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.     

Changes in forest fragment sizes and primate population trends along the River Tana floodplain, Kenya

The Tana River forest patches significantly decreased in total area by 1875 ha (34.5%), from 5439 to 3564 ha between 1979 and 2000. The area covered by forests outside the Tana River Primate National Reserve declined by 1246 ha (38%) from 3283 to 2037 ha. This loss was higher than that inside the reserve, where total forest area reduced by 629 ha (29%) from 2156 to 1527 ha. The numbers of Tana River red colobus (Procolobus rufomitratus) and Tana crested mangabey (Cercocebus galeritus galeritus) groups were significantly correlated with forest sizes suggesting that both red colobus and crested mangabeys are likely to be affected by forest loss and fragmentation. However, comparison of the 1974/75 and 2001 census data did not reveal any significant change in the number of groups of either the red colobus or crested mangabey. The two endangered primates may have developed strategies to cope with a shrinking habitat.     

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.     

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.     

Common use of sleeping sites by two primate species in Tana River, Kenya

Choice of sleeping sites by two species of primates sharing two adjacent patches of gallery forest in Tana River, Kenya, was studied between August 1992 and February 1993. One group each of the Tana crested mangabey, Cercocebus galeritus galeritus Peters, and yellow baboon, Papio cynocephalus cynocephalus L., interchangeably shared nine sleeping sites distributed among four tree species, Acacia robusta Burch., Ficus sycomorus L., Abizzia gummifera (J. F. Gmel.) E. A. Sm. and Pachystela msolo (Engl.) Engl. The trees used by both species as sleeping sites were mainly tall trees with canopy level or emergent crowns. The trees had relatively larger crowns and lower percentage canopy cover compared to other trees at the site and were characterized by poor to moderate accessibility. Overlap in use of sleeping sites was never simultaneous and baboons occasionally supplanted mangabeys. Site choice by these two primates appeared to be influenced by predation risk, the feeding area used in the late afternoon, daily range and the availability of trees with the preferred structural characteristics. Sleeping sites appeared to be limited during and immediately after the wet season, when the frequency of supplantings increased. This observation is attributed to an increase in percentage canopy cover.     

Diet and habitat overlap in two sympatric primate species, the Tana crested mangabey Cercocebus galeritus and yellow baboon Papio cynocephalus

Diet and habitat overlap was studied in two sympatric primate species sharing two neighbouring patches of fragmented gallery forest in Tana River, Kenya. Systematic data on feeding and ranging behaviour was collected on one group each of the Tana crested mangabey Cercocebus galeritus and yellow baboon Papio cynocephalus between August 1992 and February 1993. When rainfall was low and fruit resources scarce, yellow baboons spent most of their foraging time in the open woodlands while mangabeys foraged within the forest. At this period, diet and habitat overlaps between the two species were low. As rainfall increased, followed by a gradual rise in fruit availability, yellow baboons shifted their foraging range and both species became confined to the forest habitat. Consequently, both diet and habitat overlaps increased, peaking at the end of the rainy season. Mangabeys showed a reduced within-group dispersal and also spent significantly less time foraging in a given forest patch when yellow baboons were also present within the same forest patch.
Increased habitat and diet overlaps during the wet season need not have resulted in increased interspecific competition for food because at this period, fruits were readily available in the forest.     

Comprehensive Conservation Profile of Tana Mangabeys

Forests along 60 kilometers of the lower Tana River, Kenya, provide habitat for one of the world’s top 25 most endangered primates, the Tana mangabey (Cercocebus galeritus). There is no current accurate estimate of the mangabey population, but a 1994 census estimated the population at 1,000–1,200. Their habitat has been severely degraded since then: visual estimates indicated that 30% of the forest area has been cleared and product use has increased in > 80% of forests surveyed. As the mean number of mangabey groups per forest is positively correlated with forest area and density of trees, this loss is damaging to the mangabey population. There has also been an increase in mangabey-human conflict, e.g., crop raiding, set traps, mangabeys chased by dogs. Mangabeys exhibit ecological flexibility, but behavioral data come from only a few mangabey groups. A new conservation approach is needed because past approaches, particularly the Tana River Primate National Reserve and a World Bank/Global Environment Facility Project, failed to protect the forests. The failure was mainly due to a disregard of the land-tenure issue within the Reserve, exclusion of local people from decision-making, and neglect of forests outside the reserve. Future actions must include community conservation programs and forest and corridor restoration. Research should focus on traditional management, status of primate groups in severely degraded forests, ecology of additional groups, and a population estimate to inform management as they implement more specific conservation strategies for the species.     

Endangered species in small habitat patches can possess high genetic diversity: the case of the Tana River red colobus and mangabey

We used mtDNA sequence data from the Tana River red colobus and mangabey to determine how their population genetic structure was influenced by dispersal and habitat fragmentation. The colobus and mangabey are critically endangered primates endemic to gallery forests in eastern Kenya. The forests are a Pliocene–Pleistocene refugium that has recently undergone significant habitat loss and fragmentation due to human activities. We expected both primates to exhibit low levels of genetic diversity due to elevated genetic drift in their small populations, and to show a strong correspondence between genetic and geographic distance due to disruption of gene flow between forests by habitat fragmentation. Additionally, because mangabey females are philopatric, we expected their mtDNA variation to be homogeneous within forest patches but to be heterogeneous between patches. In contrast, colobus have a female-biased dispersal and so we expected their mtDNA variation to be homogeneous within and between forest patches. We found high levels of haplotype and nucleotide diversity as well as high levels of sequence divergence between haplotype groups in both species. The red colobus had significantly higher genetic variation than the mangabey did. Most of the genetic variation in both primates was found within forest fragments. Although both species showed strong inter-forest patch genetic structure we found no correspondence between genetic and geographic distances for the two primates. We attributed the high genetic diversity to recent high effective population size, and high sequence divergence and strong genetic structures to long-term habitat changes in the landscape.     

Pregnancy,gestation and parturition in free-ranging tana river crested mangabeys (Cercocebus galeritus galeritus)

Mean gestation for seven free-ranging Tana River crested mangabeys (Cercocebus galeritus galeritus) is 180 days (SE = 4.49). All females showed postconception sexual swellings after the first 2 months of pregnancy, and two of the seven copulated with males at this time. One birth was observed; observations of a second infant began less than 1 hr after birth. Details of parturition are given, with responses of group members to the events. Adult and juvenile females showed more sustained interest in the new infants than adult or juvenile males.     

Ecological correlates of abundance in the Tana mangabey (Cercocebus galeritus)

I investigated the ecological correlates of abundance in the Tana mangabey (Cercocebus galeritus), one of the world's most endangered primates, with the goal of recommending management strategies. I systematically selected 31 forest fragments throughout the mangabey's 60-km distribution along the lower Tana River in southeastern Kenya. Within the 31 fragments, I measured vegetation structure, food abundance, and human forest product use in 107 belt transects, and conducted 370 mangabey surveys. I used a weighted multiple regression analysis to determine whether there was a dependence between the selected forest attributes and the mean number of mangabey groups per fragment. Fragment area and density of trees > or =10 cm diameter at breast height (DBH) were the only variables that significantly correlated with the variation in mangabey abundance. No additional variables were significant when the analysis was limited to forest fragments inside the Tana River Primate National Reserve (TRPNR) or to fragments outside the TRPNR. When I estimated the resources available before recent human forest product use by adding nonharvested and harvested variables, the total basal area of the top 15 food species became significant. This was only within the TRPNR, however. Management, therefore, should focus on increasing forest area, density of trees > or =10 cm DBH, and coverage of food trees throughout the mangabey's distribution. Solutions must be found for the problem of forest clearing, and forest product use must be better managed to protect the habitat of this critically endangered primate. The significance of food abundance only within the TRPNR suggests a need to collect dietary data from mangabey groups in fragments toward the southern limit of the mangabey's distribution, where plant species composition differs from that in fragments in which dietary data have been previously collected.     

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.     

Effects of habitat disturbance on the behavioral ecology and demographics of the Tana river red colobus (Colobus badius rufomitratus)

Annual surveys in 1985–1987 revealed that, since 1975, the total population of the Tana River red colobus (Colobus badius rufomitratus)declined by approximately 80%. An intensive study in 1986–1988 of two groups of colobus in the Tana River Primate National Reserve indicated that habitat disturbance from the changing river course and shifting agricultural practices were primarily responsible for the decline. Clearcutting around Mchelelo forest in the late 1960s compressed colobus populations to levels probably above the carrying capacity. Between 1975 and 1986 primate population density declined dramatically, the number of red colobus groups in Mchelelo forest decreased by half, and the size of the remaining group was greatly reduced. In 1986, there were fewer solitary colobus and small parties in the forest, harem male takeovers did not occur, infant survivorship increased, and demographic parameters generally had improved. The colobus groups in Mchelelo in 1973–1975, living at higher densities, showed different feeding and ranging behaviors than 1986–1988 groups. Range size was smaller in 1975, range overlap occurred, and a greater portion of the forest was used per day and per month. Mature leaves accounted for a much higher proportion of the diet. Time spent feeding and resting was the same in both studies. Social organization in predominantly one- male groups was maintained and adult and subadult females transferred between groups.     

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.     

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

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

Human and natural impacts on forests along lower Tana river,Kenya: implications towards conservation and management of endemic primate species and their habitat

Seventy-three forest patches were assessed to determine the effects of human and natural impact on native forests along the Lower Tana River flood plains in Kenya between January and March 2001. Seventeen of these forests were within the Tana River Primate National Reserve (TRPNR) while 56 were outside the protected area. Cultivation and dyke construction had the most devastating human impact, which involved partial or complete forest clearing resulting in further fragmentation of forest patches [Suleman MA, Wahungu GM, Mouria PK, Karere GM, Oguge N, Moinde NN (2001) Tana River primate census and forest evaluation. A report to Kenya Wildlife Services]. Natural impacts were either die back or flooding, which appeared to cause progressive degradation of forest structure and biodiversity. Overall, forest area in the Lower Tana significantly reduced by 34.5% (P < 0.001) over a 21-year period. Forest loss was greater outside the reserve (38%) than inside (29.2%) reiterating the significant role played by this protected area in habitat and species conservation. Continued forest loss increases extinction risks for the endemic primate species the Tana River Red Colobus (Procolobus rufomitratus) and the Crested Mangabey sub-species (Cercocebus galeritus galeritus). Initiation of community conservation programmes outside the reserve and introduction of sustainable micro-economic projects were recommended to enhance sustainable livelihoods and the environment.     

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.     

Food choices and habitat use by the Tana River yellow baboons (Papio cynocephalus): a preliminary report on five years of data

The Tana River Primate National Reserve, Kenya (TRPNR) yellow baboons' (Papio cynocephalus) long‐term habitat usage and food preferences are relatively under‐reported. The author presents a preliminary food catalog and analyses of 5 years of data (January 88–October 92; n=55 mo; 875 observation days; 4,893 hourly scans) for the Mchelelo troop (x̄=75 individuals). The author predicted that the TRPNR baboons would spend more time on the much larger savanna, show a seasonal preference for fruits/seeds, and show rainfall‐influenced food preferences. Although more time was spent on the proportionately larger savanna than in the forests, more than 42% of the observations occurred in forests that accounted for only 8.7% of the area regularly used by the baboons. Fruits/seeds consumption was high throughout the period and a significantly higher proportion of each month's observations reflected fruits/seeds rather than grasses/herbs/corms consumption. Two forest species' (Phoenix reclinata and Hyphaene compressa) were particularly important. Regression analysis showed fruits/seeds consumption predicted most of the grasses/herbs/corms consumption variance. There was no statistical difference in rainy vs. non‐rainy season fruits/seeds or grasses/herbs/corms consumption. One implication of these data is the baboons' potential impact on the critically endangered Tana River mangabeys (Cercocebus galeritus), which also rely heavily on P. reclinata and H. compressa. Another is what the “savanna” designation may or may not tell us about baboons. Am. J. Primatol. 71:432–436, 2009. © 2009 Wiley‐Liss, Inc.     

Spatial distribution of primates in a mosaic of colonizing and old growth forest at Ngogo, Kibale National Park, Uganda

Primate censuses were conducted in a mosaic of colonizing (two locations) and old-growth forests using line transect methods at the Ngogo study site, Kibale National Park, Uganda. Black and white colobus monkeys (Colobus guereza) were encountered more frequently in the colonizing forests than in the old growth forest, while chimpanzees (Pan troglodytes) were encountered more frequently in the old growth forest than in colonizing forests. Although not significant, results suggest that blue monkeys (Cercopithecus mitis) frequented colonizing forests more often than old growth forest. The encounter rates of mangabey (Lophocebus albigena), and redtail (Cercopithecus ascanius) groups were ambiguous with their density being higher in some colonizing forests but not others as compared to old-growth forest. No significant differences were detected for baboons (Papio anubis), Lhoests (Cercopithecus lhoesti), and red colobus monkeys (Piliocolobus tephroscales). The conversion of forests to farmland is one of the major problems encountered in primate conservation. This study shows that secondary forests replacing anthropogenic grasslands have the potential of supporting some primate species such as black and white colobus, redtail monkeys, and possibly blue monkeys. Therefore, such areas should not be given up but should be conserved for the benefit of primates that can survive in secondary forests; as the forests mature further, primate species that are adapted to old growth forest will colonize the area provided there is a nearby source.     

A previously undescribed mangabey from Southern Tanzania

A new form ofCercocebus galeritus is described. The new mangabey was discovered recently in the Uzungwe Mountains of Tanzania. It inhabits a restricted area of lowland and transitional rain forest on the steep, dissected, southeast-facing scarp slopes. In general appearance (size, shape, hair patterns, posture, gait), it closely resembles other forms of this species:C. g. galeritus from the Tana River gallery forests in Kenya andC. g. agilis from Gabon and Zaire. The pelage is intermediate in color between these two subspecies. Areas of bare skin differ markedly from the otherC. galeritus, particularly the almost cream-colored face. Vocalizations are typical forC. galeritus. Preliminary field observations indicate that these mangabeys form multimale groups with a tendency to move as dissociated subparties, as is the case forC. g. galeritus. Although no formal classification is proposed, the evidence suggests that the new mangabey should joinC. g. galeritus,C. g. agilis andC. g. chrysogaster as a fourth distinct form within the polytypic speciesC. galeritus.     

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.