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.     

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.     

Hunting Behavior of Chimpanzees at Ngogo,Kibale National Park,Uganda

Chimpanzees (Pan troglodytes) prey on a variety of vertebrates, mostly on red colobus (Procolobus spp.) where the two species are sympatric. Variation across population occurs in hunting frequency and success, in whether hunting is cooperative, i.e., payoffs to individual hunters increase with group size, and in the extent to which hunters coordinate their actions in space and time, and in the impact of hunting on red colobus populations. Also, hunting frequency varies over time within populations, for reasons that are unclear. We present new data on hunting by chimpanzees at Ngogo, Kibale National Park, Uganda, and combine them with earlier data (Mitani and Watts, 1999, Am. J. Phys. Anthropol. 109: 439–454) to examine hunting frequency and success, seasonality, and cooperation. The Ngogo community is the largest and has the most males of any known community. Chimpanzees there mostly hunt red colobus and are much more successful and make many more kills per hunt than at other sites; they kill 6–12% of the red colobus population annually. The number of kills and the offtake of meat per hunt increase with the number of hunters, but per capita meat intake is independent of hunting party size; this suggests that cheating occurs in large parties. Some behavioral cooperation occurs. Hunting success and estimated meat intake vary greatly among males, partly due to dominance rank effects. The high overall success rate leads to relatively high average per capita meat intake despite the large number of consumers. The frequency of hunts and of hunting patrols varies positively with the availability of ripe fruit; this is the first quantitative demonstration of a relationship between hunting frequency and the availability of other food, and implies that the chimpanzees hunt most when they can easily meet energy needs from other sources. We provide the first quantitative support for the argument that variation in canopy structure influences decisions to hunt red colobus because hunts are easier where the canopy is broken.     

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.     

New Intercommunity Infanticides by the Chimpanzees of Ngogo,Kibale National Park,Uganda

Hostile intercommunity relations, including attacking and killing extra-community infants of both sexes have occurred at most wild chimpanzee sites. We describe three recent cases of intercommunity attacks on infants committed by members of the Ngogo chimpanzee community in Kibale National Park, Uganda. Two of the attacks resulted in confirmed infanticides while a third attack probably resulted in the infant's death. In common with previous accounts of chimpanzee infanticides, the attacks described here occurred during boundary patrols outside the Ngogo community's usual range, adult and adolescent males were the main participants, one infant was cannibalized after being killed, and the victims’ mothers did not accompany the attacking party back to the Ngogo range. However, the patrol parties during each infanticide were larger than before and included females from the Ngogo community. Our observations indirectly support both the range expansion and imbalance of power hypotheses, which address why and under which conditions chimpanzee intercommunity encounters lead to aggression. These cases of intercommunity infanticide add to the growing database of the phenomenon in wild chimpanzees.     

Lethal intergroup aggression by chimpanzees in Kibale National Park, Uganda

Chimpanzees (Pan troglodytes) have hostile intergroup relations throughout most or all of their geographic range. Hostilities include aggressive encounters between members of neighboring communities during foraging and during patrols in which members of one community search for neighbors near territory boundaries. Attacks on neighbors involve coalitions of adult males, and are sometimes fatal. Targets include members of all age/sex classes, but the risk of lethal intergroup coalitionary aggression is highest for adult males and infants, and lowest for sexually swollen females. The best-supported adaptive explanation for such behavior is that fission-fusion sociality allows opportunities for low-cost attacks that, when successful, enhance the food supply for members of the attackers' community, improve survivorship, and increase female fertility. We add to the database on intergroup coalitionary aggression in chimpanzees by describing three fatal attacks on adult males, plus a fourth attack on an adult male and an attack on a juvenile that were almost certainly fatal. Observers saw four of these attacks and inferred the fifth from forensic and behavioral evidence. The attackers were males in two habituated, unprovisioned communities (Ngogo and Kanyawara) in Kibale National Park, Uganda. We also summarize data on other intercommunity attacks at Ngogo. Our observations are consistent with the "imbalance of power" hypothesis [Manson & Wrangham, Current Anthropology 32:369-390, 1991] and support the argument that lethal coalitionary intergroup aggression by male chimpanzees is part of an evolved behavioral strategy.     

Tool use in insect foraging by the chimpanzees of Ngogo, Kibale National Park, Uganda

Chimpanzee tool use for resource acquisition has been reported at numerous research sites. The chimpanzees of the Kibale Forest, western Uganda, have not previously been observed to use tools in foraging for insects. Here I report the first observation of tool use by the chimpanzees of the Ngogo community of Kibale National Park, Uganda, in insect foraging. Three adult females, one adolescent male, and one juvenile male were observed making and using tools to probe into a fallen dead tree to collect insect and wood pieces. I discuss the importance of this observation, and the behavioral similarities with chimpanzees from other sites.     

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.     

Diet of chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda, 1. Diet composition and diversity

Chimpanzees (Pan troglodytes) are ecologically flexible omnivores with broad diets comprising many plant and animal foods, although they mostly eat fruit (including figs). Like other ecologically flexible nonhuman primates (e.g., baboons, Papio spp.) with broad diets, their diets vary across habitats. Much data on diets come from short studies that may not capture the range of variation, however, and data are scant on variation within habitats and populations. We present data on diet composition and diversity for chimpanzees at Ngogo, in Kibale National Park, Uganda, collected over a 15-year period, with a focus on the plant components of the diet. We compare Ngogo data to those on chimpanzees at the nearby Kibale site of Kanyawara, on other chimpanzee populations, and on some other frugivorous-omnivorous primates. Results support the argument that chimpanzees are ripe fruit specialists: Ngogo chimpanzees ate a broad, mostly fruit-based diet, feeding time devoted to fruit varied positively with fruit availability, and diet diversity varied inversely with fruit availability. Comparison of Ngogo and Kanyawara shows much similarity, but also pronounced within-population dietary variation. Chimpanzees fed much more on leaves, and much less on pith and stems, at Ngogo. Figs accounted for somewhat less feeding time at Ngogo, but those of Ficus mucuso were quantitatively the most important food. This species is essentially absent at Kanayawara; its abundance and high productivity at Ngogo, along with much higher abundance of several other important food species, help explain why chimpanzee community size and population density are over three times higher at Ngogo. High inter-annual variation at Ngogo highlights the value of long-term data for documenting the extent of ecological variation among chimpanzee populations and understanding how such variation might affect population biology and social dynamics.     

Diet of chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda, 2. Temporal variation and fallback foods

Highly frugivorous primates like chimpanzees (Pan trogolodytes) must contend with temporal variation in food abundance and quality by tracking fruit crops and relying more on alternative foods, some of them fallbacks, when fruit is scarce. We used behavioral data from 122 months between 1995 and 2009 plus 12 years of phenology records to investigate temporal dietary variation and use of fallback foods by chimpanzees at Ngogo, Kibale National Park, Uganda. Fruit, including figs, comprised most of the diet. Fruit and fig availability varied seasonally, but the exact timing of fruit production and the amount of fruit produced varied extensively from year to year, both overall and within and among species. Feeding time devoted to all major fruit and fig species was positively associated with availability, reinforcing the argument that chimpanzees are ripe fruit specialists. Feeding time devoted to figs-particularly Ficus mucuso (the top food)--varied inversely with the abundance of nonfig fruits and with foraging effort devoted to such fruit. However, figs contributed much of the diet for most of the year and are best seen as staples available most of the time and eaten in proportion to availability. Leaves also contributed much of the diet and served as fallbacks when nonfig fruits were scarce. In contrast to the nearby Kanywara study site in Kibale, pith and stems contributed little of the diet and were not fallbacks. Fruit seasons (periods of at least 2 months when nonfig fruits account for at least 40% of feeding time; Gilby & Wrangham., Behavioral Ecology and Sociobiology 61:1771-1779, 2007) were more common at Ngogo than Kanyawara, consistent with an earlier report that fruit availability varies less at Ngogo [Chapman et al., African Journal of Ecology 35:287-302, 1997]. F. mucuso is absent at Kanyawara; its high density at Ngogo, combined with lower variation in fruit availability, probably helps to explain why chimpanzee population density is much higher at Ngogo.     

Parasitological analyses of the male chimpanzees (Pan troglodytes schweinfurthii) at Ngogo, Kibale National Park, Uganda

Numerous intestinal parasites identified in populations of wild nonhuman primates can be pathogenic to humans. Furthermore, nonhuman primates are susceptible to a variety of human pathogens. Because of increasing human encroachment into previously nonimpacted forests, and the potential for disease transmission between human and nonhuman primate populations, further detailed investigations of primate ecological parasitology are warranted. For meaningful comparisons to be made, it is important for methods to be standardized across study sites. One aspect of methodological standardization is providing reliable estimates of parasite prevalence and knowing how many samples are needed to adequately estimate an individual's parasite prevalence. In this study the parasitic fauna of 37 adult, adolescent, and juvenile male chimpanzees from the Ngogo group, Kibale National Park, Uganda, were assessed from 121 fecal samples collected over a 3-month period. Twelve taxa of intestinal species (five helminth and seven protozoan) were recovered from the samples. The four most prevalent species were Troglodytella abrassarti (97.3%), Oesophagostomum sp. (81.1%), Strongyloides sp. (83.8%), and Entamoeba chattoni (70.3%). No one species was found in all samples from any one animal, and Troglodytella abrassarti, the most common intestinal organism, was found in all of the serial samples of only 69.4% of the chimpanzees. The cumulative species richness for individuals significantly increased for every sequential sample (up to three to four samples) taken per animal during this study. The results indicate that to accurately diagnose total intestinal infection and evaluate group prevalence, three to four sequential samples from each individual must be collected on nonconsecutive days. This conclusion applies only to short study periods in which possible seasonal effects are not taken into consideration. Validation of these results at different study sites in different regions with different climatic patterns is needed.     

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.     

Primate population dynamics over 32.9 years at Ngogo, Kibale National Park, Uganda

We present census data for eight primate species spanning 32.9 years along the same transect at Ngogo, Kibale National Park, Uganda, demonstrating major changes in the composition of the primate community. Correlated with an estimated decline of ～89% in the red colobus population was an increase in encounter rates with chimpanzee parties. Our data, along with the unusually high rates of predation by chimpanzees on red colobus at Ngogo and the fact that the chimpanzee community at Ngogo is the largest ever recorded, support the conclusion that the red colobus decline was caused primarily by chimpanzee predation. This seems to be the first documented case of predation by one nonhuman primate causing the population decline in another. We evaluated disease and interspecific competition as other possible causes of the red colobus decline, but judged them to be relatively insignificant compared with predation by chimpanzees. Notable changes in encounter rates with other primate species may have resulted from forest expansion. Those for mangabeys, redtails, and black and white colobus increased significantly. Encounter rates increased for l'Hoest's monkeys too, but the increased sightings may have been an artifact of increased habituation. Sightings of blue monkey and baboon groups declined. There was no significant change in encounter rates for all species combined. The Ngogo primate community seemed to be in a nonequilibrium state, changing from one dominated by two species, a folivore (red colobus) and a frugivorous omnivore (redtails), to one dominated by three species of frugivorous omnivores (redtails, mangabeys, and chimpanzees). This study demonstrates the importance of long-term monitoring in understanding population dynamics and the role of intrinsic variables in shaping the species composition of a community.     

A preliminary analysis of wound care and other-regarding behavior in wild chimpanzees at Ngogo,Kibale National Park,Uganda

Primates - Caring for others is a key feature of human behavior. Mothers, fathers, siblings, grandparents, and other group members provide care in the form of provisioning, protection, and first...     

Grooming Between Male Chimpanzees at Ngogo,Kibale National Park. I. Partner Number and Diversity and Grooming Reciprocity

Allogrooming serves many social functions in primates. Grooming can help individuals to service social relationships generally, sometimes reciprocally, and may be particularly important in the development and maintenance of alliances. However, time constraints limit the number of partners with whom one individual can groom enough to maintain cooperative relationships. As a result, the size of its grooming network may reach an asymptote as the size of its group increases, and it may distribute its grooming less equally among potential partners. Chimpanzees live in multimale, fission-fusion communities; males are philopatric, and commonly associate and groom with each other. Males form within-community alliances that influence dominance rank and access to mates, and allies groom with each other regularly; males also cooperate in aggression between communities. The chimpanzee community at Ngogo, in Kibale National Park, Uganda, is unusually large and has more males than any other known community. Field data show that adult Ngogo males groomed far more with other adult males than with females or with adolescent males, in contrast to a previous report (Ghiglieri, 1984). Adolescent males groomed adults much more than the reverse; males groomed and were groomed by females about equally. Individual males groomed mostly with a small number of other males. On average, males at Ngogo had only slightly more male grooming partners overall and had the same number of important partners as those of males in a much smaller community in the Mahale National Park, Tanzania, and they distributed their grooming less equitably. These results fit those expected if limits on available grooming time cause males to have a loyalty problem as the number of potential grooming and alliance partners increases. Despite differences in the extent and equitability of their grooming networks, males at both Ngogo and Mahale showed reciprocity in grooming. Grooming reciprocity has been demonstrated for captive chimpanzee males, but the Ngogo findings are the first demonstrations of reciprocity in wild communities.     

Intracommunity Coalitionary Killing of an Adult Male Chimpanzee at Ngogo,Kibale National Park,Uganda

Intercommunity coalitionary killing of adult and adolescent males has been documented in two chimpanzee communities in the wild, and it was strongly suspected in a third. It may increase survivorship for the attackers, their mates, and their offspring by reducing the combined strength of hostile neighbors and/or by increasing territory size and food availability, and it may help the attackers to attract mates. Lethal coalitionary attacks by males on other male members of their own communities would not provide these benefits and are not expected, given the importance of cooperation among male community members in contests for dominance rank and in both defense and offense against neighboring males. Nevertheless, intracommunity coalitionary killings associated with struggles for alpha rank occur in the wild and in captivity, and observers have seen serious gang attacks on maturing adolescent and young adult males at Mahale and Budongo: the victim in the Budongo case was killed (Fawcett and Muhumuza, 2000). I describe a lethal attack on a young adult male by a large coalition of males from his community at Ngogo, Kibale National Park, Uganda. The Ngogo community is the largest known for chimpanzees and has an unusually large number of males. The attack was not related to a struggle for alpha rank: the victim was low-ranking and the community had a well-established alpha at the time. However, the victim had risen substantially in the male hierarchy over the past few years and might have appeared threatening to many higher-ranking males. Simultaneously, he associated relatively little with most other adult males, had relatively few grooming partners and was not well integrated into the male grooming network, and had no influential allies. The combination of these social factors with the unusual demographic circumstances – which presumably meant that mating competition was relatively high and the cost of losing one male relatively low – might have triggered the attack.     

Taphonomic analysis of skeletal remains from chimpanzee hunts at Ngogo, Kibale National Park, Uganda

This study provides a taphonomic analysis of the largest known sample of bone fragments collected from chimpanzee hunts. The entire sample consists of 455 bone fragments from 57 chimpanzee hunting episodes of 65 prey individuals at Ngogo, Kibale National Park, Uganda. It has low taxonomic diversity, consisting overwhelmingly of primates, especially red colobus monkeys. The age distribution of the prey remains is skewed towards pre-adults. Cranial bones are the dominant element, followed by long bones. Axial postcranial elements have low survivorship, with a complete absence of pre-caudal vertebrae. Bone is damaged in distinct ways, such as: destruction of long bone ends, typically with intact but chewed shafts; fragmentation and compression cracking of crania; and preservation of only the iliac blades of the innominates. Tooth marks are present but uncommon (4.4% of total NISP). These analyses enable us to: 1) describe and characterize consistent patterns of bone damage inflicted by chimpanzees across a much larger prey sample than has been previously studied; 2) make a preliminary comparison of the generalized chimpanzee taphonomic signature to that of leopard and eagle consumption of primates, as well as modern human consumption of small mammals; and 3) assess the utility of such samples for recognition of early hominin small mammal carnivory. We present a model that may be useful for detecting a pre-technological hominin carnivory and suggest some fossil locales at which close inspection of cercopithecoid remains for the above patterns might reveal traces of hominin hunting, though we caution that a pre-technological hominin hunted "assemblage" is not likely to be archaeologically visible.     

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.