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.     

The Value of Measuring Food Availability on the Ground for a Semiterrestrial Frugivore, the Tana River Mangabey (Cercocebus galeritus) of Kenya

Collecting phenological data, seasonal availability of plant resources that primates feed on, allows us to understand feeding ecology better. A number of primates are terrestrial or semiterrestrial frugivores, yet phenology is generally measured only in the canopy. I hypothesized that combining measurements of food availability on the ground with canopy measurements would more strongly correlate with diet than canopy measurements alone for a semiterrestrial frugivore, the Tana River mangabey (Cercocebus galeritus). From July 2005 until June 2006, I conducted monthly follows on a mangabey group. Phenology was measured in 105 individuals of their top seven food tree species. I measured canopy phenology on a 0–5 scale and counted fruits in three 1 m³ areas of the canopy, and measured ground phenology by counting fruits and seeds in four 1 m² quadrats under the canopy. I calculated each tree’s canopy volume and canopy shadow, and each species’ mean fruit weight, mean seed weight, and density. Monthly biomasses were calculated as kilograms per hectare. Spearman correlations were performed between diet contribution and canopy biomass, ground biomass, and total biomass. The hypothesis was not supported for seven species individually or combined. The hypothesis was supported for 3 of 12 diet items, although canopy biomass was also significant for 2 of those items. Two diet items correlated only with ground biomass. Studies of the Tana River mangabey may benefit from measuring ground phenology only for those items eaten exclusively on the ground. Primatologists studying terrestrial or semiterrestrial frugivores should consider feeding height when deciding on phenology methods.     

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.     

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.     

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.     

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.     

Brief communication: Puncture and crushing resistance scores of Tana river mangabey (Cercocebus galeritus) diet items

Cercocebus mangabeys are characterized by dental traits that have been interpreted as adaptations to eat hard diet items. Although there are data that mangabeys include a large proportion of fruit and especially seeds in their diets, no hardness measurements have been done on mangabeys' food items. This study measured puncture and crushing resistance of food items in the diet of the Tana River mangabey (C. galeritus). Feeding data were collected by the use of scan samples from one mangabey group from August 2000 to July 2001 and from July 2005 to June 2006. Food items were collected during the latter period only, and from the same tree in or under which mangabeys had been observed eating. A portable agricultural fruit tester was used to measure the puncture resistance of fruit and a valve spring tester was used to measure the crushing resistance of seeds. The average puncture resistance of fruit was 1.7 kg/mm², and the average crushing resistance of seeds was 12.8 kg. There were no correlations between puncture resistance, crushing resistance, or all resistance scores and frequency contribution to the diet. Resistance scores measured in this study were within the range of hardness scores of fruit and exceeded hardness scores of seeds eaten by other hard object feeders. Although this study supports the interpretation that Cercocebus dental traits are adaptations to hard object feeding, future research should investigate other material properties of food, as well as the role hard diet items play in niche separation and as fallback foods. Am J Phys Anthropol 2009. © 2009 Wiley‐Liss, Inc.     

Tree mortality due to an El Niño flood along the lower Tana River, Kenya

This study investigated forest tree mortality as a result of the extremely strong 1997–1998 El Niño flood in Tana River, Kenya, directly tested how mortality varied in relation to tree species and diameter at breast height (DBH), and indirectly tested how mortality varied in relation to floodwater depth. The study forest was under 2 m of water for approximately 71 days, from December 1997 until February 1998. Twenty-five liana, subcanopy tree, and canopy tree species were selected based on their importance in the diet of the Tana River mangabey ( Cercocebus galeritus Peters), a critically endangered primate endemic to the Tana River. Reproductive-sized individuals of these species were enumerated in 16.25 ha. I also enumerated trees killed by the El Niño flood, recorded their location in the forest, and measured their DBH. Ninety-two trees in fifteen species were killed by the flood. There were significant differences in mortality by species and by 0.25 ha quadrat. There were negative correlations between number of dead and DBH, number of dead and distance from the river, and per cent of quadrat killed and distance from the river. There appear to have been few long-term consequences of the El Niño flood in the forest or for the mangabeys.     

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.     

Diet and Feeding Behavior of <Emphasis Type="Italic">Leontopithecus chrysomelas</Emphasis> (Callitrichidae) in Degraded Areas of the Atlantic Forest of South-Bahia,Brazil

Habitat disturbance alters plant diversity and food resource availability, affecting the ecology, and ultimately the survival and reproduction, of species depending on those plants. Studies in degraded areas serve to improve our understanding of the consequences of habitat modification for endangered species and to guide conservation actions. We studied diet composition, monthly variation in feeding behavior and fruit feeding time, and dietary diversity in two golden-headed lion tamarin (Leontopithecus chrysomelas) groups ranging in a degraded area of the Atlantic Forest in South-Bahia, Brazil, over a 12-mo period. We recorded feeding behavior and food items consumed through continuous observations and focal animal sampling, and performed dietary analyses on samples from consumed fruits. Substrate manipulation to search for animal prey was the feeding activity most frequently observed, followed by fruit consumption. We observed nectar drinking and exudate feeding at low frequencies from April through July. Bromeliads were the principal foraging substrate. We observed the use of 114 plant species, confirming the large dietary diversity reported for the species. Individual trees from the family Melastomataceae, common in degraded forests, accounted for the highest visiting frequencies (40%). Fruit availability was the main factor explaining variation in monthly fruit feeding time, despite the absence of climatic seasonality. Nutritional or energetic characteristics did not affect fruit choice. Differences in floristic composition appear to be a major determinant of the species’ diet in different study areas. Regional forest restoration programs should consider including advanced forest species, to improve both forest quality and animal mobility between fragments.     

Mangabey(Cercocebus albigena). Social organization and population density in relation to food use and availability.

Data are presented on the feeding behavior and activities of mangabeys (Cercocebus albigena) in the Ngogo study area, Kibale Forest, Uganda. Mangabeys spend 47% of activity observations feeding, 27% moving, and the remainder of the activity observations is accounted for by grooming, playing, vocalizing, copulating, etc. Feeding on fruit constitutes 58% of feeding records, arthropods 25%, young leaves and flowers 10%, cambium 5% and rare and unidentified items 2%. 29 tree species are used as sources of vegetable food and 31 tree species are used as substrate for arthropod search. Mangabeys move an average distance of 1,299 m per day, and use an average of 28,50 X 50 m quadrats per day. The activity patterns, the types and number of food species, the daily distances traveled, and the number of quadrats used per day, are not significantly different from those found in the literature for mangabeys in the Kanyawara research area, Kibale Forest, Uganda. Mangabey population density in Ngogo is approximately 1.46 times that of the Kanyawara mangabeys. The difference in density is associated with Ngogo exhibiting a greater mangabey food tree density than is found at Kanyawara. The higher mangabey density in Ngogo is associated with an average group size similar to that at Kanyawara, and an increase in the number of groups per unit area. The greater number of groups is accommodated by the mangabey having smaller home ranges, and less home range overlap than do the Kanyawara mangabeys. I suggest that these results are compatible with an interpretation based on disease control via regulation of group size, and social and spatial isolation between groups. The role of food availability in regulation of group size, or determining land tenure systems remains uncertain.     

Feeding strategy of the Tana mangabey (Cercocebus galeritus galeritus) (Mammalia: Primates)

Systematic data on the feeding behaviour and ecology of the Tana mangabey ( Cercocebus g. galeritus ) were collected over a period of 13 months in a riverine forest study site on the Tana River in Kenya. A total of 1151 hours of observation was conducted on two study groups, containing 36 and 17 animals respectively. Both spatial and temporal aspects of vegetation were studied. Particular emphasis was placed on quantification of foraging behaviour , which has not been treated as a distinct category in previous primate studies. (Feeding behaviour = foraging + eating.)
Dietary composition varied according to season, but there was also evidence that the diversity of the diet increased as food availability decreased. In addition, foraging increased when food was scarce, as did total distance moved and area searched for food. Results of analysis of major food items indicated that the mangabeys were possibly selecting such items in association with their metabolisable energy values. The conspicuous foraging behaviour and locomotor versatility of the mangabeys, combined with these quantitative observations, support the interpretation that this primate is a "generalist" in terms of feeding strategy, compared with "specialist" folivores exhibiting minimal searching and manipulation of food items. It is suggested that as "generalists" the mangabeys are particularly suited to forests lining meandering river systems, with their fluctuating mosaic of vegetation and food availability.     

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.     

Tana River Mangabey Use of Nonforest Areas: Functional Connectivity in a Fragmented Landscape in Kenya

Habitat loss and fragmentation is a serious threat to biodiversity. Fragment isolation can be reduced if fragments are connected, either structurally through habitat corridors or functionally if the species can move through the surrounding matrix. One-way to evaluate landscape connectivity is to observe natural movements of animals within fragmented landscapes. The Tana River mangabey (Cercocebus galeritus) is an endangered monkey endemic to fragmented forests along the lower Tana River in Kenya, and who has been observed to move through matrix between fragments. One mangabey group moved through 1 km of matrix, while another group moved through two areas of matrix. I collected behavioral and ranging data on the latter group to describe its behavior and time spent in the matrix. Utilizing data from belt transects in the matrix and forest fragments, I characterized the vegetation structure of the matrix and compared it to the forests included in each group's home range. The group spent the majority of their time eating while in the matrix, and spent an average 36.4 min in one matrix area and 100 min in the other. The matrix is generally characterized by the highest measures for a nonforest attribute and the lowest measures for forest attributes. These results suggest that forest fragments are functionally, but not structurally, connected for the mangabey; a landscape approach to conservation, therefore, should be taken for the lower Tana River. Research investigating the limitations of the mangabey's ability to use the matrix is needed.     

Mangabey (Cercocebus albigena) population density,group size,and ranging: A twenty-year comparison

Mangabey groups studied in the Kibale Forest Reserve, Uganda, in 1971 were studied again in 1991 using similar data collection protocols. The results were used to assess the effect of group size on activity budgets and travel costs, and to document the effects of habitat changes on mangabey density and demography. Larger mangabey groups traveled longer distances per day than smaller groups. Time budgets were less clearly influenced by group size. Mangabey population density increased over the 20 year period. This increase in population density paralleled habitat changes, particularly an increase in tree density, and was accompanied by increased use of regenerating forest. © 1994 Wiley-Liss, Inc.     

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.     

Feeding Ecology of Cross River Gorillas (Gorilla gorilla diehli) at Mawambi Hills: The Influence of Resource Seasonality

Determining the composition of primate diet and identifying factors that affect food choice are important in understanding habitat requirements of primates and designing conservation plans. We studied the diet of Cross River gorillas (Gorilla gorilla diehli) in relation to availability of food resources, in a semideciduous lowland forest site (Mawambi Hills) in Cameroon, from November 2009 to September 2011. Based on 109 d of feeding trail data, 203 fecal samples, and 22 mo of phenological monitoring, we determined that gorillas consumed a total of 242 food items, including 240 plant items from 186 species and 55 taxonomic families. Mawambi gorillas diversified fruit consumption when fruit availability increased, and consumed more fibrous foods (pith, leaf, bark) during times of fruit scarcity, consistent with results of other gorilla studies. However, fruit availability was not related to rainfall, and the period of fruit scarcity was more pronounced at Mawambi than at other gorilla study sites, due to a single long dry season and extreme rainfall at the end of the rainy season that delayed fruit production and ripening. We found no relationship between the daily path length of the gorillas and fruit consumption. We found feeding habits of Mawambi gorillas to be notably similar to those of a population of Cross River gorillas at Afi Mountain, Nigeria, although subtle differences existed, possibly due to site-specific differences in forest composition and altitude. At both sites the liana Landolphia spp. was the single most important food species: the leaves are a staple and the fruits are consumed during periods of fruit scarcity. Snails and maggots were consumed but we observed no further faunivory. We suggest that tree leaves and lianas are important fallback food sources in the gorilla diet in seasonally dry forests.     

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.