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.     

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.     

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.     

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 and reproductive function in wild female chimpanzees (Pan troglodytes schweinfurthii) at Kibale National Park, Uganda

Human female reproductive function is highly sensitive to current energetic condition, indicating adaptation to modulate reproductive effort in accordance with changing ecological conditions that might favor or disfavor the production of offspring. Here, we test the hypothesis that reproductive capacity in female chimpanzees is likewise limited by current energetic condition. We used 12 years of data on wild chimpanzees (Pan troglodytes schweinfurthii) in the Kanyawara community of Kibale National Park, Uganda, to examine the relationship of dietary quality, as assessed by fruit components of the diet, to the occurrence of sexually receptive females, concentrations of ovarian steroid hormones, and timing of conception. We found that the frequency of females having sexual swellings was positively related to the consumption of drupe fruits. Estrogen levels of both cycling and noncycling females increased during seasonal peaks in the consumption of drupe fruits. When average fruit consumption remained high across months, females conceived more quickly. These results support the hypothesis that cycling and conception in chimpanzees are contingent upon high energy balance, and they indicate that the availability of fruit is a key variable limiting reproductive performance in chimpanzees. Chimpanzees appear to share with humans a reproductive system that is primed to respond to proximate levels of energy acquisition.     

Female Mate Preferences Among Pan troglodytes schweinfurthii of Kanyawara, Kibale National Park, Uganda

Studies of reproduction among chimpanzees traditionally have focused on the mating strategies of males. However, less is known about the mating strategies of female chimpanzees and whether they demonstrate mate choice. I investigated sexual behavior and female mate preference in the chimpanzees of the Kanyawara community. To estimate mate preferences, I analyzed female proceptivity and resistance rates of 6 estrous females toward a total of 13 males as well as male solicitation and aggression rates toward females. Males solicited some females more often than others for mating and preferred them throughout estrus, not only during the periovulatory period (POP), when conception was most likely. In contrast, though females had strong mate preferences in both non-POP and POP, their mate preferences were not consistent between the 2 phases. The shift in mate preferences is evidence of a promiscuous yet tactical mating strategy to confuse paternity. Further, females were more proceptive and generally less resistant toward eschewed males in non-POP and more proceptive and less resistant toward preferred males in POP. Hence, the results indicate that females attempted to mate selectively during the fertile phase. Kanyawara female chimpanzees appear to change their mating strategies and selectivity during estrus and thus may pursue a mixed reproductive strategy. The tactic may allow females to deceive males, indicating that promiscuity among chimpanzee females may be more strategic than previously thought.     

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.     

Sources of variation in the nesting behavior of chimpanzees (Pan troglodytes schweinfurthii) in the Budongo forest, Uganda

Data on nesting behavior and nests of the Sonso community of chimpanzees (Pan troglodytes schweinfurthii) living in the Budongo Forest, Uganda, were collected between October 1995 and December 1996. Analysis of the selection of nests shows a preference for particular tree species, especially Cynometra alexandri. Male chimpanzees nested lower than females. Day nests were found to be structurally simpler than night nests and were built in tree species used for feeding, at the same height as feeding activity. Day and night nests serve different functions, and should be clearly distinguished in studies of nesting behavior.     

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.     

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.     

Anxiety-related behavior of orphan chimpanzees (Pan troglodytes schweinfurthii) at Gombe National Park, Tanzania

This study examined the anxiety levels and social interactions of two orphan and four mother-reared adolescent chimpanzees (Pan troglodytes schweinfurthii) in the Kasekela community at Gombe National Park, Tanzania. We used focal sampling in the field at Gombe to observe these adolescent individuals. Their social interactions and anxious behavior, measured as rough scratching, were recorded. The two orphans differed from others of a similar age by exhibiting higher levels of anxiety and lower levels of play. These results suggest that a mother’s absence, even in naturalistic conditions in which other members of the community are available to the orphan, may have long-lasting impact on an adolescent’s anxiety and its ability to engage in complex social interactions, such as play.     

Body weights of wild chimpanzees (Pan troglodytes schweinfurthii) of the Mahale Mountains National Park, Tanzania

Ten male and nine female habituated chimpanzees (Pan troglodytes schweinfurthii) in the Kasoje area of the Mahale Mountains National Park, Tanzania, were weighed intermittently between December 1973 and March 1980 by luring them up a rope hung on a spring balance: six adult males averaged 42.0 kg and eight adult females 35.2 kg. Seasonal change in body weight was recognized at least partially; body weights tended to decrease in the later part of the wet season presumably because of food shortage in the middle of the wet season. Comparison of body weight among three populations of the same subspecies suggests that adult female chimpanzees of Mahale appear to be heavier than those of the Gombe National Park, Tanzania, and that they seem to be similar to the forest-living counterparts of eastern Zaire. On the other hand, body weights of adult male chimpanzees from the three populations do not show significant differences. Perhaps feeding competition among adult females in a small, isolated habitat is more severe than that among adult males, which may result in the body weight reduction among adult female chimpanzees at Gombe.     

Parallel lasers and digital photography to estimate limb size of chimpanzees (Pan troglodytes) at Ngogo,Kibale National Park,Uganda

Primates - How animals grow and when they stop growing are key variables for understanding life history evolution. Although theoretically straightforward, it is logistically difficult to take body...     

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.     

Food Supply and Chimpanzee (Pan troglodytes schweinfurthii) Party Size in the Budongo Forest Reserve,Uganda

A central issue in socioecology is the nature of the relationship between an organism's environment and its social structure. In chimpanzees, the fission-fusion social system is thought to minimize feeding competition for primary dietary components: ephemeral, dispersed patches of ripe fruit. Intragroup feeding competition is thought to force individuals into small parties. Informal observations in the Sonso region of the Budongo forest had suggested that in this habitat, food supply was such that feeding competition was less important in determining grouping patterns than elsewhere. We used data collected on food supply and party sizes over a 4-year period to investigate this suggestion. In accord with theoretical expectation, sizes of foraging parties fluctuated with the size of food patches. However, party sizes showed either negative or no relationship with habitat-wide measures of food abundance. Likewise party sizes showed little relationship to overall measures of food dispersion. For important dietary items, both fruit and leaves had patchy distributions, though the degree of clumping was not strong, and fruit was not more clumped than leaves. Generally, abundant food appeared to be less patchy, and chimpanzees appeared to use more patches as food became more abundant rather than forming larger parties. We suggest that both dispersal and abundance need to be considered when investigating the impact of food supply on grouping patterns, and that the importance of food as a factor in determining chimpanzee grouping patterns declines with increasing levels of abundance.     

Testosterone and energetics in wild chimpanzees (Pan troglodytes schweinfurthii)

Ovarian function in female hominoids is sensitive to both energy flux and energy balance, resulting in a reduced probability of conception during periods when a successful reproductive outcome is less likely. However, the extent to which energetic factors constrain gonadal function in male hominoids is not clear. We examined the effects of both acute and chronic variation in energy availability on urinary testosterone (T) levels in adult male chimpanzees. Acute changes in energy availability, which were assayed by means of observational data on feeding behavior, did not result in decreased T production for 11 individuals at Kibale National Park, Uganda. Chronic energy shortages, on the other hand, may be associated with lower T levels in this population. Adult males in Kibale (n=11), who maintain suboptimal access to energy, exhibit significantly lower urinary T levels than males in captivity (n=11), who are more sedentary and better fed. These results suggest that data on hormonal function in captive chimpanzees should be interpreted with caution because individuals may produce T at levels well above those that are typical in the wild. They also suggest that short-term variations in T levels in male hominoids are more likely to be explained by social factors than by energetic ones.     

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.