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.     

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.     

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.     

Giardia sp. and Cryptosporidium sp. infections in primates in fragmented and undisturbed forest in western Uganda

In June 2005, we collected 115 fecal samples from wild primates in western Uganda and examined them for Cryptosporidium sp. and Giardia sp. with the use of immunofluorescent antibody (IFA) detection. We sampled primates from an undisturbed forest in Kibale National Park and from 3 highly disturbed forest fragments outside the park. Of disturbed forest samples, red colobus (Pilocolobus tephrosceles) and red-tailed guenons (Cercopithecus ascanius) harbored species of Cryptosporidium or Giardia, but black-and-white colobus (Colobus guereza) did not. All primate samples from undisturbed forest were negative for both parasites. Seven of 35 (20%) red colobus and 1 of 20 red-tailed guenons (5%) from forest fragments were infected with either Cryptosporidium sp. or Giardia sp. The presence of Cryptosporidium and Giardia species in primates living in forest fragments, but not in primates in undisturbed forest, suggests that habitat disturbance may play a role in transmission or persistence of these pathogens.     

Time Constraints Do Not Limit Group Size in Arboreal Guenons but Do Explain Community Size and Distribution Patterns

To understand how species will respond to environmental changes, it is important to know how those changes will affect the ecological stress that animals experience. Time constraints can be used as indicators of ecological stress. Here we test whether time constraints can help us understand group sizes, distribution patterns, and community sizes of forest guenons (Cercopithecus/Allochrocebus). Forest guenons typically live in small to medium sized one-male–multifemale groups and often live in communities with multiple forest guenon species. We developed a time-budget model using published data on time budgets, diets, body sizes, climate, and group sizes to predict maximum ecologically tolerable group and community sizes of forest guenons across 202 sub-Saharan African locations. The model correctly predicted presence/absence at 83% of these locations. Feeding-foraging time (an indicator of competition) limited group sizes, while resting and moving time constraints shaped guenon biogeography. Predicted group sizes were greater than observed group sizes but comparable to community sizes, suggesting community sizes are set by competition among guenon individuals irrespective of species. We conclude that time constraints and intraspecific competition are unlikely to be the main determinants of relatively small group sizes in forest guenons. Body mass was negatively correlated with moving time, which may give larger bodied species an advantage over smaller bodied species under future conditions when greater fragmentation of forests is likely to lead to increased moving time. Resting time heavily depended on leaf consumption and is likely to increase under future climatic conditions when leaf quality is expected to decrease.     

Better to Live with Allogenerics Than to Live Alone? The Case of Single Male Cercopithecus pogonias in Troops of Colobus satanas

We report the integration of single male crowned guenons (Cercopithecus pogonias) into troops of black colobus (Colobus satanas). We observed one male Cercopithecus pogonias in three troops of Colobus satanas on 30% of observation days (n = 231). Activities of single males guenons did not differ significantly from those of the colobus with which they associated. Moreover, both species performed simultaneously the same activities more often than expected by chance. Interspecific grooming occurred on several occasions. Furthermore, single male guenons spent as much in time social activities when part of a colobus troop, as they typically do when part of a conspecific group. Unlike solitary male crowned guenons, which are silent, a male that is integrated into a troop of colobus is vocal and emits social alarm calls to which colobus monkeys respond. During the single file movements of colobus troops, single male crowned guenons were integrated in the core of the troop and used the same branches at the same height with the colobus. Thus, the life of a single male crowned guenon with black colobus was social. We suggest that the main benefits that he gained is the possibility to live in a social context. Social interactions could be the key element to explain why single males Cercopithecus pogonias join troops of monkeys so different from their natal groups.     

Ecology of the Zanzibar Red Colobus Monkey: Demographic Variability and Habitat Stability

We examined the Zanzibar red colobus' (Procolobus kirkii) social structure and population dynamics in relation to the density, diversity and dispersion of food resources in ground-water forest and agricultural land, which we characterized in terms of red colobus food species density, diversity, basal area and dispersion. We used transect sampling and group follows to describe population dynamics and social systems. Two agricultural areas, SJF Shamba and Pete Village, had higher densities and more uniformly dispersed red colobus food tree species than those of the ground-water forest. Red colobus at these two sites had greater population densities and natality, and smaller home ranges than red colobus in the ground-water forest. However, these findings apply to a very small area of agricultural land (approximately 18 ha) that is contiguous with an area of the forest reserve having a high density of red colobus. It is not representative of agricultural areas elsewhere on Zanzibar which support much lower densities or no red colobus. Although agricultural areas contiguous with the forest reserve had high densities of red colobus, they appear to be very unstable. Within the agricultural areas, we observed higher intergroup variation in group size and composition, study groups that decreased dramatically in size and disappeared from the study site, significantly lower levels of juvenile recruitment, and red colobus food trees that exhibited definite signs of overbrowsing. This apparent instability in the subpopulation of red colobus utilizing agricultural systems probably reflects the lower basal area of food trees and the greater fragmentation of suitable habitat and floristic dynamics due to human activities in these areas. A fusion-fission social system occurred only in the ground-water forest subpopulation, which we hypothesize to be due to highly clumped food resources.     

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.     

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.     

Red-Tailed Guenons (Cercopithecus ascanius) and Strychnos mitis: Evidence for Plant Benefits Beyond Seed Dispersal

I report data collected on red-tailed guenon (Cercopithecus ascanius schmidti) fruit processing behaviors between June 1993 and April 1994. Red-tailed guenons consumed the fruit of Strychnos mitis in 542 of 2,930 fruit-eating events (FEEs). The monkeys spat out cleaned seeds of Strychnos mitis in a majority of these records (477/542; 88%); seeds were occasionally swallowed whole, but only when pulp was unripe (69/542; 12%). In 83% of the FEEs on Strychnos, the red-tailed guenons spat out seeds within 10 m of the removal site; they typically stayed in the same tree while processing fruit, and in 56% of the FEEs, they moved <1 m before spitting seeds. I monitored spat seeds to evaluate the impact of monkey fruit processing on seed fate. Results indicate that 83% of seeds spat out by the red-tailed guenons germinated, while only 12% of unprocessed seeds survived to germination (p < 0.01). Of the processed seeds that germinated, 60% survived to germination and seedling establishment, while only 5% of unprocessed seeds survived to seedling establishment (p < 0.01). Unprocessed seeds were also more likely to be attacked by seed predators (p < 0.01) and fungus (p < 0.01). Although there is generally high mortality in seeds/seedlings, mature trees of Strychnos mitis are found in groves of adults, under which dense populations of seedlings and saplings can occur. These data suggest that Strychnos mitis does not conform to expectations of the Janzen-Connell model of seed escape from parent trees. Instead, I suggest that by removing pulp, a process that results in a reduction of fungal pathogen attack, red-tailed guenons positively effect the seed survivorship of Strychnos mitis. Although this effect has been observed in pulp-cleaning ant species, it is a hitherto undescribed effect of primates on their fruit resources.     

Species,age and sex differences in type and frequencies of injuries and impairments among four arboreal primate species in Kibale National Park,Uganda

Animals in the wild often have physical impairments that can affect their fitness. The aim of this study was to compare injuries and impairments of four different primate species (black-and-white colobus, red colobus, red-tailed monkeys, and grey-cheeked mangabeys) living in Kibale National Park (Uganda), and estimate the proportion of injured and impaired individuals among the sexes and age classes. The species differed in the proportion of individuals with injuries and impairments, with 16.7% in black-and-white colobus, 23.1% in red colobus, 16.2% in red-tailed monkey and 30.2% in grey-cheeked mangabeys. Species also differed in the types and location on the body of injuries. Adult animals had more injuries than immatures. Males had more injuries than females, in all but red-tailed monkeys. The results are discussed in relation to the literature on aggressive behavior, locomotion, and predation in these species.     

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.     

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

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

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.     

Variation in guenon skulls (I): species divergence, ecological and genetic differences

Guenons are the most diverse clade of African monkeys. They have varied ecologies, include arboreal and terrestrial species, and can be found in nearly every region of sub-Saharan Africa. Species boundaries are often uncertain, with a variable number of species and subspecies mostly recognised on the basis of their geographic distribution and pelage. If guenon soft tissue patterns show high variability, the same does not seem to hold for skull morphology. Guenon skulls are traditionally considered relatively undifferentiated and homogeneous. However, patterns of variation in skulls have never been examined using a large number of specimens sampled across the breadth of species diversity. Thus, in the present study, skulls of adult guenons and two outgroup species are analysed using three-dimensional geometric morphometrics. Three-dimensional coordinates of 86 anatomical landmarks were measured on 1,315 adult specimens belonging to all living guenon species except Cercopithecus dryas. Species are well-discriminated using shape but the best discrimination occurs when species have either a long evolutionary history (e.g., Allenopithecus nigroviridis) or represent extremes of size variation (Miopithecus sp. and Erythrocebus patas). Interspecific phenetic relationships reflect size differences. Four main clusters are found that mainly correspond to four size groups: the smallest species (Miopithecus sp.), the largest species (E. patas plus the study outgroups), a group of medium-small arboreal guenons, and a group of medium-large arboreal and terrestrial guenons. Correlations between interspecific shape distances and interspecific differences in size are higher than between shape distances and genetic distances. However, if only the component of interspecific shape variation which is not correlated to evolutionary allometry is used in the comparison with genetic distances, correlations are up to 1.4 times larger than those including allometric shape. The smallest correlations are those between shape and ecological distances, which is consistent with the lack of clusters clearly reflecting broad ecological specialisations (e.g., arboreality versus terrestriality). Thus, size, which is generally considered more evolutionarily labile than shape, seems to have played a major role in the evolution of the guenons. The incongruence between interspecific shape differences and phylogeny might be explained by a large proportion of shape changes having occurred along allometric trajectories that tend to be conserved within this clade.     

Demographic Variation Among Udzungwa Red Colobus in Relation to Gross Ecological and Sociological Parameters

We evaluated variation in group size and composition of Udzungwa red colobus (Procolobus gordonorum) in relation to gross-habitat and sociological parameters. The endangered species is endemic to the Udzungwa Mountains and nearby forests in the Kilombero Valley of south-central Tanzania. We counted 63 groups in 10 forests, ranging in altitude from 250 to 1,800 m. Group size ranged from 7 to 83 (x = 36.3) individuals and adult sex ratios (females/male) ranged from 1.5 to 7.3 (x = 3.5), excluding solitary individuals. Group size was influenced by several habitat parameters, including tree density, degree of deciduousness, and forest size. Groups were largest in large blocks of mature, moist, mixed evergreen and semideciduous forests, but group size is not correlated with altitude. Groups in a highly degraded forest appeared to have fission-fusion societies. The effect of habitat quality on age-sex composition of groups was most apparent in natality and less so in survivorship of adult females and juveniles. The number of adult males in groups accounted for 50% of the variance in group size and 34–39% of the variance in numbers of adult females in groups. Habitat quality affects natality more than demographic parameters do. Groups with a low proportion of adult females had greater juvenile survivorship, perhaps because of lower food competition between these two classes. We proffer hypotheses based on our study and previous intertaxonal comparisons to explain cause and effect relationships between habitat quality and demography. Finally, our study demonstrates the importance of large blocks of old-growth forest to the conservation of Udzungwa red colobus, and we make recommendations for conservation and research.     

Ecological Partitioning of Cercopithecus campbelli, C. petaurista, and C. diana in the Taï Forest

I determined the degree of ecological partitioning among 3 species of guenons (Cercopithecus campbelli, C. petaurista, and C. diana) in the Taï Forest, Côte d’Ivoire and used the partitioning data to understand competitive relationships among them. Over a 13-mo period, I measured ecological partitioning in terms of food and canopy stratum use for 2 habituated groups of each guenon species and also collected data on food availability. I found that the study species diverged primarily in food items consumed and vertical strata occupied. Cercopithecus petaurista ate much more foliage than the other species did and used mostly the middle strata (5–20 m). Cercopithecus diana ate primarily fruit and used mostly the upper strata (>20 m). Cercopithecus campbelli ate mostly fruit together with large amounts of animal matter and primarily occupied the ground and low strata (<5 m). Of the specific pairs, the diets of Cercopithecus campbelli/C. diana overlapped the most overall and decreased during the season of low fruit availability. Cercopithecus campbelli and C. diana age/sex classes also overlapped more than the age/sex classes of other species pairs. The results suggest that the potential for competition was more intense for Cercopithecus campbelli/C.diana relations than it is for other species pairs. I compare my results from Taï with those from other primate and guenon communities and demonstrate that dietary overlaps and seasonal dietary divergence are lower in Taï than in most other guenon communities.     

Seminomadic Ranging in a Population of Black Colobus (Colobus satanas) in Gabon and its Ecological Correlates

We observed ranging patterns in a black colobus population in the Forêt des Abeilles, Central Gabon. We compared the results with those for two other populations (Lopé Reserve in Central Gabon, Douala-Edéa in coastal Cameroun) in order to estimate the extent of specific variability in population structure and ranging behavior and to identify ecological factors influencing interpopulation differences. The mean number of monkeys in a group is 17, and all groups had a multimale structure. Home ranges were large, and the fact that they continued to increase with increasing number of observations indicated that the monkeys did not frequently resample their habitat. Ranging patterns varied according to the staple food consumed: distances travelled daily increased with increasing seed intake and decreased with increasing leaf intake. The ranging patterns of groups of Colobus satanas are seminomadic. Up to 6 or 7 groups shared the same space, and two group ranges could overlap by as much as 65–75%. Comparisons with the two populations previously studied showed that group size and group structure are broadly similar. At all three sites, black colobus were mainly seed eaters and ate large amounts of leaves in the season of fruit shortage. In the Forêt des Abeilles, however, group home ranges were much larger than at other sites, and this population had the lowest density. This is correlated with vegetation composition and with harshness of the main dry season. This colobus population appears limited by both recurring food shortage in the dry season and episodic periods of seed shortage resulting from irregular fruiting of the dominant family Caesalpiniaceae. Their seminomadic ranging would constitute the least costly strategy to cope with the low carrying capacity of their habitat.     

Competing pressures on populations: long-term dynamics of food availability,food quality,disease, stress and animal abundance

Despite strong links between sociality and fitness that ultimately affect the size of animal populations, the particular social and ecological factors that lead to endangerment are not well understood. Here, we synthesize approximately 25 years of data and present new analyses that highlight dynamics in forest composition, food availability, the nutritional quality of food, disease, physiological stress and population size of endangered folivorous red colobus monkeys (Procolobus rufomitratus). There is a decline in the quality of leaves 15 and 30 years following two previous studies in an undisturbed area of forest. The consumption of a low-quality diet in one month was associated with higher glucocorticoid levels in the subsequent month and stress levels in groups living in degraded forest fragments where diet was poor was more than twice those in forest groups. In contrast, forest composition has changed and when red colobus food availability was weighted by the protein-to-fibre ratio, which we have shown positively predicts folivore biomass, there was an increase in the availability of high-quality trees. Despite these changing social and ecological factors, the abundance of red colobus has remained stable, possibly through a combination of increasing group size and behavioural flexibility.     

Patch depletion behavior differs between sympatric folivorous primates

Food competition in group-living animals is commonly accepted as a critical determinant of foraging strategies and social organization. Here we examine food patch depletion behavior in a leaf-eating (folivorous) primate, the guereza (Colobus guereza). Snaith and Chapman (2005) studied the sympatric folivorous red colobus (Procolobus rufomitratus), which shares many food resources with the guereza. They determined that red colobus deplete the patches (feeding trees) they use, while we found contrary evidence for guerezas using the same methods. We found that the time guerezas spent feeding in a patch was affected by neither tree size, an indicator of food abundance, nor the size of the feeding group, an indicator of feeding competition. For their principal food item (young leaves), intake rate remained constant and coincided with a decrease in the distance moved to find food within a patch, implying that guerezas do not deplete patches. This points to a fundamental difference in the use of food by guerezas and red colobus, which may be linked to the large difference in their group sizes and/or to a disparity in their digestive physiologies. However, further analyses revealed that the number of feeders within a patch did not affect patch depletion patterns in either species, leaving the potential for a physiological basis as the most plausible explanation. Our research highlights the need for a more critical examination of folivorous primate feeding ecology and social behavior, as all folivorous primates are typically lumped into a single category in socioecological models, which may account for conflicting evidence in the literature.