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.     

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.     

Ranging behaviour and its relation to diet selection in Tana River Red colobus (Colobus badius rufomitratus)

Ranging behaviour of a group of Red colobus monkeys, Colobus badius rufomitratus, on the Tana River, Kenya, is described. The main study group had a mean day journey of 603 in and an annual range area of 9 ha (measured in 0.25 ha quadrats). Relationships between ranging patterns and diet selection are sought on both spatial and temporal dimensions. Differential use of the annual range is related to the distribution of major food species, while the diversity of monthly ranging patterns is inversely related to the availability of young growth in the canopy. These findings lead to a discussion of why range areas at the Tana are much smaller than those reported from rain-forest sites.     

The diet of the olive colobus monkey,Procolobus verus,in Sierra Leone

Observations of the feeding behavior of wild olive colobus monkeys (Procolobus verus)were made in southern Sierra Leone, West Africa. Most data came from systematically sampling one habituated social group, which inhabited old secondary rain forest on Tiwai Island. Olive colobus at Tiwai were highly selective feeders, obtaining most of their food from a small number of uncommon middle-canopy trees, from the forest understory, and from climbers. Mature leaf blades were largely ignored; young foliage (particularly of climbers) was a year-round dietary staple, while seeds, flowers, and mature leaf petioles were seasonally important. It is argued that this diet results largely from selection for two different attributes of food: high digestibility and physical location. Preferred foods had low fiber and tannin contents, while preferred feeding sites were in thick low growth and climber tangles. P. verusis the smallest extant primate species using a foregut fermentation system. Observations of its diet accord with inferences drawn from dental anatomy, digestive physiology, and considerations of body size.     

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.     

Patterns of size variation and correlation in the dentition of the red colobus monkey (Colobus badius)

There have been numerous studies on variability and correlation in dental crown size, but the significance of the resulting patterns remains unclear. Regions of low variation and high correlation have been hypothesized to represent the poles of Butler's morphological fields, to be related to absolute tooth size, or to be related to morphological complexity of the teeth and functional efficiency. Variation and correlation of tooth lengths and breadths were investigated in 138 red colobus monkeys to further assess the relations among size associations, crown morphology, and absolute tooth size. In the maxilla and mandible, the postcanine teeth are the most highly correlated and least variable, followed by the incisors, then the canines. There are also lower correlations between premolars and molars than within either group. While there appears to be a relation between degree of morphological differentiation and levels of correlation and variation, there are no notable differences in the correlation of opponents along the dental arcade, which is the most important functional consideration. This suggests that different levels of correlation and variation within upper or lower teeth are “artifacts” of tooth dimensions that contribute to different geometric designs in different tooth groups as the germs develop. This morphological effect is coupled with the influence of integration fields, indicated by higher variability and lower correlations of the third molar, the largest or most molarized tooth. It is concluded that there are wide functional tolerances in occlusion with respect to the gross dimensions of dental crowns and their interrelationships.     

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.     

Object manipulation by wild red colobus monkeys living in the Abuko Nature Reserve,the Gambia

Temminck's red colobus (Procolobus badius temminckii) inhabiting the Abuko Nature Reserve, the Gambia, manipulate objects during solitary play, social play where there is an obvious goal involved, agonistic and intimidation displays, and tug-of-war contests. Some of the object manipulation may be regarded as true tool use and manufacture. Variation in the form and frequency of manipulative activities shows clear sex differences which may relate to sex differences in social behavior. All observed cases of tool manufacture occurred at times of maximum social upheaval for the individual concerned in the act.     

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.     

Functional implications of enamel thickness in the lower molars of red colobus (Procolobus badius) and Japanese macaque (Macaca fuscata)

The purpose of this study is to determine whether teeth are likely to retain their functional efficiency throughout an individual's life time. This was done by comparing the enamel volume, the cross-sectional enamel area and the pattern of enamel distribution on unworn M(2)s of folivorous (Procolobus badius: red colobus; n=8) and frugivorous (Macaca fuscata: Japanese macaque; n=6) cercopithecids. The enamel volume of M. fuscata is significantly greater than that of P. badius. As the lower molars of colobines become worn, the dentine is exposed on the buccal cusps and narrow enamel rims are formed around the dentine exposures. The buccal enamel rims are especially well-developed and sharp, a pattern that has probably been selected for as being advantageous for shredding fibrous plant materials. The results of this study demonstrate that the enamel on the lingual side of the protoconid, where dentine exposure occurs first, is much thinner in P. badius than it is in M. fuscata. In addition, the dentine is exposed and thin enamel rims are formed faster in P. badius than in M. fuscata. Also, P. badius has significantly thinner and more uniform enamel distribution on the buccal wall of the crown and a higher protoconid. The buccal flare is well-developed in M. fuscata, but poorly developed in P. badius. It is tentatively suggested that the undeveloped flare and thinner enamel of P. badius combine to enable this species to maintain narrow rims, even after dental attrition, while the high cusps may be an adaptation for providing narrow enamel rims throughout life.     

The radiation of red colobus monkeys (Primates,Colobinae): morphological evolution in a clade of endangered African primates

Red colobus monkeys are a group of African monkeys that include some of the most endangered primate populations. Despite urgently needing to understand the importance of particular populations for preserving the biodiversity of this lineage, their evolutionary relationships remain poorly understood, and their taxonomy is unstable, and often enigmatic. Data on behaviour, ecology, genetics, and morphology are thus strongly needed to address taxonomic issues that are not only relevant for primatologists, but also for conservation biologists. In this study, we investigated the morphological diversity and evolution of red colobus by examining the cranial variation of 369 individuals from most living populations. Crania were measured using a set of 64 anatomical landmarks, and were analysed using geometric morphometric methods for the study of three‐dimensional landmark coordinates. We found significant differences among most of the populations traditionally described on the basis of pelage colour and geographic distribution. However, differences tended to be smaller within biogeographic assemblages, which might be related to mountain refugia during periods of forest contraction in the Pleistocene.We also found a tendency towards large taxonomic distances, which suggested that populations might have originated earlier than has been traditionally thought, a result congruent with a recent molecular phylogenetic analysis. However, the distinctive forms of East African relict populations might be related to an acceleration of morphological evolution in small peripheral isolates, under strong selective pressures. This indicates that small and isolated populations, which are also the most endangered ones, might indeed be unique representatives of the red colobus radiation, and hence contribute to its biodiversity significantly. However, in‐ depth morphological studies of red colobus, particularly those in peripheral populations that tend to be rare in the wild, as well as in museum collections, is hampered by a paucity of data. In these cases, populations might be extinct before primatologists and conservationsts can even appreciate what was lost.     

Seed dispersal by red howling monkeys (Alouatta seniculus) in the tropical rain forest of French Guiana

A 2-year field study of the frugivorous diet of a howling monkey troop, in a tropical rain forest in French Guiana, shows that they disperse by endozoochory ≥95% of plant species from which they eat ripe fruit. Passage through the digestive tract of howlers does not significantly modify the germination success of most plant species samples. Their low digestion rate (X = 20 hr 40 min) is the ultimate cause of a bimodal defecation rhythm that results in the concentration of 60% of defecations being deposited under sleeping sites. The distance of seed dispersal can reach more than 550 m from parent trees,with a mean of 260 m. Although howling monkeys consume fruits differing in morphological characteristics, they are particularly able to disseminate seeds of species whose fruits have a hard and indehiscent external coat or large seeds or both. In French Guiana, they may be especially important dispersers of the Sapotaceae with fruits that simultaneously present both characteristics.     

Killing of a pearl-spotted owlet (Glaucidium perlatum) by male red colobus monkeys (Procolobus tephrosceles) in a forest fragment near Kibale National Park, Uganda

Adult male red colobus (Procolobus tephrosceles) were observed capturing and killing an owl (Glaucidium perlatum) in the Rurama forest fragment near Kibale National Park in western Uganda. The owl was not subsequently eaten by the colobus, their conspecifics, or the other primates present during the attack. Because the incident was preceded by an agonistic encounter with a raptor, the event is best interpreted as a misdirected antipredator behavior. Although antipredator behaviors are not unknown in red colobus, this is the first such incident directed against a raptor to be documented.     

Patterns of Frugivory in Three West African Colobine Monkeys

We studied the comparative feeding ecology of three species of colobus (Procolobus badius, Procolobus verus, and Colobus polykomos) on Tiwai Island, Sierra Leone. We collected dietary data on each species by scan-sampling habituated groups. Because these groups were observed in the same study area during overlapping time periods, the confounding effects of temporal and spatial variability in food availability were reduced. Our results show that the annual diets of the two larger species (Procolobus badius and Colobus polykomos) include roughly equal proportions of fruits (including seeds), young leaf parts, and mature leaf parts, although P. badius had a greater intake of floral parts. Procolobus verus consumed almost no mature leaf parts, few fruits and seeds, and many young leaf parts. Colobus polykomos commonly fed from lianas. Seeds were the dominant fruit item eaten by all three colobus, and the fruits they selected were generally dull and non-fleshy, in contrast to the brightly-colored, pulpy fruits eaten by guenons. Leguminous plants contributed substantially to the diets of both the larger species, but comparisons with other African forest sites indicate that colobine biomass is not closely correlated with the abundance of leguminous trees in the forest. (Deceased)     

Seed-eating by red leaf monkeys (Presbytis rubicunda) in dipterocarp forest of northern borneo

Data are presented on the feeding behavior ofPresbytis rubicunda at Sepilok, north Borneo. Emphasis is given to describing the fruit-eating behavior of this small colobine monkey, which specializes in eating seeds from large, dull-colored, and fleshless fruits. The seed predation is conspicuously different from the seed dispersal effected by sympatric monogastric primates and is characteristic of colobine frugivory at other forest sites. Most seed-eating occurred during the period of maximum fruit production and fewer small-seeded, animal-dispersed fruits were eaten at other times.     

Seasonal variation in the positional behavior of red howling monkeys (Alouatta seniculus)

Recent studies on the positional behavior of primates reveal that significant seasonal variation occurs in both locomotion and postures that is related to changes in diet and foraging techniques. Howling monkeys (genusAlouatta), which also have a seasonally varied diet, are predicted to have correspondingly varied positional behaviors. Two groups of red howling monkeys were studied in a primary rain forest in French Guinana during the dry and wet seasons. During the dry season, when howler diet is based mainly on leaves, howlers traveled more frequently by quadrupedal walking on large supports, a mode of progression that is probably inexpensive energetically and relatively stable. During feeding, quadrupedal and tripedal stand contributed considerably, a posture probably associated with the equal distribution of leaves within a tree crown. In contrast, during the wet season, when fruit was abundant, howlers fed very frequently by sitting on large supports, probably because fruit consumption required more time for special manipulation. However, most seasonal changes in feeding postures, and in travel and feeding locomotion, were difficult to associate directly with dietary shifts. These behavioral changes may be more highly correlated with slight modifications in microhabitat use (horizontal and vertical daily ranges, similar and alternative arboreal pathways) that are not considered in this paper.     

Nutritional ecology of Preuss's red colobus monkey (Colobus badius preussi Rahm 1970) in Korup National Park, Cameroon

Studies on the nutritive ecology of red colobus monkeys (Colobus badius preussi) in Korup National Park, Cameroon, investigated food plants and the parts eaten as well as nutritive values of the various food items. Food plants were identified through direct observations and collected for laboratory determination of nutrient content. Food plants were analysed for crude protein (CP), crude fibre (CF), ether extract (EE), nitrogen‐free‐extractive (NFE) and total ash (A). A total of seventeen species belonging to nine different families were identified as food plants for red colobus. Food and feeding habits showed that the species were highly folivorous, tending to prefer the young leaves of food plants. Lecomtedoxa klaineana (27.0%) and Xylopia aethiopica (22.2%) of families Sapotaceae and Annonaceae, respectively, constituted about 50% of total food items consumed. Results of nutrient composition indicated individual nutrients varied significantly (P < 0.01) with food species.     

Seed predation ofCariniana estrellensis (Lecythidaceae) by black howler monkeys,Alouatta caraya

Seed predation by howler monkeys is poorly documented. Here we report the seed predation onCariniana estrellensis (Lecythidaceae) fruits by the black howler monkeyAlouatta caraya in south-east Brazil during an intense dry season. This observation suggests that even non-specialized seed predators such as howlers can use seeds in critical periods of dry season.