Comparative Feeding Ecology of Two Communities of Chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>) in Kibale National Park,Uganda

Several recent studies have documented considerable intraspecific and intrapopulation ecological variation in primates. However, we generally lack an understanding of how such variability may be linked to concomitant demographic variation among groups or populations of the same species, particularly in regard to large-bodied and wide-ranging species with high ecological flexibility, such as chimpanzees (Pan troglodytes). We compared the feeding ecology of chimpanzees inhabiting 2 sites in Kibale National Park, Uganda that differ 3-fold in chimpanzee density and support notably different plant communities. Chimpanzees at Ngogo, a site with the largest known chimpanzee community and unusually high chimpanzee density, spent a significantly lower percentage of time resting (and pregnant and lactating females spent more time feeding), incorporated higher percentages of ripe fruit in their diet, had lower dietary diversity values, and had shorter and less variable average patch residency times than did their counterparts at the nearby Kanyawara site, which supports a relatively low density of chimpanzees. In addition, feeding party size was significantly and positively related to feeding patch size at Ngogo, but not at Kanyawara. Together these findings aid in explaining the noted disparity in chimpanzee community size and density between Ngogo and Kanyawara by suggesting that the diet of Ngogo chimpanzees is of higher overall quality than that of Kanyawara chimpanzees. They also highlight the potentially profound influence of even small-scale habitat heterogeneity on the ecology of primates. Researchers must take such influences into account when attempting to draw conclusions about species- or population-level characteristics.     

Mangabey (Cercocebus albigena) population density,group size,and ranging: A twenty-year comparison

Mangabey groups studied in the Kibale Forest Reserve, Uganda, in 1971 were studied again in 1991 using similar data collection protocols. The results were used to assess the effect of group size on activity budgets and travel costs, and to document the effects of habitat changes on mangabey density and demography. Larger mangabey groups traveled longer distances per day than smaller groups. Time budgets were less clearly influenced by group size. Mangabey population density increased over the 20 year period. This increase in population density paralleled habitat changes, particularly an increase in tree density, and was accompanied by increased use of regenerating forest. © 1994 Wiley-Liss, Inc.     

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.     

Suitable Habitats for Endangered Frugivorous Mammals: Small-Scale Comparison,Regeneration Forest and Chimpanzee Density in Kibale National Park,Uganda

Landscape patterns and chimpanzee (Pan troglodytes schweinfurthii) densities in Kibale National Park show important variation among communities that are geographically close to one another (from 1.5 to 5.1 chimpanzees/km²). Anthropogenic activities inside the park (past logging activities, current encroachment) and outside its limits (food and cash crops) may impact the amount and distribution of food resources for chimpanzees (frugivorous species) and their spatial distribution within the park. Spatial and temporal patterns of fruit availability were recorded over 18 months at Sebitoli (a site of intermediate chimpanzee density and higher anthropic pressure) with the aim of understanding the factors explaining chimpanzee density there, in comparison to results from two other sites, also in Kibale: Kanyawara (low chimpanzee density) and Ngogo (high density, and furthest from Sebitoli). Because of the post-logging regenerating status of the forest in Sebitoli and Kanyawara, smaller basal area (BA) of fruiting trees most widely consumed by the chimpanzees in Kanyawara and Sebitoli was expected compared to Ngogo (not logged commercially). Due to the distance between sites, spatial and temporal fruit abundance in Sebitoli was expected to be more similar to Kanyawara than to Ngogo. While species functional classes consumed by Sebitoli chimpanzees (foods eaten during periods of high or low fruit abundance) differ from the two other sites, Sebitoli is very similar to Kanyawara in terms of land-cover and consumed species. Among feeding trees, Ficus species are particularly important resources for chimpanzees at Sebitoli, where their basal area is higher than at Kanywara or Ngogo. Ficus species provided a relatively consistent supply of food for chimpanzees throughout the year, and we suggest that this could help to explain the unusually high density of chimpanzees in such a disturbed site.     

Random walks and the gas model: spacing behaviour of Grey-Cheeked Mangabeys

1. Simple mechanical models (random walks and the 'gas model') were used to investigate the movement patterns and intergroup encounter rates of a high- and low-density subpopulation of Grey-Cheeked Mangabeys ( Cercocebus albigena johnstoni, Lydeker) at two sites in the Kibale Forest, Western Uganda.
2. Random walk simulations showed that the presence of conspecific groups could act as 'social barriers' which constrained group movements, and promoted high levels of site attachment to a specific home range area.
3. Encounter rate models showed that in the low-density subpopulation (Kanyawara), intergroup encounters occurred no more frequently than expected if groups were moving randomly and independently of each other. This was in contrast to previous analyses which suggested that Grey-Cheeked Mangabeys employed a social spacing mechanism (mediated by male loud calls) in order to reduce the frequency of encounter to below chance levels.
4. Encounters in the high-density subpopulation (Ngogo) were found to occur less frequently than expected at short range (within 100 m). This was suggested to be due to the operation of a territorial mate defence strategy by males at this site.     

Mangabey (Cercocebus albigena) ranging patterns in relation to fruit availability and the risk of parasite infection in Kibale National Park,Uganda

Two opposing hypotheses concerning determinants of mangabey (Cercocebus albigena) ranging patterns have been advocated. One hypothesis suggests that ranging patterns of mangabeys are largely a response to fruit availability, while the other hypothesis advocates that concerns of fruit availability are supplemented or overridden by concerns of fecal contamination and that the risk of parasite infection, especially during dry weather, determines their pattern of range use. In this 9 month study of mangabeys in the Kanyawara study area of Kibale National Park, mangabeys moved longer distances during the wet season than during the dry season. There were no seasonal differences in group spread, number of 50 by 50 m quadrats used, or in quadrat overlap between sequential sample periods. Intensity of quadrat use was closely related to the number of fruiting trees/lianas in the quadrats, irrespective of season. These findings are consistent with the hypothesis that fruit availability is a main factor influencing mangabey ranging patterns. The results are not consistent with the hypothesis that mangabey ranging patterns largely reflect differential seasonal risk of parasite infection. Am. J. Primatol. 43:65–78, 1997. © 1997 Wiley-Liss, Inc.     

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.     

Dietary Variability in Redtail Monkeys (<Emphasis Type="Italic">Cercopithecus ascanius schmidti</Emphasis>) of Kibale National Park,Uganda: the Role of Time,Space, and Hybridization

Studies of the diet of different groups of the same species allow us to understand intraspecific dietary variability. I collected dietary data from six neighboring groups of redtail monkeys (Cercopithecus ascanius schmidti) and three hybrid monkeys over 12 years at Ngogo and from one group at Kanyawara in Kibale National Park, Uganda and compared these results with previous studies of redtail diets elsewhere in Kibale and from the Kakamega Forest of Kenya. I scored feeding as a particular monkey ingesting a species-specific plant part, or catching insects from a species-specific substrate. A new feeding score was tallied for the same combination of parameters only after a 30-min interval or if the identity of one of the three parameters changed. I counted trees along transects in the home ranges of the two main study groups to calculate food selection ratios. I used chi-square tests to compare diets between groups and time periods and Spearman rank correlation coefficient tests for dietary correlates. These comparisons reveal considerable variation in plant parts and species eaten by redtails between months, years, and neighboring groups with overlapping ranges. Selection ratios show that some tree species are important sources of plant food, while others are more important as sources of invertebrates. The high incidence of insectivory by redtails demonstrates another ecological role they play in addition to seed dispersal. The intrademic variation in diets I describe for Kibale was often as great as and sometimes greater than the interdemic variation. The diets of the hybrid monkeys at Ngogo differed in some ways from their parental species, particularly in their greater consumption of invertebrates. Introgression may have led to some of these differences within and between redtail demes. The pronounced variability in redtail diets demonstrates why a typological perspective of species is unwarranted and that the validity of interspecific comparisons requires a thorough understanding of intraspecific variation.     

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.     

Forest succession in Kibale National Park, Uganda: implications for forest restoration and management

Forest succession was studied in four plots in former grasslands at the Ngogo study area in Kibale National Park, Uganda. The plots were located in areas that had been protected from fire for 0.58, 25, 9 and ≈30 years for plots 1, 2, 3 and 4, respectively. Species richness reflected the length of time that the plot had been protected from fire; it was highest in plot 4 and lowest in plot 1. Species density, stem density and basal area were all highest in plot 4 and lowest in plot 1. The species densities of plots 2 and 3 were not different. Similarly, plots 2 and 4 did not differ with regard to stem density or basal area. Animal seed dispersers played a vital role in the colonization of grasslands by forest tree species.     

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.     

Changes in group size and composition of the blue monkeys (Cercopithecus mitis stuhlmanni) between 1984 and 2009 at Ngogo,Kibale National Park,Uganda

Group counts were conducted on five groups of blue monkeys at the Ngogo study site, Kibale National Park, Uganda between January and June 2009. Group sizes were compared with those obtained using similar methods at the same site during 1983‐84 by Tom Butynski. During the present study, group size ranged from 16 to 28 monkeys. The results show that the group size of blue monkeys (Cercopithecus mitis stuhlmanni) has increased significantly between 1984 and 2009. Mean group size has increased over two‐fold from 9 after the fission of group 33 during Butynski s study to 21.6 animals per group in 2009. These results strongly suggest that the density of blue monkeys at Ngogo has increased although census data indicate that group density has remained more or less the same.     

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.     

The Value of Measuring Food Availability on the Ground for a Semiterrestrial Frugivore, the Tana River Mangabey (Cercocebus galeritus) of Kenya

Collecting phenological data, seasonal availability of plant resources that primates feed on, allows us to understand feeding ecology better. A number of primates are terrestrial or semiterrestrial frugivores, yet phenology is generally measured only in the canopy. I hypothesized that combining measurements of food availability on the ground with canopy measurements would more strongly correlate with diet than canopy measurements alone for a semiterrestrial frugivore, the Tana River mangabey (Cercocebus galeritus). From July 2005 until June 2006, I conducted monthly follows on a mangabey group. Phenology was measured in 105 individuals of their top seven food tree species. I measured canopy phenology on a 0–5 scale and counted fruits in three 1 m³ areas of the canopy, and measured ground phenology by counting fruits and seeds in four 1 m² quadrats under the canopy. I calculated each tree’s canopy volume and canopy shadow, and each species’ mean fruit weight, mean seed weight, and density. Monthly biomasses were calculated as kilograms per hectare. Spearman correlations were performed between diet contribution and canopy biomass, ground biomass, and total biomass. The hypothesis was not supported for seven species individually or combined. The hypothesis was supported for 3 of 12 diet items, although canopy biomass was also significant for 2 of those items. Two diet items correlated only with ground biomass. Studies of the Tana River mangabey may benefit from measuring ground phenology only for those items eaten exclusively on the ground. Primatologists studying terrestrial or semiterrestrial frugivores should consider feeding height when deciding on phenology methods.     

Mixed-species primate groups in the kibale forest: Ecological constraints on association

Five species of diurnal primates in the Kibale Forest of western Uganda— red colobus (Colobus badius),black- and- white colobus (Colobus guereza),redtail monkeys (Cercopithecus ascanius),blue monkeys (Cercopithecus mitis),mangabeys (Cercocebus albigena)-often associate in mixed- species groups that vary in size and composition from day to day. Across this range of species, we found no consistent effect of association on feeding rate. In addition, there is no systematic difference between the species- specific individual feeding rates when animals were in mixed- species groups feeding in a specific tree on one day and when individuals of one of the same species were feeding in the same individual tree on a subsequent day. If associating in a mixed- species group lowers the risk of predation, one might expect that the number of vigilant events would decrease in mixed- species groups. However, the only species to exhibit a consistent decrease in vigilant behavior when in association was the red colobus. Redtail monkeys were more vigilant when in association. We predicted that the density and distribution of food resources would both constrain the frequency of association and the size of mixed- species groups. Based on 22 months of data on food resources and bimonthly censuses, we found no relationship between the frequency of association (except mangabeys) or mean mixed- species group size and the density and distribution of food resources for all species. Finally, we examined the behavior of the monkeys in and out of association before and after the playback of a crowned hawk eagle call (Spizaetus coronatus),a known predator. When more species were in association, the amount of time they spent being vigilant following the playback was greater and the response more intense than when fewer species were in association or when the group was alone. The results of this study illustrate that the nature of the costs and benefits of polyspecific associations for these different monkey species are complex and vary from species to species.     

Urinary C-peptide tracks seasonal and individual variation in energy balance in wild chimpanzees

C-peptide of insulin presents a promising new tool for behavioral ecologists that allows for regular, non-invasive assessment of energetic condition in wild animals. C-peptide is produced on an equimolar basis with insulin, thus is indicative of the body's response to available glucose and, with repeated measurement, provides a biomarker of energy balance. As yet, few studies have validated the efficacy of C-peptide for monitoring energy balance in wild animals. Here, we assess seasonal and interindividual variation in urinary C-peptide concentrations of East African chimpanzees (Pan troglodytes schweinfurthii). We assayed 519 urine samples from 13 adult male chimpanzees in the Kanyawara community of Kibale National Park, Uganda. C-peptide levels were significantly predicted by the total amount of fruit and the amount of preferred fruit in the diet. However, chimpanzees had very low C-peptide titers during an epidemic of severe respiratory illness, despite highly favorable feeding conditions. Kanyawara males had significantly lower C-peptide levels than males at Ngogo, a nearby chimpanzee community occupying a more productive habitat. Among Kanyawara males, low-ranking males had consistently higher C-peptide levels than dominant males. While counterintuitive, this result supports previous findings of costs associated with dominance in male chimpanzees. Our preliminary investigations demonstrate that C-peptide has wide applications in field research, providing an accessible tool for evaluating seasonal and individual variation in energetic condition, as well as the costs of processes such as immune function and reproduction.     

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.     

Primate polyspecific associations: Do they occur by chance?

Contrary to subjective impressions, the frequency of mixed-species associations of African forest primates is often no greater than would be expected by ‘chance’. Two null hypotheses predicting association frequency are developed and compared with data on mangabeys in the Kibale forest, Uganda; association frequencies imply behavioural attraction in the the case of only one of six species present. For other species, the simpler possibilities that associations reflect high population density or use of mutual feeding sites cannot be rejected. Comparative data from West African associations suggest more ‘significant’ association tendencies there. It is suggested that, even where the evidence indicates that tendencies to associate between species have been favoured by selection, association need not benefit both species.     

Primates take weather into account when searching for fruits

Temperature and solar radiation are known to influence maturation of fruits and insect larvae inside them . We investigated whether gray-cheeked mangabeys (Lophocebus albigena johnstonii) of Kibale Forest, Uganda, take these weather variables into account when searching for ripe figs or unripe figs containing insect larvae. We predicted that monkeys would be more likely to revisit a tree with fruit after several days of warm and sunny weather compared to a cooler and more cloudy period. We preselected 80 target fig trees and monitored whether they contained ripe, unripe, or no fruit. We followed one habituated monkey group from dawn to dusk for three continuous observation periods totalling 210 days. Whenever the group came within a 100 m circle of a previously visited target tree for a second time, we noted whether or not individuals proceeded to the trunk, i.e., whether they "revisited" or simply "bypassed" the tree. We found that average daily maximum temperature was significantly higher for days preceding revisits than bypasses. The probability of a revisit was additionally influenced by solar radiation experienced on the day of reapproach. These effects were found only for trees that carried fruit at the previous visit but not for trees that had carried none. We concluded that these nonhuman primates were capable of taking into account past weather conditions when searching for food. We discuss the implication of these findings for theories of primate cognitive evolution.     

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.