Animals and mushrooms consumed by bonobos ( Pan paniscus ): New records from lilungu (Ikela), Zaire

We list the animal species, mushrooms and honey, which are consumed by bonobos (Pan paniscus)in the Ikela region (Lilungu), Republic of Zaire, and compare these data with those obtained from other populations of bonobos: Lomako, Yalosidi, and Wamba. Lilungu bonobos consume earthworms more regularly than bonobos do at other localities. They also eat larvae, termites, and ants, but they probably do not consume invertebrates as regularly as chimpanzees do. Lilungu bonobos ate a squirrel and a chiropteran. We report our detailed observations of bonobo foraging, feeding and manipulating foods, including washing some items and complicated handling operations. We note intra- and intergroup differences in the consumption of specific foods and in the way they are handled by the females.     

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.     

Behavior of bonobos (Pan paniscus) following their capture of monkeys in Zaire

For the first time, three cases of capture and forced interaction were observed between bonobos (Pan paniscus)and two other species of primates (Colobus angolensisand Cercopithecus ascanius)in the Lilungu (Ikela) region, Republic of Zaire. The bonobos interacted with the captured primates as if they were dealing with individuals of their own species. They sought cooperation in their interactions with the captured young primates without scccess. There is no evidence that they ate the captives.     

Social grooming among wild bonobos (Pan paniscus) at Wamba in the Luo Scientific Reserve, DR Congo, with special reference to the formation of grooming gatherings

Chimpanzees (Pan troglodytes) groom in gatherings in which many individuals may be connected via multiple chains of grooming and they often exchange partners with each other. They sometimes groom another while receiving grooming; that is, one animal can play two roles (i.e., groomer and groomee) simultaneously. Although this feature of chimpanzees is notable from the viewpoint of the evolution of human sociality, information on our other closest living relative, the bonobo (Pan paniscus), is still lacking. In this study, I describe grooming interactions of bonobos at Wamba in the Luo Scientific Reserve, Democratic Republic of the Congo (DR Congo), with a particular focus on the formation of grooming gatherings. Like chimpanzees, the bonobos also performed mutual grooming (two individuals grooming each other simultaneously) and polyadic grooming (three or more individuals). However, unlike chimpanzees, these sessions lasted for only a short time. Bonobos rarely groomed another while receiving grooming. Because social grooming occurred not only in trees but also in open spaces, including treefall gaps, the conditions did not necessarily limit the opportunity to make multiple chains of grooming. However, bonobos also engaged in social grooming in different ways from chimpanzees; That is, many individuals were involved simultaneously at a site, in which they separated for dyadic grooming. Some cases clearly showed that bonobos preferred a third party not to join while grooming in a dyad, suggesting that bonobos have a preference for grooming in dyads and that immature individuals formed the preference that was shared among adults while growing up. Most members of the study group ranged together during the majority of the study period. Although bonobos show a fission–fusion grouping pattern, when group members frequently encounter one another on a daily basis, they may not be motivated to form multiple grooming chains at this site, as do 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.     

Evidence for the consumption of arboreal,diurnal primates by bonobos (Pan paniscus)

We present evidence for the consumption of a diurnal, arboreal, group living primate by bonobos. The digit of an immature black mangabey (Lophocebus aterrimus) was found in the fresh feces of a bonobo (Pan paniscus) at the Lui Kotale study site, Democratic Republic of Congo. In close proximity to the fecal sample containing the remains of the digit, we also found a large part of the pelt of a black mangabey. Evidence suggests that the Lui Kotale bonobos consume more meat than other bonobo populations and have greater variation in the mammalian species exploited than previously thought [Hohmann & Fruth, Folia primatologica 79:103–110]. The current finding supports Stanford's argument [Current Anthropology 39:399–420] that some differences in the diet and behavior between chimpanzees (P. troglodytes) and bonobos are an artefact of the limited number of bonobo study populations. If bonobos did obtain the monkey by active hunting, this would challenge current evolutionary models relating the intra‐specific aggression and violence seen in chimpanzees and humans to hunting and meat consumption [Wrangham, Yearbook of Physical Anthropology 42:1–30]. Am. J. Primatol. 71:171–174, 2009. © 2008 Wiley‐Liss, Inc.     

Factors underlying party size differences between chimpanzees and bonobos: a review and hypotheses for future study

Differences in party size and cohesiveness among females have been primary topics in socio-ecological comparisons of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). This paper aims to review previous studies that attempted to explain these differences and propose some hypotheses to be tested in future studies. Comparisons of recent data show that relative party size (expressed as a percentage of total group size) is significantly larger for bonobos than chimpanzees. Although the prolonged estrus of females, close association between mother and adult sons, female social relationships including unique homosexual behavior, and high female social status might be related to the increased party size and female cohesiveness of bonobos, these social and behavioral factors alone do not appear to explain the differences between the two species. Differences in ecological factors, including fruit-patch size, density of terrestrial herbs, and the availability of scattered foods that animals forage as they travel between large fruit patches could also contribute to the differences between chimpanzees and bonobos. However, these factors cannot fully account for the increased party size and female cohesiveness of bonobos. The higher female cohesiveness in bonobos may be explained by socio-ecological systems that reduce the cost in feeding efficiency incurred by attending mixed-sex parties. These systems may include female initiatives for party ranging movements as well as the factors mentioned above. Because of their geographical isolation, the two species probably evolved different social systems. Chimpanzees, whose habitats became very dry during some periods in the Pleistocene, likely evolved more flexible fission–fusion social systems to cope with seasonal and annual variation in food availability. On the other hand, bonobos had a large refugia forest in the middle of their range even during the driest periods in the Pleistocene. Therefore bonobos, whose habitats had more abundant food and smaller variation in food availability, probably evolved systems that help females stay in mixed parties without incurring large costs from contest and scramble competition.     

Vertebrate DNA in Fecal Samples from Bonobos and Gorillas: Evidence for Meat Consumption or Artefact?

Background

Deciphering the behavioral repertoire of great apes is a challenge for several reasons. First, due to their elusive behavior in dense forest environments, great ape populations are often difficult to observe. Second, members of the genus Pan are known to display a great variety in their behavioral repertoire; thus, observations from one population are not necessarily representative for other populations. For example, bonobos (Pan paniscus) are generally believed to consume almost no vertebrate prey. However, recent observations show that at least some bonobo populations may consume vertebrate prey more commonly than previously believed. We investigated the extent of their meat consumption using PCR amplification of vertebrate mitochondrial DNA (mtDNA) segments from DNA extracted from bonobo feces. As a control we also attempted PCR amplifications from gorilla feces, a species assumed to be strictly herbivorous.

Principal Findings

We found evidence for consumption of a variety of mammalian species in about 16% of the samples investigated. Moreover, 40% of the positive DNA amplifications originated from arboreal monkeys. However, we also found duiker and monkey mtDNA in the gorilla feces, albeit in somewhat lower percentages. Notably, the DNA sequences isolated from the two ape species fit best to the species living in the respective regions. This result suggests that the sequences are of regional origin and do not represent laboratory contaminants.

Conclusions

Our results allow at least three possible and mutually not exclusive conclusions. First, all results may represent contamination of the feces by vertebrate DNA from the local environment. Thus, studies investigating a species'' diet from feces DNA may be unreliable due to the low copy number of DNA originating from diet items. Second, there is some inherent difference between the bonobo and gorilla feces, with only the later ones being contaminated. Third, similar to bonobos, for which the consumption of monkeys has only recently been documented, the gorilla population investigated (for which very little observational data are as yet available) may occasionally consume small vertebrates. Although the last explanation is speculative, it should not be discarded a-priori given that observational studies continue to unravel new behaviors in great ape species.     

Feeding ecology of bonobos living in forest‐savannah mosaics: Diet seasonal variation and importance of fallback foods

Primates along with many other animal taxa are forced to cope with large shifts in basic ecological conditions because of rapid anthropogenically induced changes of their habitats. One of the coping strategies for primates is to adjust their diet to these changes, and several studies have demonstrated the importance of fallback resources for this. Bonobos, like chimpanzees, might be particularly vulnerable to habitat fragmentation because of their high dependence on fruit availability. Little is known, however, about bonobo feeding ecology in fragmented habitats and their use of fallback resources. In this study, we investigate diet seasonal variation and the exploitation of preferred and fallback foods in a bonobo population living in forest‐savannah mosaics. Results show that bonobos have adapted to this fragmented habitat by feeding on only a few fruit species, including an important number of non‐tree species (liana, herb and savannah shrub), in comparison to populations living in dense forests. These non‐tree plants have been defined as fallback and non‐preferred foods, which are most probably consumed to maintain high frugivory. Interestingly, we identified that preferred foods are all typical of mature forests while fallback resources are mainly found in forest edges or disturbed areas. This finding indicates that bonobos prefer to use mature forests when feeding, as they do for nesting, but extend their range use to forest areas in close proximity to humans when the availability of preferred fruits is low. Finally, we show that bonobo diet relies heavily on two abundant fallback fruits: Musanga cecropioides and Marantochloa leucantha. Other studies have demonstrated that the selection of abundant fallback resources enables primates to subsist at high densities and to maintain cohesive groups, as observed at this study site. Our findings suggest that bonobos living in forest‐savannah mosaics can be considered as staple fallback food consumers. Am. J. Primatol. 77:948–962, 2015. © 2015 Wiley Periodicals, Inc.

     

Is Diet Flexibility an Adaptive Life Trait for Relictual and Peri-Urban Populations of the Endangered Primate Macaca sylvanus?

Habitat loss, fragmentation and urban expansion may drive some species to marginal habitats while others succeed in exploiting urban areas. Species that show dietary flexibility are more able to take advantage of human activities to supplement their diet with anthropogenically abundant and accessible resources. The Barbary macaque (Macaca sylvanus) is an endangered species due to the loss of its habitat, and human pressure. The population of Gouraya National Park (Algeria) lives in a relictual habitat that constitutes about 0.6% of the species range. In addition, this population is a unique case where urban expansion favours contact zones between Barbary macaque habitats and a big city (Bejaia). We quantified the dietary composition of Gouraya macaques over an annual cycle with the objective to understand how diet flexibility of this species may help it adapt to a relictual habitat or cope with urban expansion. We recorded the phenology of plant species every month. This study shows that Gouraya macaques, compared to those living in other forest types of the distribution area, are under lower seasonal constraints. They consume a greater amount of fruit and seeds that are available throughout much of the year, and a lesser amount of costly to find and extract subterranean foods. Therefore the Gouraya relictual habitat appears as a favourable environment compared to other major habitats of that species. This study also shows that colonizing peri-urban zones increases the availability and species richness of diet resources for Barbary macaques as they consume more human foods and exotic plants than in farther sites. Adult males eat more human foods than adult females and immatures do. The exploitation of high-energy anthropogenic food could favour macaque population growth and expansion towards the city center associated with human/macaque conflicts. We recommend applying management actions to restore macaques back to their natural habitat.     

Theft in an ultimatum game: chimpanzees and bonobos are insensitive to unfairness

Humans, but not chimpanzees, punish unfair offers in ultimatum games, suggesting that fairness concerns evolved sometime after the split between the lineages that gave rise to Homo and Pan. However, nothing is known about fairness concerns in the other Pan species, bonobos. Furthermore, apes do not typically offer food to others, but they do react against theft. We presented a novel game, the ultimatum theft game, to both of our closest living relatives. Bonobos and chimpanzee ‘proposers’ consistently stole food from the responders'' portions, but the responders did not reject any non-zero offer. These results support the interpretation that the human sense of fairness is a derived trait.     

Tooth Chipping as a Tool to Reconstruct Diets of Great Apes (Pongo, Gorilla, Pan)

Most methods of dietary reconstruction are limited in their applicability to either extant or extinct taxa. We apply and discuss a method in which dietary information can be reconstructed from chips in the tooth enamel of both living and fossil primates. Such chips can be used to indicate the presence of large hard foods in the diet, and also to provide an estimate of the bite force that was used when the chip was created. Furthermore, the equations derived from this method allow an estimate of maximum bite force to be obtained from a simple measurement of tooth size. We use this method to investigate dietary differences in nonhuman great apes (Pongo, Gorilla, Pan). The high frequency of chips on teeth of Pongo indicate that they frequently use high forces to process hard foods such as seeds and nuts. Gorilla can generate even higher bite forces, but their low incidence of tooth chips suggests that they do so when consuming soft but tough foods. Tooth chips provide a lasting dietary signal that is not easily masked or erased, making them particularly useful for the study of rarely eaten items such as some fallback foods.     

Plant foods consumed by Pan: Exploring the variation of nutritional ecology across Africa

It has been shown that differences in resource density and nutrient supply affect variation in ranging patterns, habitat use, and sociality. Among nonhuman primates, chimpanzees (Pan troglodytes) and bonobos (P. paniscus) have often been used as models for the link between social system and habitat ecology. Field reports suggest that resource density is higher in habitats occupied by bonobos (compared to chimpanzee habitats), and in the West (compared to the East) of the range of chimpanzees. In this study we compared diet quality at the level of species and populations using information from nutritional analyses of fruit and leaves consumed by chimpanzees (three) and bonobos (one population). Quality of plant foods was assessed on the basis of a) the concentration of macronutrients, fiber, and anti‐feedants, and b) associations of different nutrient components. Overall plant samples collected at each site differed in terms of macronutrient content. However, nutritious quality and gross energy content of food samples were similar suggesting that dietary quality reflects selectivity rather than habitat ecology. The quality of plant foods consumed by bonobos was within the range of chimpanzees and the quality of plant foods consumed by western chimpanzees was not higher than that of eastern chimpanzees. While the results showed significant variation across forests inhabited by Pan, they did not match with geographical patterns between and within Pan species as proposed in previous studies. This suggests that the nutritional quality of the habitat is not always a reliable predictor of the quality of the diet. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

Comparing infant and juvenile behavior in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes): a preliminary study

The dichotomy between the two Pan species, the bonobo (Pan paniscus) and chimpanzee (Pan troglodytes) has been strongly emphasized until very recently. Given that most studies were primarily based on adult individuals, we shifted the “continuity versus discontinuity” discussion to the infant and juvenile stage. Our aim was to test quantitatively, some conflicting statements made in literature considering species differences between immature bonobos and chimpanzees. On one hand it is suggested that infant bonobos show retardation in motor and social development when compared with chimpanzees. Additionally it is expected that the weaning process is more traumatic to chimpanzee than bonobo infants. But on the other hand the development of behaviors is expected to be very similar in both species. We observed eight mother–infant pairs of each species in several European zoos. Our preliminary research partially confirms that immature chimpanzees seem spatially more independent, spending more time at a larger distance from their mother than immature bonobos. However, the other data do not seem to support the hypothesis that bonobo infants show retardation of motor or social development. The development of solitary play, environmental exploration, social play, non-copulatory mounts and aggressive interactions do not differ between the species. Bonobo infants in general even groom other group members more than chimpanzee infants. We also found that older bonobo infants have more nipple contact than same aged chimpanzees and that the weaning process seems to end later for bonobos than for immature chimpanzee. Additionally, although immature bonobos show in general more signs of distress, our data suggest that the weaning period itself is more traumatic for chimpanzees.     

Bonobos have a more human-like second-to-fourth finger length ratio (2D:4D) than chimpanzees: a hypothesized indication of lower prenatal androgens

The ratio of the second-to-fourth finger lengths (2D:4D) has been proposed as an indicator of prenatal sex differentiation. However, 2D:4D has not been studied in the closest living human relatives, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus). We report the results from 79 chimpanzees and 39 bonobos of both sexes, including infants, juveniles, and adults. We observed the expected sex difference in 2D:4D, and substantially higher, more human-like, 2D:4D in bonobos than chimpanzees. Previous research indicates that sex differences in 2D:4D result from differences in prenatal sex hormone levels. We hypothesize that the species difference in 2D:4D between bonobos and chimpanzees suggests a possible role for early exposure to sex hormones in the development of behavioral differences between the two species.     

Behavioral laterality in captive bonobos (Pan paniscus): Replication and extension

We report observational data on behavioral laterality in 10 captive bonobos (Pan paniscus)at the San Diego Zoo. The unimanual measures include carrying, leading limb in locomotion, self-touching, face-touching, reaching, and gestures. We also recorded bimanual feeding in these subjects. A significant population level left-hand bias exists for carrying. Right-hand biases occur for leading limb in locomotion and gestures. During bimanual feeding, the bonobos hold food items with the left hand while feeding with the right hand. Overall, bonobos exhibit behavioral asymmetries that are similar to previous findings in other pongid ape species. The asymmetries in gestures and bimanual feeding represent novel findings with theoretical implications for the origins of tool use and language.     

On the Diversity of Malaria Parasites in African Apes and the Origin of Plasmodium falciparum from Bonobos

The origin of Plasmodium falciparum, the etiological agent of the most dangerous forms of human malaria, remains controversial. Although investigations of homologous parasites in African Apes are crucial to resolve this issue, studies have been restricted to a chimpanzee parasite related to P. falciparum, P. reichenowi, for which a single isolate was available until very recently. Using PCR amplification, we detected Plasmodium parasites in blood samples from 18 of 91 individuals of the genus Pan, including six chimpanzees (three Pan troglodytes troglodytes, three Pan t. schweinfurthii) and twelve bonobos (Pan paniscus). We obtained sequences of the parasites'' mitochondrial genomes and/or from two nuclear genes from 14 samples. In addition to P. reichenowi, three other hitherto unknown lineages were found in the chimpanzees. One is related to P. vivax and two to P. falciparum that are likely to belong to distinct species. In the bonobos we found P. falciparum parasites whose mitochondrial genomes indicated that they were distinct from those present in humans, and another parasite lineage related to P. malariae. Phylogenetic analyses based on this diverse set of Plasmodium parasites in African Apes shed new light on the evolutionary history of P. falciparum. The data suggested that P. falciparum did not originate from P. reichenowi of chimpanzees (Pan troglodytes), but rather evolved in bonobos (Pan paniscus), from which it subsequently colonized humans by a host-switch. Finally, our data and that of others indicated that chimpanzees and bonobos maintain malaria parasites, to which humans are susceptible, a factor of some relevance to the renewed efforts to eradicate malaria.     

Food-Associated Calling in Gorillas (Gorilla g. gorilla) in the Wild

Many nonhuman primates produce food-associated vocalizations upon encountering or ingesting particular food. Concerning the great apes, only food-associated vocalizations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) have been studied in detail, providing evidence that these vocalizations can be produced flexibly in relation to a variety of factors, such as the quantity and quality of food and/or the type of audience. Only anecdotal evidence exists of eastern (Gorilla beringei) and western gorillas (Gorilla gorilla) producing food-associated vocalizations, termed singing or humming. To enable a better understanding of the context in which these calls are produced, we investigated and compared the vocal behavior of two free-ranging groups of western lowland gorillas (Gorilla g. gorilla) at Mondika, Republic of Congo. Our results show that (a) food-associated call production occurs only during feeding and not in other contexts; (b) calling is not uniformly distributed across age and sex classes; (c) calls are only produced during feeding on specific foods; and (d) normally just one individual gives calls during group feeding sessions, however, certain food types elicit simultaneous calling of two or more individuals. Our findings provide new insight into the vocal abilities of gorillas but also carry larger implications for questions concerning vocal variability among the great apes. Food-associated calls of nonhuman primates have been shown to be flexible in terms of when they are used and who they are directed at, making them interesting vocalizations from the viewpoint of language evolution. Food-associated vocalizations in great apes can offer new opportunities to investigate the phylogenetic development of vocal communication within the primate lineage and can possibly contribute novel insights into the origins of human language.     

Bonobos extract meaning from call sequences

Studies on language-trained bonobos have revealed their remarkable abilities in representational and communication tasks. Surprisingly, however, corresponding research into their natural communication has largely been neglected. We address this issue with a first playback study on the natural vocal behaviour of bonobos. Bonobos produce five acoustically distinct call types when finding food, which they regularly mix together into longer call sequences. We found that individual call types were relatively poor indicators of food quality, while context specificity was much greater at the call sequence level. We therefore investigated whether receivers could extract meaning about the quality of food encountered by the caller by integrating across different call sequences. We first trained four captive individuals to find two types of foods, kiwi (preferred) and apples (less preferred) at two different locations. We then conducted naturalistic playback experiments during which we broadcasted sequences of four calls, originally produced by a familiar individual responding to either kiwi or apples. All sequences contained the same number of calls but varied in the composition of call types. Following playbacks, we found that subjects devoted significantly more search effort to the field indicated by the call sequence. Rather than attending to individual calls, bonobos attended to the entire sequences to make inferences about the food encountered by a caller. These results provide the first empirical evidence that bonobos are able to extract information about external events by attending to vocal sequences of other individuals and highlight the importance of call combinations in their natural communication system.     

Multi-Modal Use of a Socially Directed Call in Bonobos

‘Contest hoots’ are acoustically complex vocalisations produced by adult and subadult male bonobos (Pan paniscus). These calls are often directed at specific individuals and regularly combined with gestures and other body signals. The aim of our study was to describe the multi-modal use of this call type and to clarify its communicative and social function. To this end, we observed two large groups of bonobos, which generated a sample of 585 communicative interactions initiated by 10 different males. We found that contest hooting, with or without other associated signals, was produced to challenge and provoke a social reaction in the targeted individual, usually agonistic chase. Interestingly, ‘contest hoots’ were sometimes also used during friendly play. In both contexts, males were highly selective in whom they targeted by preferentially choosing individuals of equal or higher social rank, suggesting that the calls functioned to assert social status. Multi-modal sequences were not more successful in eliciting reactions than contest hoots given alone, but we found a significant difference in the choice of associated gestures between playful and agonistic contexts. During friendly play, contest hoots were significantly more often combined with soft than rough gestures compared to agonistic challenges, while the calls'' acoustic structure remained the same. We conclude that contest hoots indicate the signaller''s intention to interact socially with important group members, while the gestures provide additional cues concerning the nature of the desired interaction.