Predicting folivorous primate abundance: validation of a nutritional model

Understanding the determinants of animal abundance has become more vital as ecologists are increasingly asked to apply their knowledge to the construction of informed management plans. However, there are few general models are available to explain variation in abundance. Some notable exceptions are studies of folivorous primates, in which the protein-to-fiber ratio of foods has been shown to predict biomass. Here we examine the generality of Milton's [American Naturalist 114:363-378, 1979] protein/fiber model by providing a detailed analysis of diet selection in black-and-white colobus monkeys (Colobus guereza), and applying the model to populations shown to be stable; an assumption not previously examined. Based on observations of two groups of black-and-white colobus in Kibale National Park, Uganda, and one group in a forest fragment, we documented that the animals selected young leaves that had more protein, were more digestible, and had a higher protein-to-fiber ratio than mature leaves. The mature leaves did not differ from young leaves with respect to secondary compounds or mineral content (with the exceptions of copper and zinc). All of the colobus groups selected foods with a high protein-to-fiber ratios. However, one group also selected more digestible foods, and in another group, foraging efforts were positively related to zinc and negatively related to potassium. Previous studies that examined Milton's protein/fiber model did not demonstrate that the study populations were stable. If some populations were not at carrying capacity, then the correlations drawn between food availability and/or quality and folivore biomass may have been spurious. To address this issue, we censused a series of forest fragments in 1995 and again in 2000. We found that the populations in these fragments had declined from 165 in 1995 to 119 animals in 2000. However, based on evidence of population stability and lack of forest disturbance, we concluded that five of the original populations were stable. The biomass of these populations was related to the protein-to-fiber ratio of the fragment's trees. Combining our data with published data, we demonstrate that the protein-to-fiber ratios of mature leaves available to these folivorous primates accounted for 87% of the variance in their biomass.     

Application of Protein-to-Fiber Ratios to Predict Colobine Abundance on Different Spatial Scales

The biomass of arboreal folivorous primates in Africa and Asia is related to an index of mature leaf quality: the ratio of protein-to-fiber concentration. Investigations have considered variation in folivore biomass and forest composition among sites separated by hundreds or thousands of km. However, large variation in folivore abundance has been documented over much smaller spatial scales. We quantify the degree to which the average protein-to-fiber ratio of mature leaves of the 20 most abundant tree species predicts the biomass of western red colobus (Piliocolobus trephosceles) and black-and-white colobus (Colobus guereza) over very small spatial scales. Four sites within Kibale National Park, Uganda, varied markedly in forest structure. Colobine biomass varied among sites from 191 to 2675 kg/km² and was related to the average protein-to-fiber ratio of mature leaves of the 20 most abundant tree species at each site. We examined the generality of the relationship between protein-to-fiber ratios and colobine abundance by adding our biomass and leaf chemistry values to previously published values to produce 9 comparable sites. At these locations, colobine biomass varied from 84 to 2675 kg/km² (mean biomass among sites = 910 kg/km²), and mean protein/fiber ratios varied from 0.167 to 0.577. Colobine biomass was related to the protein-to-fiber ratios of mature leaves (R ² = 0.616, P = 0.012).     

Variation in the Nutritional Value of Primate Foods: Among Trees, Time Periods, and Areas

The study of nutritional ecology has proven to be useful for understanding many aspects of primate behavior and ecology and is a valuable tool in primate conservation. However, to date this approach has had limited application since chemical analyses of food items is very time-consuming and collections of perishable food material are often made in remote field locations. Such logistic difficulties have led to plant material being collected in a variety of fashions, and it is not known how variation in collection method might influence our understanding of the chemical basis of dietary selection. A standardization of collection methods is greatly needed to allow for direct comparison among studies. To develop an appropriate standardized method and to evaluate past research, it is necessary to understand along what dimensions plant chemistry varies. We evaluated variation in nutritional value—protein, fiber, digestibility, alkaloids, saponins, cyanogenic glycocides, and minerals—of leaf material from species eaten by red colobus (Piliocolobus tephrosceles) and black-and-white colobus (Colobus guereza) of Kibale National Park, Uganda. We consider variation at 3-levels: among trees, time periods, and areas. While there was considerable variation among species with respect to protein, digestibility, and saponins, there was also variation among individuals of the same species; in fact, individuals may vary by as much as 20%. The average coefficients of variation (CV) among individuals of the same species are 13.4 for protein, 12 for digestibility, and 43 for saponins, while the average CV among species are 35, 31.3, and 82.4, respectively. No species showed a variable response with respect to testing for the presence or absence of cyanogenic glycocides, while 2 of 11 species tested for alkaloids showed a variable response. Over 2 years there was evidence of variation among time periods in the chemical composition of the same food items. The protein-to-fiber ratio of mature leaves of the same species collected from 4 sites separated by 12 km within Kibale was also variable and in some cases the variation among sites was greater than the differences among species. For example, while Funtumia latifolia had little variation in protein-to-fiber ratio at 3 sites (0.44 at all sites), the remaining site was 28% greater. Because temporal variation is less than variation among individuals, it is likely more important to sample from multiple trees at a single point in time than to sample across time. However, the most accurate assessment of nutrient intake is obtained by collecting plant material from the specific trees selected for consumption.     

Tree leaf chemical characters: selective pressures by folivorous primates and invertebrates

Plants have evolved a variety of chemical means to deter herbivory. Several studies have documented that secondary compounds are strong deterrents to certain herbivores, while others have demonstrated that some herbivores ingest large quantities of these compounds without exhibiting deleterious effects. This inconsistent response suggests that plants have evolved compounds to deter specific herbivores. Based on a study in Kibale National Park, Uganda, we explored how two major groups of herbivores, invertebrates and colobus monkeys, respond to chemical characteristics of leaves: protein, attractive from a nutritional perspective, and alkaloids, saponins and cyanogenic glycosides, which are all plant defences, detering herbivory. The intensity that colobus monkeys fed on leaves of different tree species was determined by observations (1300 h), and invertebrate herbivory was indexed by collecting leaves from 20 species and digitizing tracings to quantifying invertebrate damage. Invertebrate damage to leaves varied among species (1.5–22.5%), but showed no relationship with saponin or protein content, or the presence or absence of alkaloids. Colobine foraging effort did not relate to the saponin and protein of leaf species, nor to the presence or absence of alkaloids. Prunus africana, the only species to test positive for cyanogenic glycosides, was fed on by colobus monkeys for 8.1% of their foraging time, but, as it occurred at low densities, it was the most preferred species. These results can be interpreted in different ways. First, it is possible that inactive compounds are retained because they increase the probability of producing new active compounds. Secondly, the indices used to evaluate compound effects may be inappropriate. For example, monkeys may only be able to tolerate a toxin to a specific threshold in a single feeding session, but our index of foraging effort was averaged over the year. Thirdly, it may be that these compounds play an active role with organisms not considered (e.g. prevent fungal attack). Finally, these compounds may serve some unknown function and selection may operate for that purpose.     

Mineral Resource Availability and Consumption by Colobus in Kibale National Park,Uganda

Very little information exists on mineral nutrition of tropical, forest-dwelling species, yet minerals are critical to growth, reproduction, and survival. We examined the mineral resources available to and consumed by colobus in Kibale National Park, Uganda. We combined behavioral data on black-and-white (Colobus guereza) and red colobus (Piliocolobus tephrosceles) in a section of unlogged forest, a heavily logged area, and a forest fragment with mineral analysis of their foods to estimate the proportion of the diet containing specific minerals (mineral content). We compared mineral content of colobus foods (natural and crops) across plant parts and among plant species. Additionally, we estimated mineral intake of frugivorous primates in Kibale from published dietary data and our estimates of mineral content of foods. Dietary mineral content for all colobus groups and frugivorous species is similar despite significant differences in the mineral content of foods. Ripe and unripe fruits are lower in mineral content than most foods. Foods rarely consumed, such as bark, petioles, and caterpillars have high levels of some minerals. The mineral content of crops is low in comparison to that ofnatural foods. For all colobus groups of both species, sodium content of foods was extremely low and iron content was generally low, suggesting that intake isbelow suggested requirements, though current suggested iron requirements may overestimate physiological needs. Copper content was marginal and deficient seasonally for most colobus groups. Despite a sodium-limiting environment, only one of 8 colobus groups appeared to select sodium; however, this may be due to a lack of variation in sodium content among plant species and a positive correlation between high plant sodium content and secondary compounds. Despite the lack of selection for sodium by colobines, some behaviors point to a potential sodium deficiency, including urine drinking, consumption of high-sodium swamp plants, and use of mud-puddles.     

How do differences in species and part consumption affect diet nutrient concentrations? A test with red colobus monkeys in Kibale National Park,Uganda

Within a primate species, diet can be highly variable in composition, even at small spatial scales within the same forest, or temporally, suggesting that primates use different plant species and parts to meet similar nutritional needs. To test whether such differences in the plant species and parts that primates eat affects the nutrient concentrations that they obtain, we observed feeding of seven groups of red colobus monkeys ( Procolobus rufomitratus) residing in Kibale National Park, Uganda. The different groups consumed mostly young leaves from many of the same plant species, but spent different amounts of time feeding on them. As protein and fibre are suggested to be important determinants of colobine food choice and abundance, we analysed multiple samples of 47 food species for protein and fibre. Despite the differences in the plant species and parts eaten, the protein and fibre concentrations for the seven red colobus groups were similar. Our results suggest that colobus monkeys eating diets with differing amounts of species and parts may ultimately receive similar concentrations of nutrients.     

Constraints on Group Size in Red Colobus and Red-tailed Guenons: Examining the Generality of the Ecological Constraints Model

The ecological constraints model proposes that an increase in group size will increase intragroup feeding competition and thereby constrain group size. Although this model has received wide acceptance, tests of it are based only on a few studies of species that have similar ecological requirements and social organizations, and there are reasons to question the widespread acceptance of the assumptions underpinning it. Via a 2-year study, we explored determinants of group size in species that feed on markedly different types of foods: the folivorous red colobus (Procolobus pennantii) and the frugivorous/insectivorous red-tailed guenon (Cercopithecus ascanius). We established 4 study sites approximately 15 km apart in Kibale National Park, Uganda, to examine the relationship between average group size and food availability. In both species, we quantified interdemic variation in diet, density of food trees, rate of travel, and group size. Red colobus at all sites relied heavily on leaf resources (75.5%–86.9%), but fruit (6.4%–13.9%) and flowers (2.0%–13.9%) were important in some populations. In general, red-tailed guenons fed on fruit (35.7%–59.7%), insects (14.5%–17.6%), and young leaves (12.2%–32.8%), but the amount of time allocated to these foods varied among sites. Average monthly density of trees bearing food items ranged among sites from 45 to 79 trees/ha for red colobus and from 19.6 to 67.3 trees/ha for red-tailed guenons. For both species, rate of travel was similar among sites, with one exception for red colobus. Average red colobus group size varied among sites from 14 to 40 (28 groups counted). Red-tailed guenon group size varied among sites from 11 to 24 (16 groups counted). As predicted by the ecological constraints model, group size increased with food tree density across sites for both species.     

Frequency of cyanogenesis in tropical rainforests of far north Queensland, Australia

BACKGROUND AND AIMS: Plant cyanogenesis is the release of toxic cyanide from endogenous cyanide-containing compounds, typically cyanogenic glycosides. Despite a large body of phytochemical, taxonomic and ecological work on cyanogenic species, little is known of their frequency in natural plant communities. This study aimed to investigate the frequency of cyanogenesis in Australian tropical rainforests. Secondary aims were to quantify the cyanogenic glycoside content of tissues, to investigate intra-plant and intra-population variation in cyanogenic glycoside concentration and to appraise the potential chemotaxonomic significance of any findings in relation to the distribution of cyanogenesis in related taxa. METHODS: All species in six 200 m(2) plots at each of five sites across lowland, upland and highland tropical rainforest were screened for cyanogenesis using Feigl-Anger indicator papers. The concentrations of cyanogenic glycosides were accurately determined for all cyanogenic individuals. KEY RESULTS: Over 400 species from 87 plant families were screened. Overall, 18 species (4.5 %) were cyanogenic, accounting for 7.3 % of total stem basal area. Cyanogenesis has not previously been reported for 17 of the 18 species, 13 of which are endemic to Australia. Several species belong to plant families or orders in which cyanogenesis has been little reported, if at all (e.g. Elaeocarpaceae, Myrsinaceae, Araliaceae and Lamiaceae). A number of species contained concentrations of cyanogenic glycosides among the highest ever reported for mature leaves-up to 5.2 mg CN g(-1) d. wt, for example, in leaves of Elaeocarpus sericopetalus. There was significant variation in cyanogenic glycoside concentration within individuals; young leaves and reproductive tissues typically had higher cyanogen content. In addition, there was substantial variation in cyanogenic glycoside content within populations of single species. CONCLUSIONS: This study expands the limited knowledge of the frequency of cyanogenesis in natural plant communities, includes novel reports of cyanogenesis among a range of taxa and characterizes patterns in intra-plant and intra-population variation of cyanogensis.     

The role of phytochemistry in dietary choices of Tana River red colobus monkeys(Procolobus badius rufomitratus)

We conducted a phytochemical survey of tree species growing within the riverine forests of the Tana River National Primate Reserve in Kenya to understand better the feeding ecology of an endangered resident primate, the Tana River red colobus monkey (Procolobus badius rufomitratus).Young leaves, which make up a large percentage of this monkey's diet, are significantly higher in nitrogen and lower in acid detergent fiber than more abundant mature leaves are. Phenolic chemistry had little inhibitory effect on feeding by P. b. rufomitratus.Choice among tree species by P. b. rufomitratusappears to be influenced largely by leaf availability,once an acceptable threshold of nitrogen and fiber is reached When mature leaves are eaten, they selected species that are high in nitrogen and low in fiber. A significantly higher nitrogen content was found for the mature leaves of all leguminous versus nonleguminous tree species. Consequently, the availability of certain types of mature leaf species during periods of preferred food scarcity may prove critical to groups of Tana River red colobus monkeys.     

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.     

Estrogenic plant foods of red colobus monkeys and mountain gorillas in Uganda

Phytoestrogens, or naturally occurring estrogen-mimicking compounds, are found in many human plant foods, such as soybeans (Glycine max) and other legumes. Because the consumption of phytoestrogens may result in both health benefits of protecting against estrogen-dependent cancers and reproductive costs of disrupting the developing endocrine system, considerable biomedical research has been focused on the physiological and behavioral effects of these compounds. Despite this interest, little is known about the occurrence of phytoestrogens in the diets of wild primates, nor their likely evolutionary importance. We investigated the prevalence of estrogenic plant foods in the diets of two folivorous primate species, the red colobus monkey (Procolobus rufomitratus) of Kibale National Park and mountain gorilla (Gorilla beringei) of Bwindi Impenetrable National Park, both in Uganda. To examine plant foods for estrogenic activity, we screened 44 plant items (species and part) comprising 78.4% of the diet of red colobus monkeys and 53 plant items comprising 85.2% of the diet of mountain gorillas using transient transfection assays. At least 10.6% of the red colobus diet and 8.8% of the gorilla diet had estrogenic activity. This was mainly the result of the red colobus eating three estrogenic staple foods and the gorillas eating one estrogenic staple food. All estrogenic plants exhibited estrogen receptor (ER) subtype selectivity, as their phytoestrogens activated ERβ, but not ERα. These results demonstrate that estrogenic plant foods are routinely consumed by two folivorous primate species. Phytoestrogens in the wild plant foods of these two species and many other wild primates may have important implications for understanding primate reproductive ecology.     

Thirty Years of Research in Kibale National Park,Uganda, Reveals a Complex Picture for Conservation

Kibale National Park, Uganda, has a rich and abundant primate community and a complicated history of anthropogenic disturbance. Moreover, it has been the focus of over 30 yr of research and has received considerable attention from nongovernmental and governmental conservation organizations. As a result, Kibale serves as a valuable case study with which to evaluate the factors that regulate primate population density and the challenges of deriving generalizations for conservation. We review the impact of logging and forest fragmentation on primate population density and trace the efficacy of various conservation strategies. A 28-yr comparison of primate abundance in logged and unlogged forests and a 10-yr study of forest dynamics showed that primate recovery in logged areas is generally slow or not occurring at all for some species, which is likely driven by the fact that the forest is not recovering as expected. No primate species characteristic predicted their ability to live in forest fragments around Kibale. While a nutritional model was useful to predict the abundance of colobus in forest fragments outside of Kibale, a 5-yr study revealed that human land-use practices are more fundamentally shaping population dynamics. We evaluate data on primate abundance in light of Milton’s protein/fiber model to predict colobine biomass. We demonstrate that while the model can predict colobus biomass in pristine habitats, the 2 colobus species respond differently to disturbance. We offer suggestions for future conservation research and consider strategies to conserve forested national parks based on experiences gained over 30 yr.     

Primate DNA suggests long‐term stability of an African rainforest

Red colobus monkeys, due to their sensitivity to environmental change, are indicator species of the overall health of their tropical rainforest habitats. As a result of habitat loss and overhunting, they are among the most endangered primates in the world, with very few viable populations remaining. Traditionally, extant indicator species have been used to signify the conditions of their current habitats, but they have also been employed to track past environmental conditions by detecting previous population fluctuations. Kibale National Park (KNP) in Uganda harbors the only remaining unthreatened large population of red colobus. We used microsatellite DNA to evaluate the historical demography of these red colobus and, therefore, the long‐term stability of their habitat. We find that the red colobus population throughout KNP has been stable for at least ~40,000 years. We interpret this result as evidence of long‐term forest stability because a change in the available habitat or population movement would have elicited a corresponding change in population size. We conclude that the forest of what is now Kibale National Park may have served as a Late Pleistocene refuge for many East African species.     

Scale issues in the study of primate foraging: red colobus of Kibale National Park

Diet data have been used to address a number of theoretical issues. We often calculate the proportion of time spent eating different foods (e.g., fruits, leaves) to place species into dietary categories and contrast morphological or behavioral traits among categories. Yet we have little understanding of how flexible species can be in terms of the plant parts and species consumed. To address this issue, we analyzed data on the diets of red colobus monkeys (Procolobus badius) from Kibale National Park, Uganda, to evaluate temporal and spatial variability in the plant parts and species eaten. After considering observer differences and sampling issues, we evaluated how different a group's diet could be if samples were taken in different years. We found that the diet of the same groups showed significant, consistent changes over a 4-year period. For example, the time spent feeding on leaves increased from 56% in 1994 to 76% in 1998. The plant parts and species eaten by eight groups inhabiting different types of forest (e.g., pristine, logged, riverine) varied among groups. The largest interdemic difference was seen in the use of young leaves (38%). Dietary differences were also found between groups with overlapping home ranges (41-49% overlap). Different subspecies of Procolobus badius also varied in diet; however, this variation was often not of the magnitude documented within Kibale for the same population. The fact that diet can vary considerably over small spatial and short temporal scales within the same species raises the intriguing question as to what level of interspecific difference is biologically significant for addressing particular questions. We conclude that behavioral flexibility blurs our traditional stereotypic assessment of primates; a study of one group that occupies a specific habitat at one point in time may not adequately represent the species.     

Red colobus as prey: the leaping habits of five sympatric Old World monkeys

This study explored the leaping habits of five sympatric Old World monkeys (Colobus badius, Colobus guereza, Cercopithecus ascanius, Cercopithecus mitis and Cercocebus albigena) in an attempt to determine why chimpanzees prefer to hunt red colobus. We videotaped the leaps of the monkeys for 3 months in Uganda's Kibale National Park. Data were collected on leap preparation time as well as several other variables of the leaps. The leap preparation time of red colobus was found to be about double that of the other species studied. This difference is a likely reason why red colobus represent the preferred prey of chimpanzees. The hypothesis that red colobus spend more time in isolated trees than do other species was not supported.     

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.     

Killing of a pearl-spotted owlet (Glaucidium perlatum) by male red colobus monkeys (Procolobus tephrosceles) in a forest fragment near Kibale National Park, Uganda

Adult male red colobus (Procolobus tephrosceles) were observed capturing and killing an owl (Glaucidium perlatum) in the Rurama forest fragment near Kibale National Park in western Uganda. The owl was not subsequently eaten by the colobus, their conspecifics, or the other primates present during the attack. Because the incident was preceded by an agonistic encounter with a raptor, the event is best interpreted as a misdirected antipredator behavior. Although antipredator behaviors are not unknown in red colobus, this is the first such incident directed against a raptor to be documented.     

Coping with Forest Fragmentation: The Primates of Kibale National Park,Uganda

A goal of conservation biology is to determine which types of species are most susceptible to habitat disturbance and which types of disturbed habitats can support particular species. We studied 20 forest fragments outside of Kibale National Park, Uganda, to address this question. At each patch, we determined the presence of primate species, tree species composition, patch size, and distance to nearest patch. We collected demographic, behavioral, and dietary data for Abyssinian black-and-white colobus (Colobus guereza). Black-and-white colobus and red-tailed guenons (Cercopithecus ascanius) were in almost all fragments; Pennant's red colobus (Procolobus pennantii) and chimpanzees (Pan troglodytes) were in some fragments; and blue monkeys (Cercopithecus mitis) and gray-cheeked mangabeys (Lophocebus albigena) were absent from all fragments. No species characteristics—home range, body size, group size, or degree of frugivory—predicted the ability of species to live in patches. No characteristics of patches—area, distance to the nearest patch, distance to Kibale, or number of food trees present—predicted the presence of a particular species in a patch, but distance to Kibale may have influenced presence of red colobus. Black-and-white colobus group size was significantly smaller in the forest patches than in the continuous forest of Kibale. For a group of black-and-white colobus in one patch, food plant species and home range size were very different from those of a group within Kibale. However, their activity budget and plant parts eaten were quite similar to those of the Kibale group. The lack of strong predictive variables as well as differences between other studies of fragmentation and ours caution against making generalizations about primate responses to fragmentation.     

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.     

Implications of small scale variation in ecological conditions for the diet and density of red colobus monkeys

In this 3-year investigation we documented patterns of density, diet, and activity of red colobus monkeys (Procolobus tephrosceles) in six areas in or near Kibale National Park, Uganda and related these patterns to availability of food resources. There were large differences in the density and behavior of the red colobus among the sites. For example, the red colobus at one site with a diverse plant community of more than 61 tree species, had a diet that included at least 42 species. In contrast, at a second site red colobus spent 92% of their feeding time eating from one species that dominated the tree community. The density of important red colobus food trees varied among sites from 32 trees/ha to 204 trees/ha, and red colobus density ranged from 0.70 groups/km² to 7.41 groups/km². Among sites, red colobus density was related to the cumulative DBH of important food trees, when one apparently anomalous site was excluded, and populations with more plant species in their diets tended to be those that were found at higher densities. Activity budgets of the red colobus populations varied markedly among sites. For example, feeding time ranged among sites from 29 to 55%, and traveling varied from 5 to 20%. When faced with increased foraging demands, red colobus reduced the time spent resting, while the time spent socializing remained fairly constant. Comparative socioecological studies typically contrast species separated by large geographical distances to ensure there is sufficient variation in the environment to detect behavioral responses. The marked differences in ecological conditions and red colobus behavior we documented over short geographical distances, suggests that small-scale contrasts are a useful tool to examine ecological determinants of behavior and community structure.