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

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

Female contributions to the peaceful nature of bonobo society

Although chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) are closely related, females of the two species show surprisingly large differences in many behavioral aspects. While female chimpanzees tend to range alone or in small parties during non-estrous periods, female bonobos aggregate even more often than do males. Female chimpanzees do not have frequent social interactions with other females, whereas female bonobos maintain close social associations with one another. Although the ranging patterns of chimpanzee parties are generally led by males, female bonobos often take the initiative in ranging behavior. While female chimpanzees usually do not exhibit estrus during postpartum amenorrhea or pregnancy, female bonobos exhibit a prolonged pseudo-estrus during such non-conceptive periods. Studies of these two species have also shown great differences in agonistic behaviors performed by males. Male chimpanzees frequently fight with other males to compete for estrous females, but male bonobos seldom do so. While there are many records of infanticide by male chimpanzees, there is no confirmed record of such an event among bonobos. Several cases of within-group killing among adult male chimpanzees have been reported, but there is no such record for bonobos. While intergroup conflicts among chimpanzees sometimes involve killing members of the other group, intergroup conflicts among bonobos are considerably more moderate. In some cases, bonobos from two different groups may even range together for several days while engaging in various peaceful interactions. I will address two important questions that arise from these comparisons, exploring why females of such closely related species show such clear differences in behavior and whether or not the behavioral characteristics of female bonobos contribute to the peaceful nature of bonobo society.     

Chimpanzee grouping patterns and food availability in Mahale Mountains National Park,Tanzania

The aim of this study was to test for a correlation between party size and food (fruit) availability among the M group chimpanzees (Pan troglodytes) in the Mahale Mountains, Tanzania. Chimpanzee unit groups (or communities) show fission–fusion grouping patterns and form temporal parties. Fruit availability is assumed to be one of the important limiting factors in relation to the size of these parties. Different methods have been proposed to measure party size, but they all appear to focus mainly on two aspects of grouping phenomena. In “face-to-face parties”, party size is measured by scan sampling, whereas in “nomadic parties”, all members observed during a specific time period are counted. The mean monthly group size resulting from these two measures was compared with fruit availability, i.e. fruiting plant density and mean potential patch size. Nomadic party size was correlated with both values. Thus, party formation at this level was considered to be sensitive to overall fruit availability in the habitat. On the other hand, face-to-face party size remained stable and showed weak or no correlations with density and potential patch size. Although large patches are available during the peak fruiting season, Mahale chimpanzees depend on the liana species Saba comorensis, which, when fruiting, encourages individuals to spread out to eat. Thus, the lack of correlation between face-to-face-party size and fruit availability was attributed to the influence of physical limitations countervailing the fluctuation in fruit availability. Maximum face-to-face party size relative to unit-group size, regarded as the cohesiveness of a unit group, was compared among sites. The values differed largely: Mahale groups M and K, Bossou, and, in some years, Budongo, showed high cohesiveness, while others remained low. Thus, the distribution of the most important food during the fruiting season in each study site may be a crucial factor in the grouping phenomena of chimpanzees.     

Factors affecting party size and composition of chimpanzees (Pan troglodytes verus) Bossou,Guinea

I studied the party sizes of western chimpanzees (Pan troglodytes verus)and factors assumed to affect them at Bossou, Republic of Guinea, West Africa. Party size is negatively correlated with feeding ratio, and larger parties tend to be formed in more dangerous situations (i.e. crossing roads with much traffic). When parties included estrous females, young (i.e., late juvenile and adolescent) males tended to forage with them, independently from their mothers. Lactating females with infants tended to spend more time alone, but the trend was not as apparent as it is in P. t. schweinfurthiat Gombe, Tanzania. These facts suggest that several factors, in addition to food availability, affect party formation, or fission-fusion, of chimpanzees. I also briefly discuss comparatively the pattern of party formation in P. paniscus.     

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

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

Comparison of behavioral sequence of copulation between chimpanzees and bonobos

We compared sex differences in behaviors leading to copulation of chimpanzees (Pan troglodytes) in the Kalinzu Forest, Uganda with those of bonobos (Pan paniscus) at Wamba, D.R. Congo, using the same definition. Female chimpanzees were more likely to initiate copulation than female bonobos. While most of copulations (96%) were initiated by males in bonobos, among chimpanzees only 63% of copulations were initiated by males. Female bonobos initiated an interaction leading to copulation when males approached them within a short distance. On the other hand, both male and female chimpanzees initiated behavior at a longer distance. Higher proceptivity and a higher copulation rate during the maximal swelling period of female chimpanzees might suggest that they gain greater benefits from a high frequency of copulations than do female bonobos.     

Factors Affecting Party Size in Chimpanzees of the Mahale Mountains

We studied factors affecting party size and composition of wild chimpanzees at Mahale (M group) over an 11-month period. Parties with 1–5 individuals were most frequent (37.8%; 153/405 parties); they included 94.7% of all male parties (n = 76) and 81.3% of all female parties (n = 75). The median of monthly values was the standard for analysis. We divided the year into four periods based on the median size of monthly bisexual parties (30.9 individuals; includes both males and females): monthly bisexual party sizes were larger in May–June (period II) and October–January (period IV) and smaller in February–April (period I) and July–September (period III). Only bisexual parties changed in size with period. The number of fruit items (=species) eaten was fewer in periods II and IV when abundance per item appeared to be great. The sizes of bisexual parties, which included cycling females with maximal anogenital swelling, were larger, and their representation (%) in all bisexual parties was greater in periods III and IV. The numbers of both cycling females and cycling females with maximal anogenital swelling were also larger in periods III and IV. The percentage of cycling females with maximal anogenital swelling was greater in periods II and III. The results of this study and those of Nishida (1979) suggest that seasonal variation in party size of Mahale chimpanzees maintains a relatively consistent annual cycle. The factors assumed to affect party sizes are fruit availability and the presence of cycling females with maximal anogenital swelling.     

Age-related changes in urinary testosterone levels suggest differences in puberty onset and divergent life history strategies in bonobos and chimpanzees

Research on age-related changes in morphology, social behavior, and cognition suggests that the development of bonobos (Pan paniscus) is delayed in comparison to chimpanzees (Pan troglodytes). However, there is also evidence for earlier reproductive maturation in bonobos. Since developmental changes such as reproductive maturation are induced by a number of endocrine processes, changes in hormone levels are indicators of different developmental stages. Age-related changes in testosterone excretion are an indirect marker for the onset of puberty in human and non-human primates. In this study we investigated patterns of urinary testosterone levels in male and female bonobos and chimpanzees to determine the onset of puberty. In contrast to other studies, we found that both species experience age-related changes in urinary testosterone levels. Older individuals of both sexes had significantly higher urinary testosterone levels than younger individuals, indicating that bonobos and chimpanzees experience juvenile pause. The males of both species showed a similar pattern of age-related changes in urinary testosterone levels, with a sharp increase in levels around the age of eight years. This suggests that species-differences in aggression and male mate competition evolved independently of developmental changes in testosterone levels. Females showed a similar pattern of age-related urinary testosterone increase. However, in female bonobos the onset was about three years earlier than in female chimpanzees. The earlier rise of urinary testosterone levels in female bonobos is in line with reports of their younger age of dispersal, and suggests that female bonobos experience puberty at a younger age than female chimpanzees.     

Seasonality and Socioecology: The Importance of Variation in Fruit Abundance to Bonobo Sociality

The assumption that nonseasonal, evergreen, rain forests contain more continuously available food resources than seasonal rain forests is fundamental to comparisons made between the socioecology of the male-bonded Pan troglodytes and the female-based social system of the Pan paniscus. Chimpanzee females may be less social due to the high costs of feeding competition, whereas in the more food-rich central African rain forests such as the Lomako forest, female bonobos can associate and socially bond. The Lomako Forest experiences two wet and two dry seasons a year. Data on fruit abundance and sociality show that despite monthly variation in fruit availability, there was no consistent seasonal variation in fruit abundance or dietary breadth. Bonobo use of nonfig fruits, figs, THV, and leaves did not follow seasonal patterns. Leaves and THV may act as complementary sources of plant protein and their use was inversely correlated. Monthly variation in fruit abundance was associated with a significant decrease in the number of males in a party but not in the number of females. Focal males were frequently solitary during 1 of the 3 months with the smallest party sizes. In contrast, females remained social with each other throughout the year. Therefore, seaonality at Lomako appeared to be less marked than at comparable chimpanzee sites, such that the variation in fruit abundance did not fall below a level that prohibits female sociality.     

Urinary C-peptide levels in male bonobos (Pan paniscus) are related to party size and rank but not to mate competition

Within- and between-species variation in male mating strategies has been attributed to a multitude of factors including male competitive ability and the distribution of fertile females across space and time. Differences in energy balance across and within males allow for the identification of some of the trade-offs associated with certain social and mating strategies. Bonobos live in groups with a high degree of fission–fusion dynamics, there is co-dominance between the sexes and a linear dominance hierarchy among males. Males compete over access to females, breeding is aseasonal, and females exhibit sexual swellings over extended time periods. In this study we use urinary C-peptide (UCP) levels in male bonobos (Pan paniscus) obtained from 260 urine samples from a wild bonobo community, to quantify male energy balance during mate competition and levels of gregariousness in the species. Although high ranking males are more aggressive, spend more time in proximity to maximally tumescent females, and have higher mating frequencies, we found no indication that mate guarding or mate competition affected male energy balance. Our results showed a positive correlation between monthly mean UCP levels and mean party size. When traveling in large parties, high ranking males had higher UCP levels than those of the low ranking males. These results support the hypothesis that patterns of fission–fusion dynamics in bonobos are either linked to energy availability in the environment or to the energetic costs of foraging. The finding of a rank-bias in UCP levels in larger parties could also reflect an increase in contest competition among males over access to food.     

Female Coalitions Against Male Aggression in Wild Chimpanzees of the Budongo Forest

In the wild, female chimpanzees (Pan troglodytes) are subject to male aggression that at times can be prolonged or particularly violent. There are no reports of cooperative retaliation to such aggression, a strategy observed in the congeneric Pan paniscus, from the wild despite >4 decades of detailed behavioral study across a number of populations and its occurrence among captive female chimpanzees. If the reports from captivity represent an inherent capacity, then the absence of similar reports from wild populations suggests that females may be able to form coalitions only under appropriate ecological and demographic conditions. During a study of male and female aggressive interactions among chimpanzees of the Budongo Forest, Uganda, wild adult female chimpanzees sometimes formed coalitions with one another to retaliate against male aggression. This may be possible because these females tend to be more gregarious than in other populations of East African chimpanzees, as other studies of the same population have suggested; the extent and variation of female chimpanzee social strategies may, therefore, need reconsideration. Further, my observations strengthen the argument that at least some of the differences between chimpanzees and bonobos may be more of degree than of kind.     

Distribution of terrestrial herbaceous vegetation and its consumption by Pan paniscus in the Lomako Forest,Zaire

Data available on behavior and morphology of Pan paniscus (bonobos) suggest that terrestrial herbaceous vegetation (THV) is an important component of their diet and that it may be preferred by bonobos to a greater extent than by chimpanzees (Pan troglodytes). It has also been reported that THV is ubiquitously distributed in the lowland rain forests inhabited by bonobos. These data suggest that THV exploitation may be causally related to the evolution of the more cohesive social system found in bonobos compared to that of chimpanzees. Here, we present data that quantify the spatial distribution of THV in the Lomako Forest, an analysis of the nutrient content of the plant parts commonly consumed, and patterns of THV consumption in relation to its distribution. The data clearly demonstrate that THV, and particularly Haumania liebrechtsiana (Marantaceae), is ubiquitously distributed as previously suggested. However, THV feeding patches are rare because of distinct feeding preferences. Bonobos preferentially choose H. liebrechtsiana over other species of THV, choose patches with larger stems, and, within patches, choose larger stems over smaller stems. The plant parts chosen are high in proteins and relatively low in carbohydrates. Given the selectivity of the study population and the patchy distribution of THV, it is unlikely that THV has been responsible for the evolution of the unique social system reported for bonobos. Data presented on party size are consistent with this conclusion.     

Do bonobos copulate more frequently and promiscuously than chimpanzees?

The copulatory activities of bonobos (Pan paniscus) of Wamba, Zaire, were compared with those of chimpanzees (P. troglodytes schweinfurthii) of Mahale, Tanzania. The copulation rates of adult male bonobos were equal to or lower than those of adult male chimpanzees. The copulation rates of adult female bonobos were approximately equal to those of adult female chimpanzees who were in maximal genital swelling, but it should be much higher than those of the adult female chimpanzees throughout the birth interval. The copulation rates of adolescent male bonobos were lower than those of adolescent male chimpanzees, whereas the copulation rates of adolescent female bonobos were much higher than those of adolescent female chimpanzees. It was suggested that the bonobos of Wamba did not copulate more promiscuously than did the chimpanzees of Mahale. The female bonobos may show “receptivity”, whereas female chimpanzees may show rather “proceptivity”.     

Mahale chimpanzees: grouping patterns and cycling females

The social system of chimpanzees (Pan troglodytes schweinfurthii) is characterized by the fission-fusion of social groups. Several studies have reported that females are less gregarious than males. In the current study, adult female gregariousness depended on their reproductive state. Noncycling adult females (pregnant, lactating, or post reproductive) were observed in large bisexual parties less often than cycling adult females. On the other hand, cycling adult females were observed in large bisexual parties as often as males, regardless of their estrous state. More males were in parties that included cycling adult females with maximal genital swelling (estrous females) than in parties without them. Moreover, a bisexual party including more estrous females contained more males. These results suggest that large bisexual parties of chimpanzees are constructed by a dual mechanism. First, cycling adult females are attracted to parties that consist of the top ranking male and large numbers of adult and adolescent males. Second, adult and adolescent males that did not belong to parties originally are attracted by estrous females and join them. Thus, in Mahale Mountains National Park, Tanzania, bisexual parties of chimpanzees can be characterized as "parties for reproduction."     

Influence of Seasonality on Activity Patterns, Feeding Behavior, Ranging, and Grouping Patterns in Taï Chimpanzees

Lowland rain forest chimpanzees (Pan troglodytes verus) of the Taï National Park, Ivory Coast, responded to the minor dry season (July and August) of 1988 in a predictable manner by spending more time feeding, feeding more frequently on lower quality food items, reducing day range and party size, and spending more time solitarily and less time in mixed groups than during the rainy season. These behaviors are consistent with a response to scarce resources. My findings do not support Boesch's (1991, 1996) hypothesis of bisexually bonded chimpanzees. Females spent 45% of time alone and associated with males in mixed parties only 18% of their time. This major discrepancy in our results probably stems from differences in the time of year when our studies were conducted, the year in which my study was conducted (potentially scarcer resources than on average), and methodological differences: focal animal sampling of males and females equally. Although Boesch (1991, 1996) and Steiner (1996) have demonstrated that Taï parties are usually larger and more mixed, Taï chimpanzee social structure—party size and composition—during this study closely resembles that found at other study sites.     

Grouping Patterns and Competition Among Female <Emphasis Type="Italic">Pan troglodytes schweinfurthii</Emphasis> at Ngogo,Kibale National Park,Uganda

In mammals, access to mates is probably the most important influence on male reproductive success, whereas foraging efficiency is probably the most important influence on female reproductive success Emlen and Oring (Science 197:215–223, 1977). Male chimpanzees (Pan troglodytes) are highly gregarious and form cooperative relationships with other males. In contrast, female social relationships vary within and between populations. Females in most East African populations, e.g., Gombe, Mahale, Kibale-Kanyawara, are less gregarious than males and spend most of their time alone or with only their dependent offspring. Researchers have attributed low female gregariousness to the high potential for feeding competition. I provide the first data on association patterns and agonistic interactions of female chimpanzees (Pan troglodytes schweinfurthii) from the unusually large Ngogo community, Kibale National Park, Uganda. Ngogo females were less gregarious than males, but spent a mean of 64% of their time in association with ≥1 other females and as much time in all-female parties as they did alone. Further, female dyads associated nonrandomly and they formed associative cliques. Association levels within cliques were similar to those among the relatively gregarious West African chimpanzee females at Taï (Pan troglodytes verus) and among bonobo (P. paniscus) females. Agonistic interfemale interactions were extremely rare, and monthly mean party size and the numbers of anestrous females per party do not correlate significantly with fruit availability. Thus, Ngogo females maintained relatively high levels of gregariousness, but avoided detrimental feeding competition by preferentially associating with a small subset of other community females.     

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.     

Reproductive Parameters of Female<Emphasis Type="Italic">Pan paniscus</Emphasis> and <Emphasis Type="Italic">P. troglodytes</Emphasis>: Quality versus Quantity

We investigated intra- and interspecific differences in life history and reproductive parameters in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We compare the parameters of wild and captive females in order to shed light on the influence of habitat or specific differences or both on reproduction. We present new and additional information on reproductive parameters from captive bonobos and chimpanzees. Captive chimpanzees birth more live offspring and have a shorter interbirth interval, but experience higher infant mortality than captive bonobos. Although captive bonobo females tend to start reproduction at a younger age than chimpanzees, this is effectively only so for wild-born females of both species. Ultimately both species reach the same rate of production of offspring surviving to 5 yr. These results contrast with data from the wild. Wild bonobos tend to have higher reproductive success, a higher fertility rate and a shorter interbirth interval than wild chimpanzees. Reproduction is similar for wild and captive bonobos, which suggests that they are producing at their maximum under both conditions. Overall captive chimpanzees perform better than their wild conspecifics, probably because of lower feeding competition. Infant survival is the only specific difference not affected by captivity. Bonobo infants survive better, which suggests that chimpanzee infants are more at risk. We argue that the interspecific variation in reproductive parameters in captivity is related to the different influence of captivity on reproduction and different pressures of external sources of infant and juvenile mortality.     

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.     

How fruit abundance affects the chimpanzee party size: a comparison between four study sites

We examined the relationship between fruit abundance and chimpanzee (Pan troglodytes) party size by comparing data from four study sites: the Kalinzu Forest Reserve, Uganda, the Djinji Camp and Guga Camp in the Ndoki Forest, Congo, and Kahuzi-Biega National Park, Democratic Republic of Congo. Although the difference in the fruit abundance between the sites was responsible for the difference in the party size between the sites, the seasonal changes in fruit abundance did not explain the changes in the party size in each study site. Across the four study sites, there were significant correlations of the mean and minimum of monthly party size with the mean of monthly fruiting-tree density, and a significant correlation of the maximum of monthly party sizes with the minimum of monthly fruiting-tree density. We proposed a hypothesis that (1) the monthly fruit abundance affects the monthly party size in the sites where the fruit availability is as low as to limit the party size during a major part of a year, while (2) the party size does not increase with the increase in the monthly fruit abundance, but is affected by other social factors, in the sites where the minimum of monthly fruit abundance is high enough for chimpanzees to form parties of an adequate size. Electronic Publication