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.     

Feeding Ecology of Guerezas in the Kakamega Forest,Kenya: The Importance of Moraceae Fruit in Their Diet

Eastern black-and-white colobus (Colobus guereza), or guerezas, have long been considered to be one of the most folivorous primates. I conducted a study of the feeding ecology of two guereza groups (T and O) over an annual cycle in the Kakamega Forest of western Kenya. I found that the annual diets of both groups comprised mostly of leaves (T: 48%, O: 57%) though fruit (T: 44%, O: 33%) also accounted for a substantial portion of the diet. In the six months when fruit was most abundant, fruit consumption constituted an average of 58% of T-group's monthly diet and 42% of O-group's monthly diet. In contrast to most previous studies of colobines, in which seeds were the primary fruit item consumed, almost all of the fruit eaten by guerezas at Kakamega consisted of whole fruits. At least 72% of the whole fruits consumed by T-and O-groups were whole fruits from trees in the Moraceae family, which dominates the tree family biomass at Kakamega. Unlike at sites where guerezas consumed fruit primarily when young leaves were scarce, at Kakamega guerezas ate fruit in accordance with its availability and irrespective of the availability of young leaves. My findings demonstrate that guerezas are more dietarily flexible than was previously known, which may help to explain why the species can survive in such a wide variety of forested habitats across equatorial Africa.     

The effect of depletion and predictability of distinct food patches on the timing of aggression in red deer stags

For group-foraging ungulates, forage is generally widely and relatively evenly dispersed. However, for free-ranging red deer Cervus elaphus supplementary winter feeding provides distinct patches of predictable food. These patches differ in size, but also in temporal distribution and depletion rate. Interference competition is known to increase with increasing spatial clumping (decreasing patch size), but the influence of temporal clumping and the predictability of food occurrence has received much less attention. Therefore in this study we investigated the effects of different degrees of spatial and temporal clumping of food on interference competition during feeding. Patch size was the main parameter influencing participation in feeding as well as interference competition during feeding on the respective patch. Temporal dispersion and the predictability of food occurrence were however, important parameters for the timing of aggressive interactions. Generally, aggression occurs during feeding and increases with decreasing patch size. But when depletion rate was high food availability was predictably short and the patch occurred predictably (such as hay), middle ranking stags increased aggression already prior to feeding at the respective patch. We suggest that in this way they confirmed hierarchy outside feeding on the quickly depleted patch and as a result gained actual feeding time when feeding on the respective patch. With the patch occurring predictably but varying in size the number of participating subordinates varied concomitantly with variation in patch size. Subordinates assessed patch profitability and left without having fed when patch size was too small for an efficient participation. When patch size was predictably small enough to be defended exclusively (feed blocks), subordinate stags did not assess profitability each time but did not participate at all in feeding at the respective patch. The relative importance of these various food-related parameters (patch size depletion rate, predictability) influencing feeding competition and the timing of aggression will vary with group size, rank, alternative food sources, physical characteristics of the food as well as different hierarchy systems of the feeding animals.     

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.     

Nutritional ecology of Preuss's red colobus monkey (Colobus badius preussi Rahm 1970) in Korup National Park, Cameroon

Studies on the nutritive ecology of red colobus monkeys (Colobus badius preussi) in Korup National Park, Cameroon, investigated food plants and the parts eaten as well as nutritive values of the various food items. Food plants were identified through direct observations and collected for laboratory determination of nutrient content. Food plants were analysed for crude protein (CP), crude fibre (CF), ether extract (EE), nitrogen‐free‐extractive (NFE) and total ash (A). A total of seventeen species belonging to nine different families were identified as food plants for red colobus. Food and feeding habits showed that the species were highly folivorous, tending to prefer the young leaves of food plants. Lecomtedoxa klaineana (27.0%) and Xylopia aethiopica (22.2%) of families Sapotaceae and Annonaceae, respectively, constituted about 50% of total food items consumed. Results of nutrient composition indicated individual nutrients varied significantly (P < 0.01) with food species.     

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.     

Group size in folivorous primates: ecological constraints and the possible influence of social factors

The ecological-constraints model assumes that food items occur in depletable patches and proposes that an increase in group size leads to increased day range due to more rapid patch depletion. Smaller groups become advantageous when an increase in travel costs is not repaid by an increase in energy gained or some other fitness advantage. On the other hand, we also know that group size can be influenced by social factors. Here we contrast the diet and group size of red colobus (Procolobus badius) and black-and-white colobus (Colobus guereza) in Kibale National Park, Uganda to consider how ecological and social factors are affecting their group sizes. Subsequently, we examine whether the insights gained from this detailed comparison can provide an understanding of why the social organization and group size of mantled howlers (Alouatta palliata) and black howlers (A. pigra) differ. Two groups of red colobus and two groups of black-and-white colobus were studied over 10 months. Red colobus groups were larger (48 and 24) than black-and-white colobus groups (9 and 6). The two groups of red colobus overlap home ranges with the two groups of black-and-white colobus; 75% and 95% of their home ranges were within red colobuss home range. There was a great deal of similarity in the plant parts eaten by the two species and both species fed primarily on young leaves (red colobus 70%, black-and-white colobus 76%). In terms of the actual species consumed, again there was a great deal of similarity between species. The average dietary overlap among months for the two neighboring groups of red colobus was 37.3%, while the dietary overlap between the red colobus and the black-and-white colobus group that had its home range almost entirely within the home range of the red colobus groups averaged 43.2% among months. If ecological conditions were responsible for the difference in group size between the two colobine species, one would expect the density of food trees to be lower in the home ranges of the black-and-white colobus monkeys, since they have the smaller group size. We found the opposite to be true. Both black-and-white colobus groups had more food trees and the cumulative size of those trees was greater than those in the red colobuss home ranges. We quantify how these differences parallel differences in mantled and black howlers. The average group size for mantled howlers was 12.9 individuals, and for black howlers it was 5.3 individuals. We explore possible social constraints, such as infanticide, that prevent black-and-white colobus and black howlers from living in large groups.This revised version was published online in April 2005 with corrections to the cover date of the issue.     

Group Size Dynamics over 15+ Years in an African Forest Primate Community

Group size affects many aspects of the ecology and social organization of animals. We investigated group size stability for five primate species in Kibale National Park, Uganda from 1996 to 2011 at three nested spatial scales. Survey data indicated that group sizes did not change for most species, with the exception of red colobus monkeys (Procolobus rufomitratus), in which group size increased at all spatial scales. Mangabey (Lophocebus albigena) group size increased in old‐growth forest, but the sample size and increase were small. To augment this survey data, we collected several years of demographic data on three habituated groups of redtail monkeys (Cercopithecus ascanius), eight groups of black‐and‐white colobus (Colobus guereza), and one red colobus group. The red colobus group increased from 59 to 104 individuals, while redtail monkey and black‐and‐white colobus group sizes were stable, mirroring our survey results. To understand mechanisms behind group size changes in red colobus versus stability in other primates, we monitored forest dynamics at two spatial scales between 1990 and 2013, considered changes in predator population, and explored evidence of disease dynamics. The cumulative size of all trees and red colobus food trees increased over 24 yr, suggesting that changing food availability was driving group size changes for red colobus, while predation and disease played lesser roles. Overall, our results and evidence of changing primate densities suggest that the Kibale primate community is in a non‐equilibrium state. We suggest future conservation and management efforts take this into consideration.     

Gis analysis of patch use and group cohesiveness of bearded sakis (chiropotes sagulatus) in the upper essequibo conservation concession,guyana

This study examines how northern bearded sakis (Chiropotes sagulatus) in Guyana adjust group cohesiveness according to the distribution and quality of food patches. I introduce a GIS based method for quantifying food patch quality and how it relates to bearded saki group spread and group size. While the concept of food patch is central to most models of primate socioecology, defining what constitutes a patch has been notoriously problematic in primate studies. In addition, researchers have struggled to quantify group spread and group cohesiveness. Advances in spatial analysis software in the last decade now allow primate researchers to better quantify these variables. Group spread in bearded sakis was not significantly greater in lower quality patches and sakis were not more spread out during feeding than during other activities. However, the study group was significantly less spread out during social behavior. Bearded saki group size was significantly correlated with both monthly fruit abundance and patch quality. In fact, mean daily patch quality explained ～40% of the variation in foraging party size. These results suggest that bearded sakis may rely on a highly fluid social structure to mitigate the effects of intragroup feeding competition while living in large groups. Sakis do not adjust group spread on a patch‐by‐patch basis but rather fission into smaller foraging parties when resources become scarce seasonally and patch quality is low. This study shows that GIS is a powerful tool for modeling the relationship between group cohesiveness and resource quality and distribution. Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

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.     

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.     

Tana river red colobus and crested mangabey: Results of recent censuses

Censuses of the Tana River red colobus (Colobus badius rufomitratus) and crested mangabey (Cercocebus galeritus galeritus), primate species endemic to riverine forests of the lower Tana River in eastern Kenya, showed significant population declines for both species between the mid-1970s and 1980s. Red colobus declined in terms of group size and number of groups per forest; the mangabey population declined only in numbers of groups per forest. There was no significant change in mean group age/sex composition between the two time periods for either species. Differences in the feeding and ranging ecology of the two species may explain why the mangabey population suffered a less severe decline than the red colobus. Similarities in census results over 3 years in the late 1980s suggest that the primate populations are no longer decreasing.     

Characterization of a novel simian immunodeficiency virus from guereza colobus monkeys (Colobus guereza) in Cameroon: a new lineage in the nonhuman primate lentivirus family

Exploration of the diversity among primate lentiviruses is necessary to elucidate the origins and evolution of immunodeficiency viruses. During a serological survey in Cameroon, we screened 25 wild-born guereza colobus monkeys (Colobus guereza) and identified 7 with HIV/SIV cross-reactive antibodies. In this study, we describe a novel lentivirus, named SIVcol, prevalent in guereza colobus monkeys. Genetic analysis revealed that SIVcol was very distinct from all other known SIV/HIV isolates, with average amino acid identities of 40% for Gag, 50% for Pol, 28% for Env, and around 25% for proteins encoded by five other genes. Phylogenetic analyses confirmed that SIVcol is genetically distinct from other previously characterized primate lentiviruses and clusters independently, forming a novel lineage, the sixth in the current classification. Cercopithecidae monkeys (Old World monkeys) are subdivided into two subfamilies, the Colobinae and the Cercopithecinae, and, so far, all Cercopithecidae monkeys from which lentiviruses have been isolated belong to the Cercopithecinae subfamily. Therefore, SIVcol from guereza colobus monkeys (C. guereza) is the first primate lentivirus identified in the Colobinae subfamily and the divergence of SIVcol may reflect divergence of the host lineage.     

Test of the ecological-constraints model on ursine colobus monkeys (Colobus vellerosus) in Ghana

For group-living mammals, the ecological-constraints model predicts that within-group feeding competition will increase as group size increases, necessitating more daily travel to find food and thereby constraining group size. It provides a useful tool for detecting scramble competition any time it is difficult to determine whether or not food is limiting. We tested the ecological-constraints model on highly folivorous ursine colobus monkeys (Colobus vellerosus) at the Boabeng-Fiema Monkey Sanctuary in Ghana. Three differently sized groups were followed for 13 months and two others were followed for 6 months each in 2004-2005 using focal-animal sampling and ranging scans; ecological plots and phenology surveys were used to determine home-range quality and food availability. There was relatively little difference in home-range quality, monthly food availability, diet, adult female ingestion rates, and rate of travel within food patches between the groups. However, home-range size, day-range length, and percent of time spent feeding all increased with group size. We performed a single large test of the ecological-constraints model by combining several separate Spearman correlations, each testing different predictions under the model, using Fisher's log-likelihood method. It showed that the ecological-constraints model was supported in this study; scramble competition in this population is manifesting in increased ranging and time spent feeding. How costly this increased energy expenditure is for individuals in larger groups remains to be determined.     

Predicting the Competitive Regime of Female <Emphasis Type="Italic">Colobus vellerosus</Emphasis> from the Distribution of Food Resources

We examined the spatial and temporal distribution of the foods of ursine colobus (Colobus vellerosus) at Boabeng-Fiema, Ghana as a means to predict the monopolizablity and usurpability of their food resources. Recent evidence suggests that food may not be limiting for folivorous primates, and that male sexual coercion may be a more important influence on folivore social organization. To address the question, we collected focal data on the feeding behavior of adult females and males over 11 mo (September 2000-August 2001) on 2 groups: WW (n = 31–33 individuals) and B (n = 8–16 individuals). We also conducted phenological monitoring and a tree survey of the two-group home ranges to establish food availability and distribution. We used 2 behavioral or organism-defined indicators of feeding behavior to assess potential resource contestability: food site residence time and distance moved between food sites. The colobus fed on a high diversity of species, most of their food trees were not clumped in distribution, within-tree interfood distances were short, and food trees were large. The only condition associated with the potential for monopolization was low food tree density. However, low food tree density may be offset by the colobus’ use of large trees. Taken together, the ecological and behavioral indicators suggest the food resources of Colobus vellerosus had a low potential for monopolization. Our results also indicate mature leaves had the longest food site residence time, which may suggest they should be the most usurpable plant part, though their presumed low quality and high abundance probably counteracted the effect. The pattern implied the potential for direct feeding competition among Colobus vellerosus at Boabeng-Fiema was low and agonistic interactions over food are not expected. Instead, a group size effect on feeding efficiency should be a more predominant influence on feeding efficiency, if food is limiting for the species.     

Activity and Ranging Patterns of Guerezas in the Kakamega Forest: Intergroup Variation and Implications for Intragroup Feeding Competition

From March 1997 to February 1998, I investigated the activity patterns of 2 groups and the ranging patterns of 5 groups of eastern black-and-white colobus (Colobus guereza), aka guerezas, in the Kakamega Forest, Kenya. Guerezas at Kakamega spent more of their time resting than any other population of colobine monkeys studied to date. In addition, I recorded not one instance of intragroup aggression in 16,710 activity scan samples, providing preliminary evidence that intragroup contest competition may be rare or absent among guerezas at Kakamega. Mean daily path lengths ranged from 450 to 734 m, and home range area ranged from 12 to 20 ha, though home range area may have been underestimated for several of the study groups. Home range overlap was extensive with 49–83% of each group's range overlapped by the ranges of other groups. Despite the high level of home range overlap, the frequently entered areas (quadrats entered on 30% of a group's total study days) of any one group were not frequently entered by any other study group. Mean daily path length is not significantly correlated with levels of availability or consumption of any plant part item. Mean daily path length is also not significantly correlated with group size, though the largest group did have the longest mean daily path length. This finding suggests that intragroup scramble competition may have been rare or absent among guerezas at Kakamega except perhaps in the largest group, which was unusually large.     

Increasing Group Size Alters Behavior of a Folivorous Primate

Group size influences many aspects of mammalian social life, including stress levels, disease transmission, reproductive rates, and behavior. However, much of what is known about the effects of group size on behavioral ecology has come from comparisons across multiple groups of different sizes. These findings may be biased because behavioral differences across groups may be more indicative of how environmental variation influences animal behavior, rather than group size itself. To partially circumvent this limitation, we used longitudinal data to examine how changes in group size across time affect the behavior of folivorous red colobus monkeys (Procolobus rufomitratus) of Kibale National Park, Uganda. Controlling for food availability, we demonstrated that increasing group size resulted in altered activity budgets, based on 6 yr of data on a group that increased from 57 to 98 members. Specifically, as group size increased, individuals spent less time feeding and socializing, more time traveling, and increased the diversity of their diet. These changes appear to allow the monkeys to compensate for greater scramble competition apparent at larger group sizes, as increasing group size did not show the predicted relationship with lower female fecundity. Our results support recent findings documenting feeding competition in folivorous primates. Our results also document behavioral flexibility, an important trait that allows many social mammals to maximize the benefits of sociality (e.g., increased vigilance), while minimizing the costs (e.g., increased feeding competition).     

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.     

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.