Phrase structure of wild chimpanzee pant hoots: Patterns of production and interpopulation variability

Recordings and behavioral observations of wild chimpanzees were made over a 2-year period in the Kibale National Park, Uganda (Kanyawara and Ngogo communities) to investigate patterns of acoustic variability in long-distance calls. The phrase structures of pant hoots, the species-typical loud call given predominantly by adult males, were analyzed. Analysis revealed that the build-up phrase was frequently absent from the pant hoots of Kibale chimpanzees. By contrast, analysis of published data on Gombe and Mahale chimpanzees (Tanzania) indicated that these animals typically included the build-up in their calls. These results were interpreted as evidence for phrase-level differences between populations in the acoustic morphology of this compound call. Data on age and sex differences in the context of production of pant hoots were analyzed, and their relevance to the possibility that aspects of pant hoot acoustic morphology are learned is discussed. Adult males initiated pant hoots more than subadult males, and adult males joined other pant hooting individuals with pant hoots more than subadult males did. It is suggested that younger males may pant hoot with specific adult males preferentially and that this may affect the development of their pant hoot acoustic morphologies. A peculiar pant hoot variant previously reported from Gombe, the whimper hoot, is described from Kibale. The production of this call by low-ranking individuals suggests that there are social constraints on pant hooting in the chimpanzee community. Ideas concerning the effect of social relationships on interpopulation variability in vocal signals are briefly discussed. © 1996 Wiley-Liss, Inc.     

Trade-offs in the production of animal vocal sequences: insights from the structure of wild chimpanzee pant hoots

Background

Vocal sequences - utterances consisting of calls produced in close succession - are common phenomena in animal communication. While many studies have explored the adaptive benefits of producing such sequences, very little is known about how the costs and constraints involved in their production affect their form. Here, we investigated this issue in the chimpanzee (Pan troglodytes schweinfurthii) pant hoot, a long and structurally complex vocal sequence comprising four acoustically distinct phases – introduction, build-up, climax and let-down.

Results

We found that in each of these phases, and for the sequence as a whole, there was a negative relationship between the number of calls produced and their average duration. There was also a negative relationship between the total duration of some adjacent phases. Significant relationships between the fundamental frequency of calls and their number or duration were found for some phases of the sequence, but the direction of these relationships differed between particular phases.

Conclusions

These results indicate that there are trade-offs in terms of signal duration at two levels in pant-hoot production: between call number and duration, and between the relative durations of successive phases. These trade-offs are likely to reflect biomechanical constraints on vocal sequence production. Phase-specific trade-offs also appear to occur between fundamental frequency and call number or duration, potentially reflecting that different phases of the sequence are associated with distinct types of information, linked in different ways to call pitch. Overall, this study highlights the important role of costs and constraints in shaping the temporal and acoustic structure of animal vocal sequences.

     

Identification of wild chimpanzee hair samples from feces by electron microscopy

A large bolus of hairs found in the feces of an adult wild chimpanzee in the Budongo Forest, Uganda, was identified as belonging to a chimpanzee below the age of 3 yrs. This represents the second case of infant-eating recorded in the Budongo Forest.     

Acoustic variation of pant hoot calls by male chimpanzees: a playback experiment

Pant hoots, a type of long-distance calls of chimpanzees (Pan troglodytes), were played back to two male chimpanzees in a group of seven captive individuals to determine if chimpanzees would modify those vocalizations in response to strange males. Subjects emitted pant hoots with higher rates of delivery, shorter duration of buildup, and lower minimum fundamental frequency of climax when they were presented with pant hoots of strangers than when they produced the calls spontaneously. Considering the direction of acoustical change, we concluded that the rate of delivery, duration of buildup, and minimum frequency of climax might be associated with the underlying emotional states of the callers rather than call matching. Individual difference between two subject males was significant in minimum frequency and duration of climax and in average frequency of call, which appears to reflect differences of the caller's age and social status. These results suggest that different acoustic variables relate to within- and interindividual differences of these vocalizations. Received: March 7, 2000 / Accepted: May 8, 2000     

Buttress drumming by wild chimpanzees: Temporal patterning, phrase integration into loud calls, and preliminary evidence for individual distinctiveness

Wild chimpanzees (Pan troglodytes) generate low-frequency sounds that are audible to humans from a distance of at least 1 km away by hitting the buttresses of trees with their hands and feet. This buttress drumming occurs in discrete bouts of rapidly delivered beats that usually accompany “pant hoots,” the species-specific long-distance vocalization. Individual differences in male chimpanzee (P.t. verus) drumming were investigated during a 6-month field study in the Taï National Park, Ivory Coast. Analysis of drumming bouts recorded from six adult males revealed significant differences between individuals in three acoustic features: (1) mean duration of inter-beat interval; (2) mean number of beats per bout; and (3) mean bout duration. Preliminary analysis indicated that individuals differ in their tendency to deliver drum beats in temporally close pairs separated by longer interbeat intervals. Qualitative examination also suggested that individuals may differ in the temporal integration of drumming into the pant hoot vocalization. These results suggest that there may be acoustic cues available for chimpanzees to recognize unseen males by their drumming performances alone. Drumming by Taï chimpanzees was also compared to drumming by chimpanzees (P.t. schweinfurthii) from the Kanyawara study group in Kibale National Park. Uganda. The Kanyawara chimpanzees appeared to drum more often without vocalizing than did the Taï chimpanzees. When they did drum and vocalize together, the Kanyawara chimpanzees appeared to integrate their drumming later into the associated pant hoots than did the Taï chimpanzees. These results suggest the possibility that interpopulation variation exists in chimpanzee buttress drumming.     

Experimental analyses of body image in the chimpanzee

It is difficult to study body image in animals. In this study, it is assumed that the perception of the body of others reflects body image. The perception of the human face was examined in a series of six experiments with a chimpanzee. Delayed-matching-to-sample tasks were employed. Although the chimpanzee mastered the tasks and showed transfer of performance to new faces, subtle changes in the matching face resulted in the deterioration of performance. Responses of the chimpanzee were often controlled by factors other than the facial stimuli. Thus, although the chimpanzee has a body image as humans do, it may not be as clear and as segmented.     

Acquisition and transfer of visual Go/No-go discrimination by a chimpanzee

An adolescent female chimpanzee was trained to press a key in the presence of a computer-graphic geometric figure (“Go” stimulus) within 5 sec and not to press the key during 5-sec presentations of another figure (“No-go” stimulus) with food reinforcement. In the acquisition training, the accuracy of performance increased primarily as a result of learning to inhibit key presses in No-go trials. The chimpanzee acquired this “Go/No-go” visual discrimination task in 1,260 trials. She was then given 14 successive transfer problems. The results for these problems suggested that learning-set formation and repeated use of the same discriminative stimuli both influenced transfer to new problems.     

Distribution of the pulmonary artery and vein in the chimpanzee lung

Lungs of two chimpanzees (Pan troglodytes) were examined. The right pulmonary artery runs across the ventral side of the right upper lobe bronchiole and, then across the dorsal side of the right middle lobe bronchiole. Thereafter, it runs between the dorsal bronchiole system and the lateral bronchiole system, along the right bronchus. During its course, it gives off arterial branches which run along each bronchiole. The left pulmonary artery runs across the dorsal side of the left middle lobe bronchiole and then between the dorsal bronchiole system and the lateral bronchiole system. The branches of the pulmonary artery run mainly along the dorsal or lateral side of the bronchiole. The pulmonary veins run mainly along the ventral or medial side of the bronchioles, and between them. Finally, they enter the left atrium with four large veins, i.e. the common trunk of the right upper lobe vein and the right middle lobe vein, right lower lobe pulmonary venous trunk, left middle lobe vein, and left lower lobe pulmonary venous trunk.     

Comparative genomic analysis of human and chimpanzee proteases

Proteolytic enzymes are implicated in multiple physiological and pathological processes. The availability of the sequence of the chimpanzee genome has allowed us to determine that the chimpanzee degradome-the repertoire of protease genes from this organism-is composed of at least 559 protease and protease-like genes and is virtually identical to that of human, containing 561 genes. Despite the high degree of conservation between both genomes, we have identified important differences that vary from deletion of whole genes to small insertion/deletion events or single nucleotide changes that lead to the specific gene inactivation in one species, mostly affecting immune system genes. For example, the genes encoding PRSS33/EOS, a macrophage serine protease conserved in most mammals, and GGTLA1 are absent in chimpanzee, while the gene for metalloprotease MMP23A, located in chromosome 1p36, has been specifically duplicated in the human genome together with its neighbor gene CDC2L1. Other differences arise from single nucleotide changes in protease genes, such as NAPSB and CASP12, resulting in the presence of functional genes in chimpanzee and pseudogenes in human. Finally, we have confirmed that the Trypanosoma lytic factor HPR is inactive in chimpanzee, likely contributing to the susceptibility of chimpanzees to T. brucei infection. This study provides the first analysis of the chimpanzee degradome and might contribute to the understanding of the molecular bases underlying variations in host defense mechanisms between human and chimpanzee.     

Effect of species-specificity in auditory-visual intermodal matching in a chimpanzee (Pan troglodytes) and humans

The goal of this study was to compare the performance of a chimpanzee and humans on auditory-visual intermodal matching of conspecifics and non-conspecifics. The task consisted of matching vocal samples to facial images of the corresponding vocalizers. We tested the chimpanzee and human subjects with both chimpanzee and human stimuli to assess the involvement of species-specificity in the recognition process. All subjects were highly familiar with the stimuli. The chimpanzee subject, named Pan, had had extensive previous experience in auditory-visual intermodal matching tasks. We found clear evidence of a species-specific effect: the chimpanzee and human subjects both performed better at recognizing conspecifics than non-conspecifics. Our results suggest that Pan's early exposure to human caretakers did not seem to favor a perceptual advantage in better discriminating familiar humans compared to familiar conspecifics. The results also showed that Pan's recognition of non-conspecifics did not significantly improve over the course of the experiment. In contrast, human subjects learned to better discriminate non-conspecific stimuli, suggesting that the processing of recognition might differ across species. Nevertheless, this comparative study demonstrates that species-specificity significantly affects intermodal individual recognition of highly familiar individuals in both chimpanzee and human subjects.     

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.     

The bronchial tree and lobular division of the chimpanzee lung

The bronchial ramification and lobular division in lungs of two chimpanzees (Pan troglodytes) were examined from the viewpoint of comparative anatomy, on the basis of the fundamental structure of bronchial ramification of the mammalian lung (Nakakuki, 1975, 1980). The right lung of the chimpanzee consists of the upper, middle, and lower lobes, whereas the left lung consists of the middle and lower lobes. The right and left lungs have the dorsal bronchiole system, lateral bronchiole system, and medial bronchiole system. The ventral bronchiole system is lacking on both sides. The right upper lobe is formed by the first branch of the dorsal bronchiole system. The right middle lobe is formed by the first branch of the lateral bronchiole system, and the right accessory lobe bronchiole is lacking. The remaining bronchioles constitute the right lower lobe. In the left lung, the upper and accessory lobes are lacking. The well developed middle lobe is formed by the first branch of the lateral bronchiole system. The left lower lobe is formed by the remaining bronchioles. Furthermore, these bronchioles are compared with those of the human lung byBoyden (1955).     

A case of offspring desertion by a female chimpanzee and the behavioral changes of the abandoned offspring

In the Mahale Mountains National Park, Tanzania, a chimpanzee mother moved to a neighboring unit-group leaving her 5-year-old son behind in the original group. The mother remained in the new group for ten months and then after conceiving, returned to the original group. The mother and son were reunited again but the son died of illness two months later. The mother gave birth to a baby in the original group but eventually transferred to the neighboring group after that baby disappeared. This is the first record of an immature chimpanzee abandoned by its emigrating mother, although a similar phenomenon has been reported for gorillas and Hanuman langurs. The abandoned offspring followed an adult male of the unit-group and the male was the individual who gave most of the care to the offspring. The offspring's time spent on grooming others increased, the time spent on being groomed decreased, and the rate of aggression toward him increased after his mother's desertion. This report will occasion to reconsider the previous notion of all-powerful mother-offspring bond in chimpanzees.     

A method of identifying chimpanzee hairs in lion feces

Hairs were detected in the feces of wild lions collected at the Mahale Mountains National Park, Tanzania. The materials were examined for their scale pattern, medulla arrangement, and ultrastructure of longitudinal sections. The observed features coincided with those of the chimpanzee, so that the hairs were judged to be from chimpanzees. The present results suggest that black hairs in lion feces can be identified as belonging to chimpanzees based on observations by scanning electron microscopy.     

Multidimensional auditory stimulus control in a chimpanzee (Pan troglodytes)

An adolescent female chimpanzee (Pan troglodytes) was trained to discriminate auditory compound stimuli differing in tonal frequency and/or tone on-off rate. Following acquisition training and overtraining, she was shifted to multidimensional stimulus control testing using redundant relevant auditory stimulus sets with discriminability of elements in each dimension varied systematically. Although the control by both dimensions changed significantly as a function of discriminability, the degree of dimensional control was stronger in the tone on-off rate than in the tonal frequency. These results clearly demonstrated “attentional” control of the chimpanzee's auditory discrimination behavior and the interaction between two dimensions of auditory stimuli. The author is now at the Department of Psychology, Primate Research Institute, Kyoto University as a transfer student of the Doctor course.     

Fruit availability and chimpanzee party size at Kahuzi montane forest,Democratic Republic of Congo

The effect of fruit availability on chimpanzee party size was investigated in the montane forest of Kahuzi. Seasonal variation in both fruit availability and party size was examined. Fruit abundance per se does not affect chimpanzee party size. However, seasonality and distribution patterns of fruits are both determinant ecological factors that control the size of chimpanzee parties at Kahuzi. There was no correlation between fruit abundance and the spatial distribution of fruits. When fruits were clumped and available in large amounts for a long period, chimpanzee party size increased, or otherwise decreased when fruits were highly available for only a limited period. Tree species that produced only a small amount of ripe fruit throughout the year did not affect the foraging party size of chimpanzees. Temporal and spatial variability in fruit abundance seems to constrain grouping patterns of chimpanzees at Kahuzi more so than in other chimpanzee habitats previously described.     

Socioecological factors of male chimpanzee migration at Bossou, Guinea

For more than 21 years a small semi-isolated group of wild chimpanzees have been studied at Bossou, Guinea, west Africa. All individuals have been identified since the beginning of the study. Remaining rates of infants (0–3 yr) and juveniles (4–7 yr) in the group were 64–80% for both sexes, however, those of adolescents (8–11 yr) dropped drastically, particularly for males (14%). As a result, most natal males as well as females disappeared before fully maturing. Two male visitors and an immigrant were observed in the group. More adult males than females disappeared from Bossou. Group males could be excluded as the genetic father of an offspring born in the group. From these demographic trends it is highly likely that some of these males emigrated rather than succumbed to sickness and death. It seems likely that they left on their own by choice. The reason for male dispersal is hypothesized to be influenced by intra-group male-male competition and the habitat ecology and structure of Bossou. There are no competitive adjacent groups or predators to prevent males from living alone and males can sire offspring out of their natal group.     

Divergent microsatellite evolution in the human and chimpanzee lineages

Comparison of the complete human genome sequence to one of its closest relatives, the chimpanzee genome, provides a unique opportunity for exploring recent evolutionary events affecting the microsatellites in these species. A simple assumption on microsatellite distribution is that the total length of perfect repeats is constant compared to that of imperfect ones regardless of the repeat sequence. In this paper, we show that this is valid for most of the chimpanzee genome but not for a number of human chromosomes. Our results suggest accelerated evolution of microsatellites in the human genome relative to the chimpanzee lineage.