Association of Terrestrial Mangabeys (Cercocebus atys) with Arboreal Monkeys: Experimental Evidence for the Effects of Reduced Ground Predator Pressure on Habitat Use

We examined the behavior of two arboreal monkeys—Piliocolobus badius (western red colobus) and Cercopithecus diana (Diana monkey)—in the presence and absence of a third, predominately terrestrial monkey, Cercocebus atys (sooty mangabey) in the Ivory Coast's Taï Forest. Via experimental data, we show that sooty mangabeys are effective sentinels for ground predators. Then we compared strata use of red colobus and Diana monkeys in the presence and absence of mangabeys. Our data indicate that red colobus and Diana monkeys descend to low forest levels and to the forest floor significantly more often when mangabeys are spatially intermingled with them, i.e. in polyspecific associations. The niche extension may provide some foraging advantage, especially for red colobus. We identified the specific causal agent—relaxed ground predator pressure—of a temporary shift in habitat use. In this instance, the presence of one species (Cercocebus atys) leads to the temporary expansion of a niche normally avoided by others Piliocolobus badius and Cercopithecus diana.     

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.     

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.     

Primate census and habitat evaluation in the Tana delta region, Kenya

Nineteen indigenous forest patches in the Tana River delta region, Kenya were surveyed between October and November 2000 for primates and habitat disturbance. Special emphasis was placed on the endangered Tana River red colobus (Procolobus rufomitratus Peters) and crested mangabeys (Cercocebus galeritus galeritus Peters), both of which are endemic to the region. Habitat disturbances evident in the forests included cutting of trees, harvesting of thatching material, firewood collection, dyke construction, cultivation, palm wine tapping and charcoal burning. A total of 85 groups of five primate species were counted. These comprised eighteen, ten, 22, 31 and four groups of red colobus, crested mangabey, baboons (Papio cynocephalus L.), sykes monkeys (Cercopithecus mitis Wolf) and vervet monkeys (Cercopithecus aethiops L.), respectively. A wider distribution of red colobus and crested mangabeys than was documented previously was noted, implying that they are probably more abundant than hitherto reported. It is hypothesized that extensive studies on some fauna considered endangered world‐wide would probably redefine their conservation status. Future studies in the lower Tana River region should cover the previously unsurveyed forests and focus on ways of curbing forest destruction.     

Impact of Commercial Hunting on Monkey Populations in the Taï region,Côte d'Ivoire1

We studied the impact of hunting on monkey species in the Taï National Park and adjacent forests in Côte d'Ivoire. The average wild meat consumption per capita per year was assessed from market surveys and interviews. We determined that the amount of primate wild meat being extracted in the Taï National Park and surrounding forests was 249 t in 1999. Hunting pressure was the highest on the larger primate species such as red colobus, Procolobus badius, black and white colobus, Colobus polykomos, and the sooty mangabey, Cercocebus torquatus atys. Estimates of population densities were based on line transect surveys. The maximum annual production of each species was calculated using the Robinson and Redford model (1991) and assuming unhunted conditions. Comparing current harvest levels with the maximum sustainable yield suggests that harvest of red colobus monkeys (Procolobus badius) is sustainable, whereas current off‐take of the black and white colobus (Colobus polykomos), the sooty mangabey (Cercocebus atys), diana monkeys (Cercopithecus diana), and Campbell's monkeys (Cercopithecus campbelli) exceeds sustainability by up to three times.     

Sooty mangabeys scavenge on nuts cracked by chimpanzees and red river hogs—An investigation of inter‐specific interactions around tropical nut trees

Carrion scavenging is a well‐studied phenomenon, but virtually nothing is known about scavenging on plant material, especially on remnants of cracked nuts. Just like meat, the insides of hard‐shelled nuts are high in energetic value, and both foods are difficult to acquire. In the Taï forest, chimpanzees (Pan troglodytes) and red river hogs (Potamochoerus porcus) crack nuts by using tools or strong jaws, respectively. In this study, previously collected non‐invasive camera trap data were used to investigate scavenging by sooty mangabeys (Cercocebus atys), two species of Guinea fowl (Agelestres meleagrides; Guttera verreauxi), and squirrels (Scrunidae spp.) on the nut remnants cracked by chimpanzees and red river hogs. We investigated how scavengers located nut remnants, by analyzing their visiting behavior in relation to known nut‐cracking events. Furthermore, since mangabeys are infrequently preyed upon by chimpanzees, we investigated whether they perceive an increase in predation risk when approaching nut remnants. In total, 190 nut‐cracking events were observed in four different areas of Taï National Park, Ivory Coast. We could confirm that mangabeys scavenged on the nuts cracked by chimpanzees and hogs and that this enabled them to access food source that would not be accessible otherwise. We furthermore found that mangabeys, but not the other species, were more likely to visit nut‐cracking sites after nut‐cracking activities than before, and discuss the potential strategies that the monkeys could have used to locate nut remnants. In addition, mangabeys showed elevated levels of vigilance at the chimpanzee nut‐cracking sites compared with other foraging sites, suggesting that they perceived elevated danger at these sites. Scavenging on remnants of cracked nuts is a hitherto understudied type of foraging behavior that could be widespread in nature and increases the complexity of community ecology in tropical rainforests.     

Primate surveys in Côte d'Ivoire's Sassandra–Bandama interfluvial region with notes on a remnant population of black‐and‐white colobus

We conducted surveys in Côte d'Ivoire's Bandama–Sassandra interfluvial region to assess the abundance of primates and investigate further a population of black‐and‐white colobus monkey whose taxonomic position has been debated. Primates were encountered in five of eight forests surveyed. The most common primates were Campbell's guenons and lesser spot nosed monkeys. Roloway monkeys were located in one reserve (Dassioko FR), sooty mangabeys in two (Dassioko and Port Gauthier FR) and olive colobus in three reserves (Dassioko, Port Gauthier, Bakadou) as well as one forest patch was considered a sacred grove (Grébouo I FG). Red colobus and chimpanzees were never observed. The only black‐and‐white colobus encountered were located in a forest adjacent to the Grébouo I village. The coat of this population is similar to that of Colobus vellerosus; however, vocal data are more complex. In one vocal attribute, the Grébouo I colobus is similar to Colobus polykomos while in another it is similar to C. vellerosus. We hope that by investigating the taxonomy of the Grébouo 1 colobus population, highlighting the conservation value of sacred forests and advocating for more active law enforcement in protected reserves, we can prevent the extirpation of all primates within the Bandama–Sassandra interfluvial zone region.     

Population Sizes and Distribution of Primates in the Lower Tana River Forests,Kenya

We studied the population size and distribution of diurnal primates in the lower Tana River forests, Kenya. They are the only remaining habitats for 2 threatened primates: the Tana River red colobus (Procolobus rufomitratus) and the Tana River crested mangabey (Cercocebus galeritus galeritus). We conducted censuses in 73 forest patches from January through March 2001. We estimate population size of the red colobus to be 788 individuals in 82 groups and that of the crested mangabeys to be 2,070 individuals in 59 groups. The data suggest that over a 7-year period (1994-2001), there was an 18% increase in the crested mangabey population and a 5% decline in red colobus numbers. Further, the red colobus range has expanded both north and south, whereas that of crested mangabeys has only expanded south. Fifty-six percent of crested mangabeys and 46% of red colobus groups were inside the Tana River Primate National Reserve (TRPNR). Other primates encountered included 170 groups of Sykes' monkeys (Cercopithecus mitis), 70 groups of yellow baboons (Papio cynocephalus) and 4 groups of grivets [Chlorocebus (Cercopithecus) aethiops]. Mean group densities of the 2 endangered primates and of baboons were higher inside than outside the TRPNR, reinforcing the importance of TRPNR for their conservation. An intervention program is required to stem further decline in the red colobus population and to protect small isolated groups in forest patches outside TRPNR.     

Female rank instability in newly formed groups of familiar sooty mangabeys (Cercocebus torquatus atys)

The formation of two new groups of sooty mangabeys (N=6; N=11) comprised of individuals removed from their natal group of 98 animals led to dominance rank challenges with aggression and wounding, though this occurred after an interval of months. Dominance rank challenges were not expected because, unlike rhesus macaques, adult female sooty mangabeys do not affiliate with adult kin significantly more than nonkin and show minimal agonistic aiding even with adult kin, thus rank would seem to be independent of aiding. Moreover, during the last nine years, severe wounding of adults in a large stable group of sooty mangabeys has been virtually absent and agonistic behavior in a stable group of sooty mangabeys is exhibited at a low rate compared to some macaque species. New members in the group of six maintained their relative ranks for 12 weeks after which the beta supplanted the alpha female with no serious wounding. This ranking remained stable for 29 weeks after which the alpha and beta females were supplanted with fatal wounds inflicted to the alpha and less severe wounds to the beta female. The second subgroup also kept their relative ranks initially. However, after 27 weeks the lowest ranking female severely wounded the next to last ranking female and 1 week later attacked and displaced the alpha female with minimal wounding. Fourteen weeks later the beta female (formerly the alpha) attacked and severely wounded the new alpha female and regained the top dominance position. These events suggest that although sooty mangabeys do not exhibit strong kin preferential behavior among adults, they do have defined relationships within the long term, stable group. Removal from those defined relationships allows the possibility of social reorganization that may be mediated by serious aggression.     

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.     

Interspecific interactions between wild pygmy chimpanzees (Pan paniscus) and red colobus (Colobus badius)

Interspecific interactions accompanied by physical contacts between wild pygmy chimpanzees (Pan paniscus) and red colobus (Colobus badius) were observed on three occasions at Wamba, Republic of Zaire. In all cases, the red colobus initiated the interactions by approaching the pygmy chimpanzees. Most of the pygmy chimpanzees, which were within 5 m of the red colobus, were juveniles or infants but the adult male pygmy chimpanzees never showed any interest in the red colobus. The red colobus groomed the chimpanzees in two cases, but the latter never groomed the former. No true aggressive interactions were observed between the two species. The lack of any evidence of hunting of red colobus through longitudinal studies of the pygmy chimpanzees of Wamba, together with the present observations, suggests that red colobus are probably not targets of hunting by the pygmy chimpanzees.     

Market Hunting in the Taï Region,Côte d’Ivoire and Implications for Monkey Populations

We studied the effect of market hunting on primate species in the Taï National Park and adjacent forests in Côte d’Ivoire. We assessed the impact of hunting by comparing the calculated maximal reproduction rate with the current off-take rate. We assessed the average bushmeat consumption per capita/per year from weekly investigations on bushmeat available in 88 bushmeat restaurants and markets over a 12-mo period in 1999. We derived data on preferences for particular game species from interviews of 162 bushmeat consumers, 25 subsistence hunters and 3 groups of professional hunters. Hunting pressure was highest on the larger primate species such red colobus (Procolobus badius), black- and- white colobus (Colobus polykomos) and sooty mangabeys (Cercocebus atys). The amount of primate bushmeat extracted from the Taï National Park and surrounding forests was 249,229 kg in 1999. We estimated population densities using line transect surveys. By referring to current population densities we calculated the maximum production of each species using the Robinson Redford model (2001) and assuming unhunted conditions. A comparison of current harvest levels with maximum production suggests that harvest of Procolobus badius is sustainable, whereas current off-take of Colobus polykomos, Cercocebus atys, Cercopithecus diana (diana monkey) and C. campbelli (Campbell’s monkeys) exceeds sustainability by ≤3 times. We recommend that wildlife managers promote programs that encourage the production of domestic animals as a substitute for wild meat.     

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.     

Gastrointestinal parasites of critically endangered primates endemic to Tana River, Kenya: Tana River red colobus (Procolobus rufomitratus) and crested mangabey (Cercocebus galeritus)

We conducted fecal egg counts of gastrointestinal parasites of 2 critically endangered primates endemic to the forest of Tana River, Kenya. We aimed to use the fecal egg counts as proxies to quantify the prevalence of gastrointestinal parasites between the 2 primates. The Tana River red colobus (Procolobus rufomitratus) and crested mangabey (Cercocebus galeritus) are of similar body size, but their behavioral ecology is very different. We predicted that mangabeys would have a higher prevalence of parasites because they are mostly terrestrial omnivores, live in larger social groups, and therefore range widely. We detected 10 nematodes and 3 protozoans in mangabeys and 7 nematodes and 2 protozoans in colobus. We detected a higher number of different parasite species in individual mangabeys, and 4 of the 5 nematodes requiring intermediate hosts were found in mangabeys. The overall prevalence of parasites was higher for mangabeys, but this difference was not statistically significant. For colobus, we found a trend whereby the number of different parasite species in individual monkeys was higher in males and in lactating females. However, there was no difference in the prevalence of parasites between the sexes or between lactating and nonlactating females.     

Flow microfluorometric analysis of peripheral blood mononuclear cells from nonhuman primates: Correlation of phenotype with immune function

A panel of monoclonal antibody reagents has been identified that can be used for routine monitoring of subsets of peripheral blood mononuclear cells (PBMC) from Macaca mulatta (rhesus macaques), Macaca nemestrina (pig-tailed macaques), and Cercocebus atys (sooty mangabeys). The procedure uses fluorescein and phycoerythrin conjugates of the monoclonal antibodies in appropriate combinations, so that two-color microfluorometric analyses can be readily performed on as little as 1.2 ml of EDTA blood. PBMC from a total of 20 normal adult rhesus macaques, 21 normal adult pig-tailed macaques, 4 SIV^? sooty mangabeys, and 16 SIV⁺ adult sooty mangabeys were analyzed with the panel of monoclonal reagents and flow microfluorometry. The mean frequency, absolute numbers, and range for each subset in these nonhuman primate species are described. Sooty mangabeys appeared markedly different from the other two primate species. The PBMCs from the mangabeys had a higher mean frequency and absolute number of total T cells, Leu-3a⁺/18^? T cells, suppressor (Leu?2a⁺) T cells, which were HLA-DR⁺, and IL-2R⁺ cells. Functional helper, suppressor, natural killer (NK), lymphokine activated killer (LAK), and antigen-presenting cell studies were also performed to correlate phenotype with immune function. Data indicate that Leu?3a⁺ T cells (CD4⁺) and Leu?2a⁺ T cells (CD8⁺) in these primate species represent human equivalents of helper and suppressor T cells, respectively. NK and LAK effector cells in the rhesus and pig-tailed macaques appear to be predominantly Leu?19⁺. In contrast, Leu?2a⁺ cells appear to be the predominant NK and LAK effector cell in sooty mangabeys. These data provide a basis for routine evaluation of lymphocyte subsets in these nonhuman primate species, and provide a means to correlate phenotype with immune function.     

Identification of multiple simian immunodeficiency virus (SIV)-specific CTL epitopes in sooty mangabeys with natural and experimentally acquired SIV infection

Host immune responses to SIV infection in sooty mangabeys are likely to be an important determinant of how such nonhuman primate species maintain asymptomatic lentivirus infection. We have previously described two patterns of asymptomatic SIV infection in sooty mangabeys: low viral loads with vigorous SIV-specific CTL activity in SIVmac239-infected sooty mangabeys, and high viral loads with generally weak or absent SIV-specific CTL activity in naturally infected sooty mangabeys. To define the specificity of the CTL response in SIV-infected mangabeys, we characterized CTL epitopes in two naturally infected and three SIVmac239-infected sooty mangabeys. Compared with that in SIVmac239-infected mangabeys, the yield of SIV-specific CTL clones was significantly lower in naturally infected sooty mangabeys. All CTL clones were phenotypically CD3+ CD8+, and lysis was MHC restricted. Seven SIV CTL epitopes were identified in five sooty mangabeys: one in Gag and three each in Nef and Envelope (Env). The CTL epitopes mapped to conserved regions in the SIV genome and were immunodominant. Several similar or identical CTL epitopes were recognized by both naturally infected and SIVmac239-infected mangabeys that shared class I MHC alleles. To our knowledge, this is the first report of SIV-specific CTL epitopes in sooty mangabeys. Longitudinal studies of viral load and sequence variation in CTL epitopes may provide useful information on the role of CTL in control or persistence of SIV infection in sooty mangabeys.     

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.     

Familiarity and dominance relations among female sooty mangabeys in the Taï National Park

Dominance relationships of female sooty mangabeys have thus far been studied exclusively in captive groups. In captivity, adult females form a stable linear hierarchy as would be expected in species exhibiting strong contest competition. However, the same individuals do not exhibit other aspects of behavior that would be expected where contest competition occurs. For example, they show no kin‐based alliances leading to hierarchies in which the members of each matriline occupy adjacent ranks. The goal of this study was to provide the first data on dominance relationships of sooty mangabey females in their natural environment in the Taï National Park, Ivory Coast. In our study group, adult females formed a linear dominance hierarchy. Aggression over food increased in food patches, as would be expected for species that experience contest competition. Moreover, females formed highly differentiated social relationships, showing particular affinities with females of adjacent rank. Am. J. Primatol. 56:137–153, 2002. © 2002 Wiley‐Liss, Inc.     

A brief report on the social behavior of the crested mangabey (Cercocebus galeritus galeritus) with a comparison to the sooty mangabey (C. torquatus atys)

A group of 38 free ranging crested mangabeys in the Tana River Primate Reserve was studied over a 6-week period for a total of 209.5 hr and behavioral comparisons made to a captive group of sooty mangabeys. Although quantitative comparisons between these two mangabey species are not possible, the present data suggest that these geographically separated mangabeys share several behavioral similarities. Copulatory behavior in both species involved a pattern of female darting and female vocalizing following the mount by the male. Several similarities in agonistic behavior also existed: 1) The victim often returned or stayed within 1 m of the aggressor following an agonistic episode; 2) retaliation in which the victim first fled or avoided the aggressor, then subsequently, chased or lunged at the aggressor, typically while screaming; and 3) frequent redirection of aggression by the victim following an agonistic episode. A dominance rank reversal occurred between the two adult male crested mangabeys with no severe wounding. The rank reversal seemed to be related to two subsequent behaviors which included infant carriage by the deposed alpha in the presence of the new alpha male and female demonstrations of extreme protectiveness of their infants in the presence of the new alpha male. Both of these behaviors have been reported in the sooty mangabey group.