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.     

The active space of blue monkey and grey-cheeked mangabey vocalizations

The audible distance of 11 primate vocalizations uttered by blue monkeys, Cercopithecus mitis, and grey-cheeked mangabeys, Cercocebus albigena, and the human utterance ‘hey’ were determined experimentally. Calculations were based on measurements of (1) sound power of vocal signals (Brown: Bioacoustics, in press), (2) the attenuation rates of sound of different frequencies in East African forests (Waser & Brown: Am. J. Primatol., 1986, 10, 135–154), and (3) sensitivity of conspecific listeners to vocal signals presented in forest noise. Calculations were made of the active space, the area over which a call is audible, and the expected number of recipients of signals in nature. Masked thresholds for test vocalizations ranged from 21·1 dB for the mangabey ‘staccato bark’ call to 41·3 dB for the blue monkey ‘boom’ vocalization. The audible distance of the test signals ranged from 79 m for the blue monkey ‘chirp’ call to 1951 m for the mangabey ‘chorused grunt’ vocalization. Calls could be grouped into short- and long-range signals. The audible distance of primate long-range calls varied between 2·4 and nine times that of a typical yell given by human subjects. The active space of the test signals ranged from 1·4 to 1031·8 ha. The mean active space of monkey long-range calls (445·4 ha) was more than an order of magnitude greater than the loudest human yell. The average blue monkey long-range call was audible for 870 m, while the average mangabey long-range call was audible for 1800 m. The typical mangabey home range is four times that of the blue monkey, and in both species the average long-range call had an audible distance twice the diameter of the median home range of each species.     

Menstrual cycle characterization and artificial insemination in the black mangabey (Cercocebus aterrimus)

Concentrations of immunoreactive estrone conjugates, pregnanediol-3-glucuronide, and luteinizing hormone were measured and indexed to creatinine in daily urine samples from three female black mangabeys (Cercocebus aterrimus). Daily observations of menstruation and perineal tumescence were recorded. The mean ± SEM lengths of the menstrual cycle [apparent cycle length of 26.0 ± 0.8 days determined by observation of intermenstrual intervals (n = 26); physiologic cycle length of 31.3 ± 5 days determined by urinary endocrine analysis (n = 4)], follicular phase [16.5 ± 4 days (n = 4)], and luteal phase [14.8 ± 1 day (n = 4)] were determined. The apparent cycle length is probably more accurate. Perineal tumescence began during or shortly after menstruation, increased concomitantly with increasing follicular phase conjugated estrone values, and reached maximal size in the periovulatory period. Ovulation was closely followed by a drop in conjugated estrone levels, an increase in urinary pregnanediol-3-glucuronide, and perineal detumescence. Peak concentrations of conjugated estrone and luteinizing hormone values were coincident. Pregnanediol-3-glucuronide accurately reflected luteal function in the black mangabey. Knowledge of the menstrual cycle parameters and their correlation to perineal tumescence was used to time artificial inseminations. Semen was obtained by rectal electroejaculation. Coagulum and extended semen, or trypsin-digested coagulum, were used for insemination. One insemination of trypsin-digested coagulum at the external os of the cervix resulted in a probable conception, follówed by apparent abortion after 3 weeks.     

Phylogenetic and population systematics of the Mangabeys (primates: Cercopithecoidea)

On the basis of original craniological studies, it is concluded that recently published claims based on blood proteins that the Mangabeys are diphletic are valid, and it is proposed to divide them into two distinct genera:Cercocebus (with three species:torquatus (includingatys),agilis, andgaleritus), which belongs to the Cercocebini but has a somewhat isolated position in this tribe, andLophocebus (with one species,albigena: includingaterrimus as a subspecies), which is closer toPapio. The inter-relationships within each genus are discussed, with particular reference to the problem of subspeciesvs. allopatric species. A new subspecies is named and described,Lophocebus albigena osmani, and the anomalous position of the poorly-known subspeciesL.a. opdenboschi is extensively discussed.     

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.     

Evidence for the consumption of arboreal,diurnal primates by bonobos (Pan paniscus)

We present evidence for the consumption of a diurnal, arboreal, group living primate by bonobos. The digit of an immature black mangabey (Lophocebus aterrimus) was found in the fresh feces of a bonobo (Pan paniscus) at the Lui Kotale study site, Democratic Republic of Congo. In close proximity to the fecal sample containing the remains of the digit, we also found a large part of the pelt of a black mangabey. Evidence suggests that the Lui Kotale bonobos consume more meat than other bonobo populations and have greater variation in the mammalian species exploited than previously thought [Hohmann & Fruth, Folia primatologica 79:103–110]. The current finding supports Stanford's argument [Current Anthropology 39:399–420] that some differences in the diet and behavior between chimpanzees (P. troglodytes) and bonobos are an artefact of the limited number of bonobo study populations. If bonobos did obtain the monkey by active hunting, this would challenge current evolutionary models relating the intra‐specific aggression and violence seen in chimpanzees and humans to hunting and meat consumption [Wrangham, Yearbook of Physical Anthropology 42:1–30]. Am. J. Primatol. 71:171–174, 2009. © 2008 Wiley‐Liss, Inc.     

Affiliative behavior of adult female sooty mangabeys (Cercocebus atys)

A 14-month study of 30 adult female members of a captive group of sooty mangabeys investigated their affiliative interactions with group members of varying age and sex. The adult females preferentially affiliated with other adults and interacted less than expected with immature group members. Dyadic frequencies suggested especially frequent affiliation with the three resident adult males, although the pattern of interaction with each male was distinct and apparently was related to age and dominance status of the males. Females of the alpha matriline showed significantly greater affiliation with the males than did those of other matrilines, but this preference was not reciprocated by the males. A preference for grooming older group members (some of the matriarchs and the oldest adult male) was also suggested. In consideration of the taxonomic distinctness of the sooty mangabey from the gray-cheeked mangabey, comparison of these results with those available for albigena were made. Few differences were apparent. Comparisons with the affiliative behavior of Papio females also suggested limited differences, despite the apparently isolated position of the sooty mangabey within the tribe Papionini.     

Functional morphology of the mangabey mandibular corpus: relationship to dental specializations and feeding behavior

Recent molecular and morphological surveys suggest that mangabeys do not represent a monophyletic group. Specifically, Cercocebus is the sister taxon of Mandrillus, whereas Lophocebus forms an unresolved trichotomy with Papio and Theropithecus. The Cercocebus-Mandrillus clade is characterized by skeletal and dental adaptations related to acquisition and processing of hard-object foods that resist decomposition for months on the forest floor. Although species of both mangabey genera can be described as frugivorous seed predators with a strong reliance on hard-object foods, a growing body of evidence indicates that Cercocebus (terrestrial) and Lophocebus (arboreal) mangabeys differ in the hardness of the seeds they consume and the manner in which seeds are processed. The taxa are also distinguished on the basis of dental morphology. Given the purported differences in feeding behaviors of the two mangabey genera, we consider whether there are predictable biomechanical consequences of these behaviors that are reflected in mandibular corpus dimensions. In addition, we present metric data summarizing functional aspects of mangabey mandibular corpus morphology. Mangabey genera are generally not distinguished by differences in relative corpus size, either in postcanine or symphyseal regions. Distinct symphyseal scaling patterns characterize the Papio-Lophocebus clade and the Mandrillus-Cercocebus clade, while the postcanine corpus scales similarly between them. The hypothesis that preferential use of the incisors vs. premolars to initially process these foods results in distinct stress environments is weakly supported, given circumstantial evidence that the relative importance of bending vs. torsion may differ between Cercocebus and Lophocebus.     

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.     

Census,habitat preference,and polyspecific associations of six monkeys in the Lomako Forest,Zaire

This paper reports preliminary data on a number of poorly known cercopithecids inhabiting the Lomako Forest, Zaire. Data include those on density, biomass, group size, the relationship between group type (mono vs. polyspecific) and forest type (mixed primary, secondary, monodominant primary, and swamp), and vertical stratification. Species examined are Colobus angolensis, Cercocebus aterrimus, Cercopithecus wolfi, Cercopithecus ascanius, Cercopithecus neglectus, and Allenopithecus nigroviridis. The density and biomass for the Lomako Forest anthropoids (excluding Cercopithecus neglectus and A. nigroviridis) are 165 ind/km² and 1,034 kg/km², respectively. Cercopithecus wolfi and Colobus angolensis are found in group sizes similar to those reported from other sites while Cercopithecus ascanius, Cercocebus aterrimus, and A. nigroviridis display group sizes unique to the Lomako. While Colobus angolensis, Cercocebus aterrimus, Cercopithecus ascanius and Cercopithecus wolfi were found, to varying extents, in all four forest types, Cercopithecus neglectus and A. nigroviridis inhabited only swamp forest. The different species sort out along vertical continua both within and between the four forest types. © 1994 Wiley-Liss, Inc.     

Mangabey (Cercocebus albigena) ranging patterns in relation to fruit availability and the risk of parasite infection in Kibale National Park,Uganda

Two opposing hypotheses concerning determinants of mangabey (Cercocebus albigena) ranging patterns have been advocated. One hypothesis suggests that ranging patterns of mangabeys are largely a response to fruit availability, while the other hypothesis advocates that concerns of fruit availability are supplemented or overridden by concerns of fecal contamination and that the risk of parasite infection, especially during dry weather, determines their pattern of range use. In this 9 month study of mangabeys in the Kanyawara study area of Kibale National Park, mangabeys moved longer distances during the wet season than during the dry season. There were no seasonal differences in group spread, number of 50 by 50 m quadrats used, or in quadrat overlap between sequential sample periods. Intensity of quadrat use was closely related to the number of fruiting trees/lianas in the quadrats, irrespective of season. These findings are consistent with the hypothesis that fruit availability is a main factor influencing mangabey ranging patterns. The results are not consistent with the hypothesis that mangabey ranging patterns largely reflect differential seasonal risk of parasite infection. Am. J. Primatol. 43:65–78, 1997. © 1997 Wiley-Liss, Inc.     

Estimating the population size of the Sanje mangabey (Cercocebus sanjei) using acoustic distance sampling

The Sanje mangabey (Cercocebus sanjei) is endemic to the Udzungwa Mountains, Tanzania, and is classified as Endangered due to its putatively declining population size, habitat degradation and fragmentation. Previous population size estimates have ranged from 1,350 to 3,500 individuals, with the last direct survey being conducted 15 years before the present study. Previous estimates are now thought to have underestimated the population due to a limited knowledge of group and habitat size, nonsystematic approaches and the use of visual methods that are not suitable for surveying the Sanje mangabey with its semi-terrestrial and elusive behaviors. We used an acoustic survey method with observers recording the distinctive “whoop-gobble” vocalization produced by mangabeys and point transect distance sampling to model a detection function and estimate abundance. Twenty-eight surveys were conducted throughout the two forests where Sanje mangabeys are found: Mwanihana forest in the Udzungwa Mountains National Park (n = 13), and the Uzungwa Scarp Nature Reserve (n = 15). Group density was found to be significantly lower in the relatively unprotected Uzungwa Scarp forest (0.15 groups/km²; 95% CI: 0.08–0.27) compared to the well-protected Mwanihana forest (0.29 groups/km²; 95% CI: 0.19–0.43; p = .03). We estimate that there are 1,712 (95% CI: 1,141–2,567) individuals in Mwanihana and 1,455 (95% CI: 783–2,702) in the Uzungwa Scarp, resulting in a total population size of 3,167 (95% CI: 2,181–4,596) individuals. The difference in group density between sites is likely a result of the differing protection status and levels of enforcement between the forests, suggesting that protection of the Uzungwa Scarp should be increased to encourage recovery of the population, and reduce the threat of degradation and hunting. Our results contribute to the reassessment of the species' IUCN Red List status and informing management and conservation action planning.     

Hematology and serum chemistry in the white-crowned mangabey (Cercocebus torquatus lunulatus) and in the mandrill (Mandrillus sphinx)

Abstract: Reference values of some hematologic and plasma chemical parameters were established in two species of clinically normal Cercopithecidae. The following variables were studied in seven mandrills (Mandrillus sphinx) and nine white-crowned mangabeys (Cercocebus torquatus lunulatus): hematocrit, hemoglobin concentration, erythrocyte and leucocyte counts, mean corpuscular volume, mean corpuscular hemoglobin, mean corpuscular hemoglobin concentration, glucose, urea, uric acid, cholesterol, creatinine, aspartate aminotransferase, alanine aminotransferase, alkaline phosphatase, creatinine phosphokinase, lactic dehydrogenase, gamma glutamyl transpeptidase, total serum proteins, albumin, globulins, albumin-globulin ratio, sodium, potassium, calcium, magnesium, total phosphorus, chloride, and serum osmolality. Few differences were observed when compared with human hematological data and with other species of Cercopithecidae Primates.     

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.     

A study of facial growth in the sooty mangabey Cercocebus atys

This study examines the pattern of facial bone growth remodelling in the sooty mangabey (Cercocebus atys) by scanning electron microscopy (SEM) of high-accuracy replicas. The efficacy of the technique is appraised by SEM interpretations of facial remodelling in the crab-eating macaque (Macaca fascicularis) and correlative histological examination. The results indicate that the distribution of depository and resorptive areas in Cercocebus closely parallels that which has been observed in Macaca. It is suggested that the different adult facial morphologies in the sooty mangabey and crab-eating macaque are the result of changes in the rates of remodelling events that may be coupled with different patterns of sutural growth (which could not be studied by SEM).     

Ontogenic development of dyadic social relationships: Assessing individual roles

Socialization processes lead to creation and differentiation of social relationships. It is often difficult to qualify them, especially due to ontogenic changes of social behavior. In this paper, an attempt is made to assess the role of each partner in a dyad by defining the quality of their overall relationship. A Social Investment Index (SII) was devised to describe these roles throughout ontogeny. SII is expressed as (G% — R%)/2, where G% and R% represent the difference between the sum of cohesive behaviors and that of disruptive behaviors divided by the overall sum of these behaviors given (G%) or received (R%) by one individual in a dyad. Results from a longitudinal study of the development of social behavior in one infant mangabey (Cercocebus albigena albigena) are used as an example. The developmental changes of the SII are presented in three dyads in a single-male group: mother-infant; “aunt”-infant; and juvenile male-infant.     

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.     

Sanje mangabey Cercocebus sanjei kills an African crowned eagle Stephanoaetus coronatus

We present the first ever reported observations of a hunting African crowned eagle Stephanoaetus coronatus being killed by a primate, in the Udzungwa Mountains of south-central Tanzania. An adult female eagle launched an attack on a young Sanje mangabey Cercocebus sanjei who was feeding in a tree, but was intercepted and bitten by an adult mangabey who was feeding nearby. The adult mangabey and the eagle then fell together 25 m to the forest floor below. The eagle subsequently died from her injuries, while the mangabey escaped and is thought to have survived. This rare event is briefly discussed in the context of previous accounts of primate-crowned eagle interactions.     

Fruit Finding by Mangabeys (Lophocebus albigena): Are Monitoring of Fig Trees and Use of Sympatric Frugivore Calls Possible Strategies?

Frugivorous forest primates face a continual challenge to locate ripe fruit due to the poor visibility characterizing a heavily vegetated habitat and the spatial and temporal unpredictability of their fruit sources. We present two hypotheses regarding fruit finding in gray-cheeked mangabeys (Lophocebus albigena). The first hypothesis is that mangabeys monitor nonfruiting fig trees by visiting and checking them for fruit at a higher rate than control trees that do not produce preferred fruit. We test this hypothesis by comparing rates of visitation to focal fig trees and control trees. The second hypothesis is that mangabeys use sympatric frugivore loud calls to locate fruit sources. We test this hypothesis (1) observationally, by comparing the rates at which mangabeys visit calling sites of sympatric frugivores and matched control areas; and (2) experimentally, by following mangabey responses to playbacks of tape-recorded calls: the black-and-white-casqued hornbill (Bycanistes subcylindricus) long call, the great blue turaco (Corythaeola cristata) rattling kok, the adult male mangabey whoopgobble, and the chimpanzee (Pan troglodytes) pant hoot. We tested the hypotheses via data from a single group of mangabeys in the Kibale National Park, Uganda. There is no evidence that mangabeys monitor fig trees for the presence of fruit, but they may use the calls of hornbills to locate fruit. Statistical evidence that mangabeys use conspecific whoopgobbles and chimpanzee pant hoots in fruit finding is lacking, though anecdotal observations suggest this possibility. There is no evidence for use of turaco calls in fruit finding.