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.     

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.     

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.     

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.     

Monkey Abundance and Social Structure in Two High-Elevation Forest Reserves in the Udzungwa Mountains of Tanzania

The effects of human activity on population and social structure are a pantropical concern for primate conservation. We compare census data and social group counts from two forests in the Udzungwa Mountains, Tanzania. The main aim is to relate differences within and between the forests to current theory on the effect of human disturbance on primate abundance and group size. The survey reveals the presence of the restricted-range red colobus, Procolobus gordonorum, in New Dabaga/Ulangambi Forest Reserve (NDUFR). The primate community of NDUFR is impoverished compared to that in Ndundulu forest. Red colobus and black-and-white colobus (Colobus angolensis palliatus) abundance and group size are lowest in NDUFR. Fission-fusion of red colobus social groups may be occurring in previously logged areas of both forests. Our observations are consistent with current theory on the effect of habitat degradation and hunting on primates, but the relative effects of the 2 factors could not be differentiated. We pooled the results with previous data to show that abundance of red colobus in the Udzungwa Mountains is lowest at high elevations. Low red colobus group sizes appear to be related to human activity rather than elevation. Black-and-white colobus and Sykes monkeys (Cercopithecus mitis) show no relationship with elevation. Future studies will require more detailed information on vegetation, diet and ranging patterns to interpret fully intraspecific variation in population demography and social structure in the Udzungwa Mountains.     

Density Estimation of the Endangered Udzungwa Red Colobus (Procolobus gordonorum) and Other Arboreal Primates in the Udzungwa Mountains Using Systematic Distance Sampling

Estimates of population density and abundance are essential for the assessment of nonhuman primate conservation status, especially in view of increasing threats. We undertook the most extensive systematic primate survey yet of the Udzungwa Mountains of Tanzania, an outstanding region for primate endemism and conservation in Africa. We used distance sampling to survey three arboreal monkey species, including the endangered and endemic Udzungwa red colobus (Procolobus gordonorum). Overall, we encountered 306 primate clusters over 287 km walked along 162 line transects. We found the lowest cluster densities for both red colobus and Angolan colobus (Colobus angolensis; 0.8 clusters/km²) in the least protected forest (Uzungwa Scarp Forest Reserve, US), while we found the highest densities (3.2 and 2.6 clusters/km² for red colobus; 3.2 and 2.7 clusters/km²for Angolan colobus) in two large and protected forests in the national park. Unexpectedly, Magombera, a small forest surrounded by plantations, had the highest densities of red colobus (5.0 clusters/km²), most likely a saturation effect due to the rapid shrinking of the forest. In contrast, Sykes’ monkey (Cercopithecus mitis monoides/moloneyi) had more similar densities across forests (3.1–6.6 clusters/km²), including US, suggesting greater resilience to disturbance in this species. For the endemic red colobus monkey, we estimated an abundance of 45–50,000 individuals across all forests, representing ca. 80% of the global population. Though this is a relatively high abundance, the increasing threats in some of the Udzungwa forests are of continued concern for the long-term survival of red colobus and other primates in the area.     

Long-term dynamics of wild primate populations across forests with contrasting protection in Tanzania

Anthropogenic activities driving tropical forests' loss imperil global biodiversity and provision of ecosystem services. In this context, systematic monitoring programs evaluating wildlife trends are essential. Non-human primates are relevant conservation targets since they represent vital components of tropical forests by serving as pollinators and seed dispersers. Here, we present primate group counts data collected over 19 years in a primate hotspot in Tanzania. We analyzed data with a hierarchical dynamic model accounting for imperfect detection that estimates local group abundance and temporal rates of change, to assess whether habitat protection explained trends of the arboreal and diurnal Peters' Angola colobus (Colobus angolensis palliatus), Udzungwa red colobus (Piliocolobus gordonorum), and Tanzania Sykes' monkey (Cercopithecus mitis subsp. moloneyi). We targeted populations occurring in two forest blocks with contrasting protection regimes, with one block impacted by targeted poaching of the two Colobus species. We found that these latter species were much less abundant in the more human impacted forest, underwent a rapid decline, and subsequently remained at low abundance and without signs of recovery once this forest was granted greater protection. Instead, Sykes' abundance did not differ between forests, and improved protection was associated with a slight increase in abundance. Age class composition for social groups of both Colobus species differed between forests, indicating altered births and survivorship rates in the impacted forest. Results suggest that targeted hunting can prevent recovery for several years and even after increased habitat protection. Our approach appears valuable to monitor population dynamics over the long term, highlighting species-specific variations in both vulnerability to anthropogenic disturbance and recovery patterns in primate populations.     

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.     

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.     

Parasitology of five primates in Mahale Mountains National Park, Tanzania

Parasitological surveillance in primates has been performed using coprological observation and identification of specimens from chimpanzees (Pan troglodytes schweinfurthii) in Mahale Mountains National Park, Tanzania (Mahale). In this study, we conducted coprological surveillance to identify the fauna of parasite infection in five primate species in Mahale: red colobus (Procolobus badius tephrosceles), red-tailed monkeys (Cercopithecus ascanius schmidti), vervet monkeys (Cercopithecus aethiops pygerythrus), yellow baboons (Papio cynocephalus), and chimpanzees. Fecal samples were examined microscopically, and parasite identification was based on the morphology of cysts, eggs, larvae, and adult worms. Three nematodes (Oesophagostomum spp., Strongyloides sp., and Trichuris sp.), Entamoeba coli, and Entamoeba spp. were found in all five primate species. The following infections were identified: Bertiella studeri was found in chimpanzees and yellow baboons; Balantidium coli was found in yellow baboons; three nematodes (Streptopharagus, Primasubulura, an undetermined genus of Spirurina) and Dicrocoeliidae gen. sp. were found in red-tailed monkeys, vervet monkeys, and yellow baboons; Chitwoodspirura sp. was newly identified in red colobus and red-tailed monkeys; Probstmayria gombensis and Troglocorys cava were newly identified in chimpanzees, together with Troglodytella abrassarti; and Enterobius sp. was newly identified in red colobus. The parasitological data reported for red colobus, vervet monkeys, and yellow baboons in Mahale are the first reports for these species.     

Primate population dynamics: variation in abundance over space and time

The rapid disappearance of tropical forests, the potential impacts of climate change, and the increasing threats of bushmeat hunting to wildlife, makes it imperative that we understand wildlife population dynamics. With long-lived animals this requires extensive, long-term data, but such data is often lacking. Here we present longitudinal data documenting changes in primate abundance over 45 years at eight sites in Kibale National Park, Uganda. Complex patterns of change in primate abundance were dependent on site, sampling year, and species, but all species, except blue monkeys, colonized regenerating forest, indicating that park-wide populations are increasing. At two paired sites, we found that while the primate populations in the regenerating forests had increased from nothing to a substantial size, there was little evidence of a decline in the source populations in old-growth forest, with the possible exception of mangabeys at one of the paired sites. Censuses conducted in logged forest since 1970 demonstrated that for all species, except black-and-white colobus, the encounter rate was higher in the old-growth and lightly-logged forest than in heavily-logged forest. Black-and-white colobus generally showed the opposite trend and were most common in the heavily-logged forest in all but the first year of monitoring after logging, when they were most common in the lightly-logged forest. Overall, except for blue monkey populations which are declining, primate populations in Kibale National Park are growing; in fact the endangered red colobus populations have an annual growth rate of 3%. These finding present a positive conservation message and indicate that the Uganda Wildlife Authority is being effective in managing its biodiversity; however, with constant poaching pressure and changes such as the exponential growth of elephant populations that could cause forest degradation, continued monitoring and modification of conservation plans are needed.     

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.     

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.     

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.     

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.     

Dyadic associations of red Colobus and diana monkey groups in the Taï National Park, Ivory Coast

Members of the genus Colobus have been observed to associate frequently with Cercopithecus monkeys in several African sites. In the Taï National Park, Ivory Coast, one group of western red colobus was found to be in association with one particular group of diana monkeys more than could be expected by chance (Holenweg et al., 1996). We show that dyadic association is not an idiosyncrasy of these two groups, but rather a pattern that is general for our study site. All five red colobus groups we studied were closely associated with diana monkeys during more than 60% of the time. Four groups had one particular diana partner group, the fifth two different partners. Apart from the red colobus, three more primate species, the olive colobus, Campbell's monkey, and the lesser spot-nosed monkey, were also strongly attracted to diana monkeys.     

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.     

Interspecific interaction of the primate groups in Kibale Forest,Uganda

An ecological survey on the influence of interspecific interaction of the primates upon the distribution of their group ranges was carried out in 100 ha of the isolated forest northern outskirts of Kibale Forest in western Uganda, Africa. The study period of 105 days was from the 12th of November, 1970 to the 24th of February, 1971, including a preliminary survey of about two months. The subjects of this study are five species of primates, i.e., black and white colobus (Colobus polykomos), red colobus (Colobus badius), red tailed monkey (Cercopithecus ascanius), blue monkey (Cercopithecus mitis), and vervet monkey (Cercopithecus aethiops), which inhabited the study area. The red colobus group is thought to be the most influential of the five in the interspecific interaction.     

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.     

Forest Age Influences In-stream Ecosystem Processes in Northeastern US

A disturbance or natural event in forested streams that alter available light can have potential consequences for nutrient dynamics and primary producers in streams. In this study, we address how functional processes (primary production and nutrient uptake) in stream ecosystems respond to changes in forest canopy structure. We focus on differences in incoming irradiance, nutrient uptake (NO₃, NH₄, and PO₄) and open-channel metabolism seasonally in 13 forested streams that drain forests with different canopy structures (10 to >300 years old) in the northeastern United States. Light irradiance was related to forest age in a U-shaped pattern, with light being the greatest in both young open forests (<50 years old) and older growth forests (>245 years old), whereas the darkest conditions were found in the secondary growth middle-aged forests (80–158 years old). Streams that had adjacent open or old-growth riparian forest had similar conditions with greater standing stock biofilm biomass (chl a), and elevated ER in October compared to streams with middle-aged riparian forests. Compared to all sites, streams with old-growth riparian forest had the greatest in-stream primary production rates (GPP) and elevated background nutrient concentrations, and to a lesser degree, increased nutrient retention and uptake (V _f). Streams draining older forests tended to be more productive and retentive than middle-aged forests, likely due to increased light availability and the age and structure of surrounding forest canopies. Middle-aged forests had the least variation in response variables compared to streams in young and old-growth riparian forests, likely a result of uniform canopy conditions. As the structure of widespread middle-aged forests in NE US is altered by loss of specific tree species, climate change, and/or human activity, it will impact in-stream production and nutrient dynamics and may ultimately alter nutrient loading in downstream catchments.