Chimpanzee insectivory in the northern half of Uganda’s Rift Valley: do Bulindi chimpanzees conform to a regional pattern?

Insects are a nutritious food source for many primates. In chimpanzees, insectivory is most prevalent among communities that manufacture tools to harvest social insects, particularly ants and termites. In contrast to other long-term study sites, chimpanzees (Pan troglodytes schweinfurthii) in Budongo Forest and Kibale National Park, Uganda, rarely eat insects and have small foraging tool kits, supporting speculation that infrequent insectivory—technically aided or otherwise—characterises chimpanzees in this part of Uganda’s Rift Valley. To expand the dataset for this region, insect foraging was investigated at Bulindi (25 km from Budongo) over 19 months during two studies in 2007–2008 and 2012–2013. Systematic faecal analysis demonstrated that insectivory is a habitual foraging activity at this site. Overall levels of insect consumption varied considerably across months but were not predicted by monthly changes in rainfall or fruit intake. Unlike their Budongo and Kibale counterparts, Bulindi chimpanzees often consume ants (principally weaver ants, Oecophylla longinoda) and use sticks to dig out stingless bee (Meliponini) ground nests. In other respects, however, insectivory at Bulindi conforms to the pattern observed elsewhere in this region: they do not manufacture ‘fishing’ or ‘dipping’ tools to harvest termites and aggressive or hard-to-access ants (e.g., army ants, Dorylus spp.), despite availability of suitable prey. The Bulindi data lend support to the supposition that chimpanzees in this part of the Rift Valley rarely exploit termites and Dorylus ants, apparently lacking the ‘cultural knowledge’ that would enable them to do so most efficiently (i.e., tool use). The study’s findings contribute to current debates about the relative influence of genetics, environment and culture in shaping regional and local variability in Pan foraging ecology.     

Tool Use by Chimpanzees at Ngogo,Kibale National Park,Uganda

Chimpanzees make and use a wide variety of tools in the wild. The size and composition of their toolkits vary considerably among populations and at least to some extent within them. Chimpanzees at several well documented sites mostly use tools in extractive foraging, and extractive tool use can substantially increase their foraging efficiency. They also use tools for hygiene and for several other purposes, including attracting the attention of conspecifics, as in leaf-clipping. Some of the interpopulation variation in toolkits results from ecological variation, but differences in the efficiency of social transmission, perhaps related to differences in social tolerance, presumably also contribute. I describe tool use by chimpanzees in an unusually large community at Ngogo, in Kibale National Park, Uganda. Researchers have described some tool use for the community previously, but this is the most extensive report and is based on observations over 11 yr. The Ngogo chimpanzees have a small toolkit and use tools rarely except in leaf-clipping displays and to clean body surfaces; notably, males often use leaf napkins to wipe their penes after copulation. Extractive tool use is rare and is limited mostly to leaf-sponging and, less often, honey-fishing. Social tolerance is not low at Ngogo, but use of tools for extractive foraging, in ways documented at other field sites, may have little potential to increase foraging efficiency. Future research will undoubtedly show more tool use by females, which were underrepresented in my observations, but will probably not document much increase in the toolkit or in the use of extractive tools.     

Chimpanzees in Bwindi-Impenetrable National Park, Uganda, use different tools to obtain different types of honey

Evidence of tool use for foraging for honey by chimpanzees in Bwindi-Impenetrable National Park, Uganda, is reported. These are the first records of tool use by chimpanzees in this region of the Albertine Rift. Tools of two types were found at sites of bee activity. Chimpanzees apparently use small stick tools to forage for the honey of a stingless bee [Meliponula bocandei (Trigonidae)] that nests in tree cavities and also in subterranean holes. They use significantly larger, thicker tools to assist in foraging for honey of African honeybees (Apis mellifera).     

Energetic costs of territorial boundary patrols by wild chimpanzees

Chimpanzees are well known for their territorial behavior. Males who belong to the same community routinely patrol their territories, occasionally making deep incursions into those of their neighbors. Male chimpanzees may obtain several fitness benefits by participating in territorial boundary patrols, but patrolling is also likely to involve fitness costs. Patrollers risk injury or even death, and patrols may be energetically costly and may involve opportunity costs. Although territorial patrols have been reported at all long‐term chimpanzee study sites, quantitative data on their energetic costs have not previously been available. I evaluated the energy costs of patrolling for male chimpanzees at Ngogo, Kibale National Park, Uganda during 14 months of observation. In 29 patrols and matched control periods, I recorded the distances covered and time spent traveling and feeding by chimpanzees. I found that male chimpanzees covered longer distances, spent more time traveling, and spent less time feeding during patrols than during control periods. These results support the hypothesis that chimpanzees incur energetic costs while patrolling and suggest that ecological factors may constrain the ability of chimpanzees to patrol. Am. J. Primatol. 72:93–103, 2010. © 2009 Wiley‐Liss, Inc.     

Infanticide and cannibalism by male chimpanzees at Ngogo, Kibale National Park, Uganda

Researchers have documented infanticide by adult males in four wild chimpanzee populations. Males in three of these have killed infants from outside of their own communities, but most infanticides, including one from Kanyawara, in Kibale National Park, Uganda, took place within communities. Here we report two new cases of infanticide by male chimpanzees at a second Kibale site, Ngogo, where the recently habituated chimpanzee community is the largest yet known. Both infanticides happended during boundary patrols, which occur at a high frequency there. Patrolling males attacked solitary females who were unable to defend their infants successfully. The victims were almost certainly not members of the Ngogo community. Males cannibalized both infants and completely consumed their carcasses. These observations show that infanticide by males is widespread in the Kibale population and that between-community infanticide also happens there. We discuss our observations in the context of the sexual selection hypothesis and other proposed explanations for infanticide by male chimpanzees. The observations support the arguments that infanticide has been an important selective force in chimpanzee social evolution and that females with dependent infants can be at great risk near range boundaries, but why male chimpanzees kill infants is still uncertain.     

Range use of the forest chimpanzees of Kibale: Implications for the understanding of chimpanzee social organization

We contrast the range use patterns of male and female chimpanzees (Pan troglodytes) based on repeated sightings over three years of 19 individuals in the Kanyawara community of Kibale Forest Reserve, Uganda. Depending on how home range size was calculated, male chimpanzees used an area that was 1.5 to 2 times greater than that of females. There was no difference between the sexes in whether their home ranges were used in a clumped or uniform fashion. However, males were more likely to be seen in boundary areas than females. These results are discussed in light of previously proposed models of chimpanzee social organization. It is concluded that the scenario in which females have smaller core areas within the defended home range of the males is most strongly supported by the range use patterns observed in Kibale chimpanzees. © 1993 Wiley-Liss, Inc.     

New cases of inter-community infanticide by male chimpanzees at Ngogo,Kibale National Park,Uganda

Infanticide by males has been recorded in four chimpanzee populations, including that in Kibale National Park, Uganda. Some infanticidal attacks occur during inter-community aggression. The sexual selection hypothesis does not easily explain these attacks because they may not directly increase male mating opportunities. However, females in the attackers’ community may benefit by expanding their foraging ranges and thereby improving their reproductive success; thus infanticide may increase male reproductive success indirectly. We report two new cases of infanticide by male chimpanzees at Ngogo, Kibale National Park. Like two previous cases, these occurred during a boundary patrol and were almost certainly between-community infanticides. The patrolling males attacked despite the proximity of males from the victims’ presumed community. This probably explains why, unlike the earlier cases, they did not completely cannibalize their victims. Such attacks seem to be relatively common at Ngogo and infanticide may be an important source of infant mortality in neighboring communities. Our observations cannot resolve questions about the sexual selection hypothesis. However, they are consistent with the range expansion hypothesis: the infanticides occurred during a period of frequent encounters between communities associated with a mast fruiting event, and Ngogo community members greatly increased their use of areas near the attack site during another mast fruiting event one year later. Our observations contribute to growing evidence that lethal intergroup aggression is a common characteristic of wild chimpanzee populations.     

The Foraging Costs of Mating Effort in Male Chimpanzees (Pan troglodytes schweinfurthii)

Costs of mating effort can affect the reproductive strategies and lifetime fitness of male primates, but interspecific and interindividual variation in the magnitude and distribution of costs is poorly understood. Male costs have primarily been recognized in seasonally breeding species that experience concentrated periods of mating competition. Here, we examine foraging costs associated with male mating effort in chimpanzees (Pan troglodytes schweinfurthii), a polygynandrous species, in which mating opportunities occur intermittently throughout the year. To quantify male feeding, aggression, and mating, we conducted focal follows on 12 males in a wild community (Kanyawara, Kibale National Park, Uganda) for 11 mo. Males fed less on days when high-value mating opportunities (estrous parous females) were available than on days without any mating opportunities. Reductions in feeding time were related to increased rates of aggression and copulation, indicating that the proximate cause of changes in male foraging was mating effort. Surprisingly, however, there was no relationship between dominance rank and the extent to which feeding time was reduced. High costs of mating effort may reduce the degree of reproductive skew and limit the use of possessive tactics in chimpanzees. We suggest that male bonding in chimpanzees may be favored not only for its benefits but because intragroup competition is so costly. Our results complement the available data on mammals, and primates in particular, by showing that mating effort can have measurable foraging costs even in species, in which breeding is aseasonal and only moderately skewed.     

Primate abundance along five transect lines at Ngogo, Kibale National Park, Uganda

Using the line transect methods, I studied the primate density at Ngogo, Kibale National Park, Uganda for 18 months. Comparisons with other studies show that the population of red colobus monkeys (Procolobus rufomitratus) and blue monkeys (Cercopithecus mitis) is declining, whereas the populations of black-and-white colobus (Colobus guereza), red-tailed monkeys (Cercopithecus ascanius), grey-cheeked mangabeys (Lophocebus albigena), baboons (Papio anubis), and chimpanzees (Pan troglodytes) remain constant or slightly increase. In this paper, I compare data on density from this study to data from previous and recent censuses at Ngogo and with data from other sites in the Kibale forest to examine the stability of primate populations. Furthermore, I test the hypothesis that the changes in red colobus and blue monkey density are due to changes in the forest structure and abundance of their most selected feeding trees, and show that changes in forest composition cannot account for changes in their red colobus abundance, but that hunting by chimpanzees provides a reasonable explanation.     

Sex Differences in Object Manipulation in Wild Immature Chimpanzees (Pan troglodytes schweinfurthii) and Bonobos (Pan paniscus): Preparation for Tool Use?

Sex differences in immatures predict behavioural differences in adulthood in many mammal species. Because most studies have focused on sex differences in social interactions, little is known about possible sex differences in ‘preparation’ for adult life with regards to tool use skills. We investigated sex and age differences in object manipulation in immature apes. Chimpanzees use a variety of tools across numerous contexts, whereas bonobos use few tools and none in foraging. In both species, a female bias in adult tool use has been reported. We studied object manipulation in immature chimpanzees at Kalinzu (Uganda) and bonobos at Wamba (Democratic Republic of Congo). We tested predictions of the ‘preparation for tool use’ hypothesis. We confirmed that chimpanzees showed higher rates and more diverse types of object manipulation than bonobos. Against expectation, male chimpanzees showed higher object manipulation rates than females, whereas in bonobos no sex difference was found. However, object manipulation by male chimpanzees was play-dominated, whereas manipulation types of female chimpanzees were more diverse (e.g., bite, break, carry). Manipulation by young immatures of both species was similarly dominated by play, but only in chimpanzees did it become more diverse with age. Moreover, in chimpanzees, object types became more tool-like (i.e., sticks) with age, further suggesting preparation for tool use in adulthood. The male bias in object manipulation in immature chimpanzees, along with the late onset of tool-like object manipulation, indicates that not all (early) object manipulation (i.e., object play) in immatures prepares for subsistence tool use. Instead, given the similarity with gender differences in human children, object play may also function in motor skill practice for male-specific behaviours (e.g., dominance displays). In conclusion, even though immature behaviours almost certainly reflect preparation for adult roles, more detailed future work is needed to disentangle possible functions of object manipulation during development.     

Tool use, aye-ayes, and sensorimotor intelligence

Humans, chimpanzees, capuchins and aye-ayes all display an unusually high degree of encephalization and diverse omnivorous extractive foraging. It has been suggested that the high degree of encephalization in aye-ayes may be the result of their diverse, omnivorous extractive foraging behaviors. In combination with certain forms of tool use, omnivorous extractive foraging has been hypothesized to be linked to higher levels of sensorimotor intelligence (stages 5 or 6). Although free-ranging aye-ayes have not been observed to use tools directly in the context of their extractive foraging activities, they have recently been reported to use lianas as tools in a manner that independently suggests that they may possess stage 5 or 6 sensorimotor intelligence. Although other primate species which display diverse, omnivorous extractive foraging have been tested for sensorimotor intelligence, aye-ayes have not. We report a test of captive aye-ayes' comprehension of tool use in a situation designed to simulate natural conditions. The results support the view that aye-ayes do not achieve stage 6 comprehension of tool use, but rather may use trial-and-error learning to develop tool-use behaviors. Other theories for aye-aye encephalization are considered.     

Floristic heterogeneity at Ngogo,Kibale National Park,Uganda and possible implications for habitat use by chimpanzees (Pan troglodytes)

Tropical forest tree communities exhibit heterogeneity at multiple spatial scales, with important implications for animals relying on these resources. However, different organisms may perceive heterogeneity in the floristic community in very different ways. Here, we characterize the overall extent of heterogeneity in the floristic community at Ngogo, in Kibale National Park, Uganda. Also, using information from studies on the diet of chimpanzees (Pan troglodytes) inhabiting Ngogo, we quantify the extent to which the habitat is likely perceived as heterogeneous by this species. The forest as a whole is slightly more diverse than comparable sites in the Congo Basin, but this diversity is driven by a relatively high proportion of rare species represented by few individuals. From the perspective of chimpanzees, the forest is, unsurprisingly, even more heterogeneous. Species that provide fruit for chimpanzees during times of low overall fruit abundance and that display interindividual synchrony in fruiting were the most common chimpanzee resource in our sample, whereas species that provide fruit during times of low overall fruit abundance and that display asynchronous fruiting were the least common. We discuss the implications of the differences in density and distribution of various classes of resources for chimpanzee habitat use and foraging efficiency.     

Scavenging by chimpanzees at Ngogo and the relevance of chimpanzee scavenging to early hominin behavioral ecology

Chimpanzees regularly hunt a variety of prey species. However, they rarely scavenge, which distinguishes chimpanzee carnivory from that of some modern hunter-gatherers and, presumably, at least some Plio-Pleistocene hominins. I use observations made over an 11-year period to document all known opportunities for scavenging encountered by chimpanzees at Ngogo, Kibale National Park, Uganda, and describe all cases of scavenging. I also review data on scavenging from other chimpanzee research sites. Chimpanzees at Ngogo encountered scavenging opportunities only about once per 100 days and ate meat from scavenged carcasses only four times. Scavenging opportunities are also rare at other sites, even where leopards are present (Mahale, Ta?, Gombe), and scavenging of leopard kills is known only from Mahale. Feeding on prey that chimpanzees had hunted but then abandoned is the most common form of scavenging reported across study sites. For example, several individuals at Ngogo ate meat from a partially consumed red colobus carcass abandoned after a hunt the previous day. Such behavior probably was not common among Oldowan hominins. Ngogo data and those from other sites also show that chimpanzees sometimes eat meat from carcasses of prey that they did not see killed and that were not killed by chimpanzees, and that scavenging allows access to carcasses larger than those of any prey items. However, chimpanzees ignore relatively many opportunities to obtain meat from such carcasses. Scavenging may be rare because fresh carcasses are rare, because the risk of bacterial infections and zoonoses is high, and because chimpanzees may not recognize certain species as potential prey or certain size classes of prey species as food sources. Its minimal nutritional importance, along with the absence of technology to facilitate confrontational scavenging and rapid carcass processing, apparently distinguishes chimpanzee foraging strategies from those of at least some Oldowan hominins.     

Invention and modification of a new tool use behavior: ant-fishing in trees by a wild chimpanzee (Pan troglodytes verus) at Bossou, Guinea

Wild chimpanzees are known to have a different repertoire of tool use unique to each community. For example, "ant-dipping" is a tool use behavior known in several chimpanzee communities across Africa targeted at driver ants (Dorylus spp.) on the ground, whereas "ant-fishing," which is aimed at carpenter ants (Camponotus spp.) in trees, has primarily been observed among the chimpanzees of Mahale in Tanzania. Although the evidence for differences between field sites is accumulating, we have little knowledge on how these tool use behaviors appear at each site and on how these are modified over time. This study reports two"ant-fishing" sessions which occurred 2 years apart by a young male chimpanzee at Bossou, Guinea. Ant-fishing had never been observed before in this community over the past 27 years. During the first session, at the age of 5, he employed wands of similar length when ant-fishing in trees to those used for ant-dipping on the ground, which is a customary tool use behavior of this community. Two years later, at the age of 7, his tools for ant-fishing were shorter and more suitable for capturing carpenter ants. This observation is a rare example of innovation in the wild and does provide insights into problem-solving and learning processes in chimpanzees.     

Skeletal pathology in Pan troglodytes schweinfurthii in Kibale National Park, Uganda

The ecological pressures shaping chimpanzee anatomy and behavior are the subject of much discussion in primatology and paleoanthropology, yet empirical data on fundamental parameters including body size, morbidity, and mortality are rare for wild chimpanzees. Here, we present skeletal pathology and body size data for 20 (19 crania, 12 postcrania) chimpanzees (Pan troglodytes schweinfurthii) from Kibale National Park, Uganda. We compare these data with other East African populations, especially Gombe National Park. Estimated body size for Kibale chimpanzees was similar to other East African populations and significantly larger than Gombe chimpanzees. The high rates of trauma and other skeletal pathology evident in the Kibale chimpanzee skeletons were similar to those in the Gombe skeletal sample. Much of the major skeletal trauma in the Kibale skeletons was attributable to falls, although other pathologies were noted as well, including apparent injuries from snares, degenerative arthritis, and minor congenital abnormalities.     

Demographic influences on the behavior of chimpanzees

Recent research has revealed substantial diversity in the behavior of wild chimpanzees. Understanding the sources of this variation has become a central focus of investigation. While genetic, ecological, and cultural factors are often invoked to explain behavioral variation in chimpanzees, the demographic context is sometimes overlooked as a contributing factor. Observations of chimpanzees at Ngogo, Kibale National Park, Uganda, reveal that the size and structure of the unit group or community can both facilitate and constrain the manifestation of behavior. With approximately 150 individuals, the Ngogo community is much larger than others that have been studied in the wild. We have taken advantage of the unusual demographic structure of this community to document new and intriguing patterns of chimpanzee behavior with respect to hunting, territoriality, and male social relationships. Chimpanzees at Ngogo hunt often and with a considerable degree of success. In addition, male chimpanzees there frequently patrol the boundary of their territory and engage in repeated bouts of lethal intergroup aggression. By forming two distinct subgroups, male chimpanzees at Ngogo also develop social bonds above the level of dyadic pairs. While the sheer number of chimpanzees contributes to differences in hunting, patrolling, mating, and subgrouping at Ngogo, the demographic situation may also constrain behavioral interactions. At Ngogo, male chimpanzees who are closely related genetically through the maternal line do not appear to affiliate or cooperate with each other. Demographic constraints may be responsible for this finding. In this paper, I use these examples to illustrate how the demographic context affects the possible range of behavioral options open to individuals and ultimately contributes to the explanation of behavioral diversity in chimpanzees.     

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.     

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

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

Influence of Chimpanzee Predation on Associations Between Red Colobus and Red-tailed Monkeys at Ngogo,Kibale National Park,Uganda

Colobines often associate with cercopithecines at various African sites. Such polyspecific associations presumably have an antipredation function. At Ngogo, Kibale National Park, Uganda, red colobus (Procolobus rufomitratus) spend considerable time in association with red-tailed monkeys (Cercopithecus ascanius), and they are also heavily hunted by chimpanzees (Pan troglodytes). I conducted behavioral observations and playback experiments to test the hypothesis that red colobus and red-tailed monkeys obtain mutual protection and predator-related benefits by associating. Despite high chimpanzee hunting pressure on red colobus and much lower hunting pressure on red-tailed monkeys, red-tailed monkeys initiate, maintain, and terminate the associations. The results suggest that rather than providing red colobus with protection against chimpanzees, the associations occur mostly because they protect red-tailed monkeys against predation by eagles.     

Male affiliation, cooperation and kinship in wild chimpanzees

Long-term field research has revealed that male chimpanzees, Pan troglodytes, affiliate and cooperate in several contexts. Assuming close genetic relationship among males, affiliative and cooperative behaviour have been hypothesized to evolve through the indirect effects of kin selection. We tested the hypothesis that matrilineal genetic relatedness affects patterns of male social affiliation and cooperation in an unusually large community of chimpanzees at the Ngogo study site, Kibale National Park, Uganda. Field observations indicated that six behavioural measures of affiliation and cooperation among 23 adult males were significantly correlated with each other. Sequences of the first hypervariable portion of the mtDNA genome revealed that three pairs of males and one quintet shared mtDNA haplotypes. Matrix permutation tests using behavioural and genetic data showed that males that affiliated and cooperated with each other were not closely related through the maternal line. These findings add to a growing body of empirical evidence that suggest kinship plays an ancillary role in structuring patterns of wild chimpanzee behaviour within social groups. Copyright 2000 The Association for the Study of Animal Behaviour.