by a chimpanzee

A female chimpanzee touched a button to produce colored slides of pictures. Slides were present as long as she kept touching the button. Repeated touch within 10 sec after the previous release produced the same slides again. The slide was changed when 10 sec passed after she released the button. The duration of a touching response and the interval between the responses were calculated for each of 100 slides. The data for each slide were plotted on the two-dimensional space constructed with response duration and response interval. A clear differentiation of distribution on this space was found between slides with humans and those without humans. The result demonstrated that the chimpanzee recognized humans as a category, as well as that this procedure is effective for the study of the perceptual world of animals based on the reinforcing function of stimuli.     

Use of exclusion by a chimpanzee (Pan troglodytes) during speech perception and auditory-visual matching-to-sample

An adult female chimpanzee showed responding through use of exclusion in an auditory to visual matching-to-sample procedure. The chimpanzee had previously learned to associate specific visuographic symbols called lexigrams with real world referents and the spoken English words and photographs for those referents. On some trials, an unknown spoken English word was presented as the sample, and the match choices could consist of photographs or lexigrams that already were associated with known English words as well as unknown lexigrams or photos of objects without associated lexigrams. The chimpanzee reliably avoided choosing known comparisons for these unknown samples, instead relying on exclusion to choose comparisons that were of unknown lexigrams or photographs of items without associated lexigram symbols.     

Case report on the death of a wild chimpanzee (Pan troglodytes verus)

The present paper gives a case report on the death of a wild young chimpanzee (Pan troglodytes verus) at Bossou, Guinea. The corpse of a 6.5-year-old male was found, and an autopsy suggested that he had died from some non-epidemic disease or from poisoning. Morphological measurements of the skeleton revealed that the chimpanzee was much smaller than corresponding individuals in captivity. The dental formula of the chimpanzee coincided with those of 5- to 5.5-year-olds in captivity. The death of this chimpanzee suggests that some of the individuals who had disappeared at Bossou had died of natural causes.     

Mortality and the magnitude of the "wild effect" in chimpanzee tooth emergence

Age of tooth emergence is a useful measure of the pace of life for primate species, both living and extinct. A recent study combining wild chimpanzees of the Taï Forest, Gombe, and Bossou by Zihlman et al. (2004) suggested that wild chimpanzees erupt teeth much later than captives, bringing into question both comparisons within the hominin fossil record and assessment of chimpanzees. Here, we assess the magnitude of the “wild effect” (the mean difference between captive and wild samples expressed in standard deviation units) in these chimpanzees. Tooth emergence in these wild individuals is late, although at a more moderate level than previously recorded, with a mean delay conservatively estimated at about 1 SD compared to the captive distributions. The effect rises to 1.3 SD if we relax criteria for age estimates. We estimate that the mandibular M1 of these wild chimpanzees emerges at about 3 ²/₃-3 ¾ years of age. An important point, often ignored, is that these chimpanzees are largely dead of natural causes, merging the effect of living wild with the effect of early death. Evidence of mortality selection includes, specifically: younger deaths appear to have been more delayed than the older in tooth emergence, more often showed evidence of disease or debilitation, and revealed a higher occurrence of dental anomalies. Notably, delay in tooth emergence for live-captured wild baboons appears lower in magnitude (ca. 0.5 SD) and differs in pattern. Definitive ages of tooth emergence times in living wild chimpanzees must be established from the study of living animals. The fossil record, of course, consists of many dead juveniles; the present study has implications for how we evaluate them.     

Hydroperoxy-cycloartane triterpenoids from the leaves of Markhamia lutea, a plant ingested by wild chimpanzees

In the framework of the phytochemical investigation of plant species eaten by wild chimpanzees in their natural environment in Uganda, leaf samples of Markhamia lutea were selected and collected. The crude ethyl acetate extract of M. lutea leaves exhibited significant in vitro anti-parasitic activity and low cytotoxicity against MRC5 and KB cells. Fractionation of this extract led to six cycloartane triterpenoids, musambins A–C and their 3-O-xyloside derivatives musambiosides A–C. The structures were elucidated on the basis of spectral studies including mass spectroscopy and extensive 2D NMR. Most of the compounds exhibited mild anti-leishmanial and anti-trypanosomal activities.     

Sperm quality and the morphology of cryopreserved testicular tissues recovered post-mortem from diverse wild species

This study compared the effects of slow and fast freezing of testicular tissue of wild animals collected at post-mortem on testicular structure and testicular sperm. The testes of seven animals that had died in captivity; three felids (jungle cat, lion and leopard), two cervids (rusa deer and fea’s muntjac) and two bovids (Sumatran serows) were cryopreserved using slow- and fast-freezing protocols. There were greater reductions in the integrity of the sperm membrane and DNA in tissues cryopreserved using slow freezing compared to fast freezing (membrane integrity reduced by 21.5 ± 12.4% vs. 13.0 ± 6.9%, P = 0.11 and DNA integrity reduced by 22.7 ± 16.3% vs. 6.6 ± 6.3%, P = 0.13). Histologically, there were similar degrees of detachment and shrinkage of the seminiferous tubules whereas, TUNEL assay revealed a tendency towards more apoptotic changes in the intra-tubular cells of tissues frozen using fast freezing compared to slow freezing (P = 0.09). In conclusion, fast freezing tended to cause less damage to testicular sperm but its protective effect on intra-tubular cells was likely compromised. This is the first report of gamete recovery in the wild and of the comparison in various wildlife species, between testicular tissues cryopreserved using different protocols.     

The learning and use of gestural signals by young chimpanzees: A trans-generational study

Observations of chimpanzee gestural communication are reported. The observations represent the third longitudinal time point of an ongoing study of the Yerkes Primate Center Field Station chimpanzee group. In contrast to observations at the first two time points, the current observations are of a new generation of infants and juveniles. There were two questions. The first concerned how young chimpanzees used their gestures, with special focus on the flexibility or intentionality displayed. It was found that youngsters quite often used the same gesture in different contexts, and different gestures in the same context. In addition, they sometimes used gestures in combinations in a single social encounter, these combinations did not convey intentions that could not be conveyed by the component gestures, however. It was also found that individuals adjusted their choice of signals depending on the attentional state of the recipient. The second question was how chimpanzees acquired their gestural signals. In general, it was found that there was little consistency in the use of gestures among individuals, especially for non-play gestures, with much individual variability both within and across generations. There were also a number of idiosyncratic gestures used by single individuals at each time point. It was concluded from these results that youngsters were not imitatively learning their communicatory gestures from conspecifics, but rather that they were individually conventionalizing them with each other. Implications of these findings for the understanding of chimpanzee communication and social learning are discussed.     

Sex differences in adult chimpanzee positional behavior: The influence of body size on locomotion and posture

Focal animal instantaneous sampling of adult male and female chimpanzee positional behavior was conducted during a 7-month study in the Tai Forest, Ivory Coast, in order to determine whether there are sex differences in the locomotion, posture, substrate use, and height preference of sexually dimorphic adult chimpanzees, and if so, whether these differences support predictions based on body size differences. Results indicate that as predicted, adult male and female chimpanzees differ in their arboreal locomotor behavior, with the larger males using less quadrupedalism and more climbing, scrambling, and aided bipedalism than females during feeding locomotion. There is a sex difference in height preference as well, with female chimpanzees consistently using more arboreal behavior than males, primarily during resting. Although it has been previously demonstrated that separate primate species of differing body size differ in locomotor and postural activities (Fleagle and Mittermeier, 1980; Crompton, 1984), this study clearly demonstrates that body size differences within a species can also be correlated with differences in locomotor behavior. These findings may influence how we interpret sex differences in body size of extinct species. © 1993 Wiley-Liss, Inc.     

Complete coding sequence and molecular analysis of hepatitis A virus from a chimpanzee with fulminant hepatitis

Background Hepatitis A virus (HAV) infects both humans and non‐human primates, in experimentally infected chimpanzees is typically milder than in humans. In 1982, Abe and Shikata reported a first case of a chimpanzee with fulminant hepatitis caused by spontaneous HAV infection, and the underlying mechanisms of the disease remain unknown. Methods To characterize denoted CFH‐HAV, we conducted cloning and near full‐length sequence analysis. Results Phylogenetic analyses of VP1‐2A and complete sequence comparison between various genotypes and the sample sequence showed clustering in genotype IB. Based on BLAST analysis, the sequence was most closely related to the wild‐type (HM175/WT) isolate. Amino acid and nucleic acid similarities were 99.8% and 94.41%, respectively. Conclusions The chimpanzee may have been infected with human HAV genotype IB. The substitutions in VP2, VP4, 2B, 2C, and 3D, which may enhance virus proliferation, contributed to disease severity culminating in fulminant hepatic failure.     

A bioluminescence assay to detect nitrification inhibitors released from plant roots: a case study with Brachiaria humidicola

A bioluminescence assay using recombinant Nitrosomonas europaea was adopted to detect and quantify natural nitrification inhibitors in plant–soil systems. The recombinant strain of N. europaea produces a distinct two-peak luminescence due to the expression of luxAB genes, introduced from Vibrio harveyi, during nitrification. The bioluminescence produced in this assay is highly correlated with NO₂⁻ production (r ² = 0.94). Using the assay, we were able to detect significant amounts of a nitrification inhibitor produced by the roots of Brachiaria humidicola (Rendle) Schweick. We propose that the inhibitory activity produced/released from plants be termed ‘biological nitrification inhibition’ (BNI) to distinguish it from industrially produced inhibitors. The amount of BNI activity produced by roots was expressed in units defined in terms of the action of a standard inhibitor allylthiourea (AT). The inhibitory effect from 0.22 μM AT in an assay containing 18.9 mM of NH₄⁺ is defined as one AT unit of activity. A substantial amount of BNI activity was released from the roots of B. humidicola (15–25 AT unit g⁻¹ root dry wt day⁻¹). The BNI activity released was a function of the growth stage and N content of the plant. Shoot N levels were positively correlated with the release of BNI activity from roots (r ² = 0.76). The inhibitor/s released from B. humidicola roots suppressed soil nitrification. Additions of 20 units of BNI per gram of soil completely inhibited NO₃⁻ formation in a 55-day study and remained functionally stable in the soil for 50 days. Both the ammonia monooxygenase and the hydroxylaminooxidoreductase enzymatic pathways in Nitrosomonas were effectively blocked by the BNI activity released from B. humidicola roots. The proposed bioluminescence assay can be used to characterize and determine the BNI activity of plant roots, thus it could become a powerful tool in genetically exploiting the BNI trait in crops and pastures.     

SIVcpz from a naturally infected Cameroonian chimpanzee: Biological and genetic comparison with HIV-1 N

Thus far, simian immunodeficiency virus from chimpanzees (SIVcpz) genomes have been characterized as Pan troglodytes troglodytes and show a strong relation with human immunodeficiency virus (HIV)-1 N in their env genes. We fully characterized another SIVcpz from P. t. troglodytes . This chimpanzee (Cam5) was, as was also the host of SIVcpz-cam3, wild born in Cameroon, a region where all three groups of HIV-1 (M, N and O) co-occur. In contrast to other SIVcpz, SIVcpz-cam5 was isolated immediately after the rescue of the animal. Our data demonstrate that SIVcpz-cam5, like SIVcpz-cam3, grows easily on human peripheral blood mononuclear cells (PBMCs) and uses CCR5 as a co-receptor similar to HIV-1 N YBF30. Phylogenetic analysis based on the entire env gene shows that SIVcpz-cam5 falls into the same unique subcluster as HIV-1 N YBF30, SIVcpz-cam3 and SIVcpz-US. A phylogenetic relationship was also found with the vif gene of HIV-1 N. This study provides proof that HIV-1 N related viruses circulate in wild P. t. troglodytes .     

The socio-economic importance of wild vegetable resources and their conservation: a case study from China

In the Xiangxi region of western Hunan province, China, 335 taxa belonging to 87 families and 119 genera are utilised as wild vegetables. In order to take advantage of this naturally occurring resource we examined the horticultural and the associated socio-economic aspects of these taxa. Wild vegetables, as the mainstay of human diet and Chinese traditional medicines, have played an important role in the daily life and income of local ethnic groups for centuries. We examine candidate species for their prevalence and their potential to offer returns, for example in cereal production and tourism, and indicate horticultural management and processing technologies which may exploit wild vegetable availability.     

Dynamics of seedling populations and tree species coexistence in a forest: a simulation study

Theoretically, temporal variation of reproduction promotes species coexistence of sessile and polycarpic organisms when the reproduction is synchronized within species but independent among species. Monopoly of vacant sites and high relative population growth rate of minor species in the absence of propagules of other species is the essence of this mechanism. The mechanism is expected to work in forests, but persistent populations of seedlings may affect the promotion of coexistence. Using a tree-based simulation model of forest dynamics, it was demonstrated that the number of coexisting tree species was sensitively affected by the seedling establishment rate. The coexistence was not enhanced by temporal variation of reproduction when seedling establishment rate was low. This is because the reproducing minor species fail to monopolize vacant sites and allow the establishment of seedlings of other species in later years. High mortality of established seedlings under shade also suppressed coexistence. This is likely to be the result of a reduced storage effect of the population of seedlings. A forest structure and dynamics pattern that appears when tree species coexistence is promoted by fluctuating reproduction was searched for, and the number of coexisting species was varied by manipulating the seedling establishment rate. No distinct difference other than the species number itself was found between species-rich and species-poor forests. For example, the seedling population size varied, reflecting the temporal variation of reproduction, irrespective of the seedling establishment rate. Further strategy development is needed to validate the proposed mechanisms of species coexistence.