Digestibility of a high-fiber biscuit-based diet by black and white colobus (Colobus guereza)

The acceptability and digestibility of a high-fiber biscuit-based diet was investigated using two adult male Colobus guereza animals. Although the animals were initially reluctant to accept the biscuit, it was eventually readily consumed. Apparent digestion coefficients for the diet (average composition, dry matter basis: 16% crude protein, 25% neutral detergent fiber (NDF), 9.5% acid detergent fiber (ADF), 1.2% acid lignin) determined by total fecal collection were 0.871 for dry matter, 0.813 for NDF, 0.693 for ADF, and 0.208 for acid lignin. Fiber digestive capabilities in C. guereza generally exceeded those reported in ruminant species based on predictive equations. Use of acid lignin and Cr₂O₃ as markers underestimated dry matter digestibility by 3.9 and 6.0%, respectively.     

Mating behavior and endocrine profiles of wild black and white Colobus monkeys (Colobus guereza): toward an understanding of their life history and mating system

Black and white colobus monkeys (Colobus guereza, "guerezas") show no external signs of estrus, and little is known about their mating behavior or reproductive endocrinology. To learn more about the life history characteristics and mating system of guerezas, we documented the mating behavior and ovarian hormone profiles of 10 cycling, lactating, and pregnant females in a wild population. We studied six groups of guerezas in Kibale National Park, Uganda, and collected ad libitum data on their mating behavior. We collected urine samples every 1.9+/-0.2 days from potentially fertile females and quantified conjugated urinary estrogen (E1S) and progesterone (PdG) metabolites using enzyme immunoassay (EIA). Females solicited 50.5% of copulations, and most copulations occurred during the interval starting 5 days before presumptive ovulation and ending 2-3 days later, with the highest copulatory levels occurring close to ovulation. We show that the median ovarian cycle length is 24 days, the median gestation length is approximately 158 days, the length of lactational amenorrhea is at least 7-8 months, and the median interbirth interval for females with surviving infants is approximately 22 months. We also document overlap between females' receptive periods in one-male, two- to three-female groups, which may mean that male transfer into such groups is potentially profitable.     

Use of sleeping trees by black and white Colobus monkeys (Colobus guereza) in the Kakamega Forest,Kenya

Groups of black and white colobus monkeys, or guerezas (Colobus guereza), observed in the Kakamega Forest, Kenya, had weak fidelity for sleeping sites. Groups often slept in trees near commonly used food sources, which might reduce the time and energetic costs of travel. Although the home range of each group overlapped with four to seven others, groups seemed to avoid sleeping near other groups, which would give them immediate and exclusive access to nearby food sources in the morning. The number of times a species of tree was slept in was positively correlated with its density. This may have occurred because so many suitable sites were available that proximity to feeding trees could be obtained whether or not groups slept in the feeding trees. Groups slept in tall trees, which provide stable sleeping sites and which may provide protection from both aerial and ground predators. Groups were more tightly clustered on nights with greater visibility, which might reduce the risk of predation. Am. J. Primatol. 45:281–290, 1998. © 1998 Wiley-Liss, Inc.     

Interactions between overlapping multimale groups of black and white colobus monkeys (Colobus guereza) in the Kakamega Forest,Kenya

Sixteen out of 18 groups of black and white colobus monkeys, or guerezas (Colobus guereza), observed in the Kakamega Forest, Kenya, included more than one adult male. Each group overlapped in its home range with 4–7 other groups, and no group appeared to have exclusive access to any part of its home range. Groups were engaged in intergroup encounters one-quarter of observation time. Encounters often occurred around preferred feeding sites as different groups were attracted to such sites in their overlapping home ranges. Wins and losses during encounters were not dependent on location and a null model suggested that groups were not increasing their encounter rate to defend boundaries, further demonstrating a lack of territoriality. Although guerezas have repeatedly been described as a territorial species living in one-male groups, nonterritorial multimale groups are common in continuous forests. Territorial one-male groups may be usual in narrow riparian forests where resources are limiting, groups are small, and defendability is high, but such organization cannot be regarded as typical of the species. Habitat affects group size, as well as the potential for territoriality, and group size determines the number of adult males per group; therefore, classifying groups as one-male or multimale appears to be an artificial dichotomy. © 1996 Wiley-Liss, Inc.     

Virus associated papillomas in colobus monkeys (Colobus guereza)

Numerous papillomas ranging in size from 1--10 mm were seen in four colobus monkeys (Colobus guereza). The lesions were confined to the fingers and toes and to the dorsal-lateral aspects of the hands and feet distal to the carpus and tarsus. Electron microscopy of two of the lesions revealed compactly arranged crystalline arrays of intranuclear virus particles in the epidermis. The particles were seen only in cells of the stratum granulosum and stratum corneum. By the negative stain technique, the non-enveloped spherical particles measured 52--58 mm in diameter. The arrangement of the capsomeres was consistent with an icosahedral symmetry. The observations suggested a viral etiology for the cutaneous papillomas similar to that of other mammalian species.     

Phylogeography of the Angolan black and white colobus monkey,Colobus angolesnsis palliatus,in Kenya and Tanzania

Little is known about genetic variation in the 6–8 subspecies of Colobus angolensis, currently distinguished by pelage differences. We present a comparative genetic analysis of one of these subspecies, C. a. palliatus, in Kenya and Tanzania that assesses evolutionary relationships and patterns of mitochondrial genetic diversity in 103 individuals across its geographic range. Fecal samples from approximately 156 individuals were collected in four localities: (1) Diani Forest, Kenya; (2) Shimoni, Kenya; (3) Udzungwa Mountains National Park, Eastern Arc Mountains, Tanzania; and (4) Mount Rungwe, Southern Highlands, Tanzania. These samples represent at least six groups, with 5–15 samples from each. Comparative sequence analysis of a 1,795 base pair mtDNA fragment revealed 19 unique haplotypes in four populations. Phylogenetic analyses suggest that sampled Kenyan haplotypes are paraphyletic, with one Kenyan haplotype basal to all other sampled haplotypes. Analysis of molecular variance (AMOVA) suggests high levels of genetic variation among populations (Φ_ST 0.72, P<0.001). Genetic data are concordant with a subspecies level differentiation between C. a. palliatus populations in Kenya and those in Central and southern Tanzania, as earlier suggested based on pelage differences. This study highlights the evolutionary distinctiveness of Kenyan populations of C. a. palliatus relative to Tanzanian populations. Although C. a. palliatus habitat in Tanzania is currently better protected than in Kenya, our results suggest Kenyan and Tanzanian populations should be considered distinct units, and the protection of C. a. palliatus habitat in Kenya, as well as habitat connectivity between Kenyan populations, should be prioritized for conservation and management. Am. J. Primatol. 72:715–724, 2010. © 2010 Wiley‐Liss, Inc.     

Individuals' behaviors following dye-marking in wild black-and-white colobus (Colobus vellerosus)

The ability to recognize individuals is a prerequisite for analyzing social relationships. We marked five adult and subadult Colobus vellerosus (three in 2002, and two in 2003) at the Boabeng Fiema Monkey Sanctuary, Ghana, to assess the feasibility of dye-marking black-and-white colobus, describe their reactions, and compare some of their behaviors with those of unmarked individuals. We used Nyanzol-D, a nontoxic black dye sprayed on the white tail (or white thigh) of the animal with a spray gun or a tree sprayer. Reactions to the marking procedure ranged from moving away and staring at the observer, without interruption in feeding (in one subject), to fleeing about 5 m away (in four subjects). In 234 hr of ad libitum observations (in 2002 and 2003), marks were scratched or otherwise were the object of attention from the bearer or other individuals on only one occasion. In 2002 we collected 22 hr of observations on the three marked monkeys and some unmarked monkeys in 10-min focal samples. Neither the marked nor the unmarked animals attended to the marks during focal samples. Marked and unmarked individuals displayed similar rates of displacement activities (autogrooming, scratching, and yawning). The proportion of scans with at least one near neighbor varied between marked and unmarked subjects, but the direction of the difference was not the same between males and females. The only aggression observed was displacements, and only in one comparison (out of four) did a difference emerge: the marked subadult male received more displacements than the unmarked males. Overall, marked and unmarked individuals did not differ consistently in our measures. Examination of the potential effects of marking should continue, since changes in pelage coloration may have longer-term social effects in species that rely largely on vision.     

The locomotor and postural repertoires of Ateles geoffroyi and Colobus guereza,and a reevaluation of the locomotor category semibrachiation

The locomotor repertoire of Ateles geoffroyi includes quadrupedal walking and running, climbing, brachiation and arm-swinging, bipedalism, and leaping. Its postural repertoire is characterized by below branch suspensory activities. In contrast, the locomotor repertoire of Colobus guereza consists primarily of quadrupedal galloping and bounding, and leaping. It does not brachiate or walk bipedally and rarely performs arm-swinging. The Colobus guereza postural repertoire is characterized by above branch sitting postures. Ateles geoffroyi is a highly mobile primate, whereas Colobus guereza is essentially sedentary. In the past, there has been a tendency to group Ateles and Colobus in a single locomotor category, semibrachiation. Comparison of the very different repertoires of these two species points out some of the shortcomings of the category semibrachiation. First, no locomotor pattern or group of patterns has been described as semibrachiation (i.e., no animals semibrachiate). Secondly, the locomotor diversity of animals included in the category is so much greater than the similarities that the category obscures more than it conveys. The usefulness of retaining this category is therefore questioned.     

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.     

Mapping homology between human and black and white colobine monkey chromosomes by fluorescent in situ hybridization

We used in situ hybridization of chromosome specific DNA probes (“chromosome painting”) of all human chromosomes to establish homologies between the human and the white and black colobus (Colobus guereza 2n = 44). The 24 human paints gave 31 signals on the autosomes (haploid male chromosome set). Robertsonian translocations between chromosomes homologus to human 14 and 15, 21 and 22, form colobine chromosomes 6 and 16, respectively. Reciprocal translocations were found between human chromosomes 1 and 10, 1 and 17, as well as 3 and 19. The alternating hybridization signals between human 3 and 19 on Colobus chromosome 12 show that in this case a reciprocal translocation was followed by a pericentric inversion. The hybridization data show that in spite of the same diploid number and similar Fundamental Numbers, the black and white colobine monkey differs from Presbytis cristata, an Asian colobine, by 6 reciprocal translocations. Comparisons with the hybridization patterns in other primates show that some Asian colobines have a more derived karyotype with respect to African colobines, macaques, great apes, and humans. Chromosome painting also clearly shows that similarities in diploid number and chromosome morphology both between colobines and gibbons are due to convergence. Am. J. Primatol. 42:289–298, 1997. © 1997 Wiley-Liss, Inc.     

Acute gastric dilatation in two black and white colobus monkeys

Acute gastric dilatation in two black and white colobus monkeys is described. The subfamily colobini have a ruminant-like stomach and a pregastric fermentation, of important for the observations described.     

Vigilance in ursine black and white colobus monkeys (Colobus vellerosus): an examination of the effects of conspecific threat and predation

Vigilance is thought to have evolved as an antipredator defense but, in primates, conspecific threat often better explains this behavior. We examined vigilance in one group of Colobus vellerosus inhabiting the Boabeng‐Fiema Monkey Sanctuary in Ghana. We aimed to (1) describe factors affecting vigilance in this population, and (2) examine the importance of predation avoidance and conspecific threat in explaining vigilance patterns. Because of a male takeover preceding the study, our focal group (B2) consisted of six adult males and three adult females. We collected 490 10‐min focal samples (82 hr) from all adults in the group (N=9) from July to November, 2001. To avoid predators, individuals should be more vigilant (i) with fewer neighbors, and (ii) in areas of the canopy with higher predation risks. Conspecific threats can be divided into extra‐ and intra‐group threats. Extra‐group threats should lead to higher vigilance levels (iii) during intergroup encounters, and (iv) in areas where the home range overlaps with other groups of colobus. Intra‐group threats should lead to greater vigilance (v) in the presence of neighbors and (vi) while feeding or occupying food patches (if resources are limiting). Our results best support the hypothesis that vigilance functions primarily to detect extra‐group, conspecific threats. Individuals were most vigilant during intergroup encounters and in areas of range overlap, and monthly vigilance rates were associated with monthly encounter rates. Individuals tended to scan less in proximity to familiar vs. unfamiliar group mates, suggesting that relationship quality may affect colobus vigilance. Finally, predation pressures or anthropogenic disturbances might have influenced vigilance, as individuals were more vigilant low in the canopy. However, this last result could also be due to the lower visibility because of dense foliage or to the fact that the monkeys have access to fewer escape routes when ranging lower in the canopy. Am. J. Primatol. 71:919–927, 2009. © 2009 Wiley‐Liss, Inc.     

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.     

Food selection by black colobus monkeys (Colobus satanas) in relation to plant chemistry*

Black colobus monkeys (Golobus salanas) in the Douala-Edea Reserve, a rain-forest on the coast of Cameroon, have been shown to avoid young and mature leaves of most of the common plants in their habitat and to feed disproportionately heavily on leaves of rare plants. The proportion of leaves in the diet was low compared to most colobines studied, and the monkeys spent over half their feeding time eating seeds. Patterns of food selection were analysed in relation to distribution of nutrients, digestion–inhibitors and toxins in the vegetation. Colobw satanas select food items that are rich in mineral nutrients and nitrogen and low in content of the general digestion-inhibitors, lignin and tannin. They achieve this in the following ways: (i) by feeding preferentially on young leaves, which have higher nutrient content and lower contents of digestion-inhibitors than mature leaves; (ii) by eating those mature leaves with highest nument content relative to content of digestion-inhibitors; and (iii) by eating seeds, which are sources of readily available energy and which, as an item class, are less rich in digestion-inhibitors. Seeds at Douala-Edea appear to contain Ins nitrogen than leaves and C. satanas selects those seeds with highest nitrogen content. It is suggested that seed-feeding may be facilitated by the ability of the forestomach flora of these ruminant-like monkeys to detoxify some of the secondary compounds contained in seeds. Avoidance of most unused young and mature leaf items is correlated with a low nutrienudigestion-inhibitor ratio; avoidance of most unused seeds could be accounted for by their low nitrogen contents. Most items whose avoidance could not be explained in terms of these major constraints on food selection possess secondary compounds likely to be toxic. It is proposed that relative importance of digestion-inhibitors, low nutrient content and toxins as constraints on food selection by generalist herbivores will vary greatly among forests with different nutrient and secondary chemistry profiles.     

Dominance style in female guerezas (Colobus guereza Rüppell 1835)

Socioecological models assume that quality and distribution of food ultimately determine female social relationships: a high quality diet and clumped food distribution should result in the establishment of a hierarchy with stable rank relations which is supported by empirical studies on frugivorous cercopithecines. By contrast, folivorous species with their low quality diet and dispersed food distribution should have egalitarian social relationships but empirical data are very rare. This study on female guerezas of a zoo group aimed to test the models in a colobine species and the results largely agreed with the predictions of the models: facial expressions, vocalizations, and gestures were not used for signalling dominance or subordination. Unritualized aggressions occurred frequently but were of low intensity, and interventions by third parties were never observed. Aggressions were exchanged bidirectionally and this was true also for food stealing and retreats. All this indicated the lack of established rank relations. Allogrooming was distributed rather equally and showed no kin bias. All these features characterize egalitarian social relationships and, hence, support the socioecological models.     

Observed case of infanticide committed by a resident male central American black howler monkey (Alouatta pigra)

Although infanticide has been witnessed in other species of howler monkey, and has been inferred for Alouatta pigra, an observed case of infanticide has not previously been recorded for this species. Here we describe the killing of a 2-week-old infant by the resident male of a small social group in southern Belize. The infanticide was witnessed as part of an intensive observational study that began in January 2003. The male was known to have resided in the group for at least 4 months, but it is not known whether he was the father of the infant. The literature proposes three main explanations for infanticide: two adaptive hypotheses (sexual selection and resource competition), and one nonadaptive hypothesis (social pathology). Individual cases of infanticide such as this one are important for comparative purposes, but when examined on their own they are difficult to interpret in relation to established theoretical frameworks. The data presented here show some consistency with the sexual-selection and resource-competition hypotheses, but the lack of critical information (i.e., as to paternity) makes it impossible to draw firm conclusions.