Species,age and sex differences in type and frequencies of injuries and impairments among four arboreal primate species in Kibale National Park,Uganda

Animals in the wild often have physical impairments that can affect their fitness. The aim of this study was to compare injuries and impairments of four different primate species (black-and-white colobus, red colobus, red-tailed monkeys, and grey-cheeked mangabeys) living in Kibale National Park (Uganda), and estimate the proportion of injured and impaired individuals among the sexes and age classes. The species differed in the proportion of individuals with injuries and impairments, with 16.7% in black-and-white colobus, 23.1% in red colobus, 16.2% in red-tailed monkey and 30.2% in grey-cheeked mangabeys. Species also differed in the types and location on the body of injuries. Adult animals had more injuries than immatures. Males had more injuries than females, in all but red-tailed monkeys. The results are discussed in relation to the literature on aggressive behavior, locomotion, and predation in these species.     

Influence of food dispersion on feeding activity and social interactions in captive Lophocebus albigena and Cercocebus torquatus torquatus

We analysed the impact of the distribution of food items on feeding activity and social interactions in captive red-capped and grey-cheeked mangabeys. Three different feeding situations were presented: food items were either placed in a single heap or dispersed in several smaller heaps on the ground or in space. Social interactions were estimated by the frequency of positive, as well as of negative social interactions and by the structure of visual social attention. Feeding activity was estimated by proximity to food and feeding frequency. When food items were presented in single heaps, the adult males monopolized the food and monitoring of conspecifics increased. Social interactions and social gazes decreased in numbers when food items were dispersed in 3D. Gazes were directed more frequently towards the adult males when food items were presented in a single heap. Juveniles and some nonreproductive adult monkeys were the most affected by food competition situations. Inter-group variations, within a given species, of the behavioural responses observed in relation to the distribution of food items were evidenced. This suggests that social context, i.e., individual histories and relationship between group members, plays an important part in the expression of the activities of each member in a group.     

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.     

Reproductive parameters of captive grey-cheeked mangabeys.

This paper reports reproductive parameters for 9 female grey-cheeked mangabeys kept in a captive colony over a 17-year period. Birth seasonality has shown a consistent trend towards an autumn peak. Oestrous cycles had an average length of 31.2 days: however 'short-cycle' (29.9 days) and 'long-cycle' (37.7 days) groups could be discriminated. Gestation was 175 days, with little variability. Variability in interbirth interval is mainly due to varying length of the cycling phase preceding the next gestation, suggesting influences of social factors. All these reproductive parameters are compared to those of baboons and macaques. Some conclusions about mangabey breeding colony management are drawn.     

Patch Occupation Time Predicts Responses by Grey-Cheeked Mangabeys (Lophocebus albigena) to Real and Simulated Neighboring Groups

When two social groups are close enough to hear each other’s short-range vocalizations but not yet close enough to see each other, they can choose whether to approach to initiate a direct contest. In this study, I evaluated whether expected payoffs and group resource-holding potential affected the likelihood of approach toward a neighboring group during naturally occurring intergroup interactions and experimental playback trials by grey-cheeked mangabeys (Lophocebus albigena). Females approached calling groups at low rates, and only if males did so as well. Groups that had recently arrived (≤30 min) at the interaction location were more likely to approach than groups that were in the interaction location for >30 min. Site residency likely indicates the degree of short-term, local resource exploitation, and explains this pattern of patch defense. There was no evidence that mangabeys defended home range core or peripheral areas, that males defended female mates, or that infant defense affected the likelihood of approach. Surprisingly, resource-holding potential had no effect on patterns of contest initiation, but may influence other aspects of intergroup contests. The unexpected importance of payoff asymmetries, relative to asymmetries in resource-holding potential, points to the need for an expanded theoretical framework.     

Cercocebus torquatus: Adaptive feeding and ranging behaviors related to seasonal fluctuations of food resources in the tropical rain forest of south-western Cameroon

The feeding and ranging behaviors of mangabeys,Cercocebus torquatus torquatus Kerr (1792), were studied over two periods for a total of 15 months in south-western Cameroon between 1983 and 1986. The mangabeys showed stable food acquisition, mainly of fruits produced by canopy trees. Their ranging area, especially the core area, shifted seasonally. The fruiting trees revealed a clumped distribution in space, and provided a fluctuating food resource for frugivores, including the mangabeys. The core area of the mangabeys possibly shifted due to the spatial distribution of fruiting trees, their highest ranking food items. Mangabeys are well adapted to such a fluctuating food distribution, regulating their ranging behaviors to ensure stable food acquisition.     

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.     

The challenge of interpreting primate diets: mangabey foraging on Blighia unijugata fruit in relation to changing nutrient content

Primates often make foraging selections that are not apparent. For example, they may eagerly consume a particular plant part and species in some instances, but reject it at other times. Blighia unijugata (Baker) fruit is one of the most frequently eaten foods of mangabeys (Lophocebus albigena) in Lwamunda Forest Reserve, Uganda; however, its use varies strikingly depending on the fruit's developmental stage. We conducted feeding observations to investigate the nutritional criteria that mangabeys may have used for the consumption of specific fruit parts by conducting analysis of fruit parts eaten and rejected at different developmental stages. When seeds had low condensed tannins, mangabeys ate them, but seeds were rejected when tannin levels increased. In the first five stages of fruit development, tannin levels in arils declined and the frequency of consumption of the aril increased. Although fat content in seeds increased with maturity, it did not appear to influence seed consumption, but fat content was related to frequency of consumption of the aril. Considering that primates are often making food selections among many species/part combinations, our results illustrate the value of using nutritional analyses to understand foraging decisions. Furthermore, they demonstrate how very specific trade‐offs between consumption of critical nutrients and antifeedants can drive which foods and parts are eaten.     

Primate abundance along five transect lines at Ngogo, Kibale National Park, Uganda

Using the line transect methods, I studied the primate density at Ngogo, Kibale National Park, Uganda for 18 months. Comparisons with other studies show that the population of red colobus monkeys (Procolobus rufomitratus) and blue monkeys (Cercopithecus mitis) is declining, whereas the populations of black-and-white colobus (Colobus guereza), red-tailed monkeys (Cercopithecus ascanius), grey-cheeked mangabeys (Lophocebus albigena), baboons (Papio anubis), and chimpanzees (Pan troglodytes) remain constant or slightly increase. In this paper, I compare data on density from this study to data from previous and recent censuses at Ngogo and with data from other sites in the Kibale forest to examine the stability of primate populations. Furthermore, I test the hypothesis that the changes in red colobus and blue monkey density are due to changes in the forest structure and abundance of their most selected feeding trees, and show that changes in forest composition cannot account for changes in their red colobus abundance, but that hunting by chimpanzees provides a reasonable explanation.     

Mating Tactics in Male Grey-Cheeked Mangabeys (Lophocebus albigena)

Reproductive tactics of males can change with individual quality, relatedness and social structure. Here we describe the behaviours of male grey-cheeked mangabeys towards other males, and females and their offspring ( Lophocebus albigena ) in relation to male status (high-ranking/low-ranking/transient) and group composition in Kibale National Park, Uganda. High-ranking males had the highest mating success, frequency of loud calls, mate guarding and aggression towards females and males. Only transient males were often observed to be aggressive towards juveniles, while some high-ranking males provided infant care. Mating tactics of high-ranking males varied greatly among the five studied groups, probably as a function of the intensity of male–male competition. These results are discussed with regard to the role of male–male competition and behaviours that could affect female mate choice as tactics to obtain reproductive success.     

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.     

Indications for female mate choice in grey-cheeked mangabeys <Emphasis Type="Italic">Lophocebus albigena johnstoni</Emphasis> in Kibale National Park,Uganda

Female sexual strategies affect male strategies and can play an important role in shaping mating systems. We investigated female sexual behaviour within five groups of grey-cheeked mangabeys in Kibale National Park, Uganda, and tested the hypothesis that females exhibit mate choice using as indications the prevalence of (1) females soliciting matings by presenting to males and (2) females refusing to mate with approaching males. In addition, we describe how these behaviours as well as grooming and copulation calls are distributed over high-ranking, low-ranking and migrating males and discuss these patterns with regard to trade-offs that could play a roll in female mate choice in multi-male groups. Females were promiscuous and initiated almost half of the matings, with both resident and migrating males. More than half of male mating approaches were refused by peak females. Female mate choice in this species may depend on individual female preferences, oestrus phase and male tactic.     

Sex differences in behavior of endangered mangabeys (Cercocebus galeritus chrysogaster)

Six adult golden-bellied mangabeys (Cercocebus galeritus chrysogaster) displayed sex differences in aggression, grooming, and vocalization. These sex differences persisted across different current living conditions, time in captivity, rearing conditions, presence of offspring, and active mating conditions. The sex differences are evidently quite robust.     

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

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

Sooty mangabeys scavenge on nuts cracked by chimpanzees and red river hogs—An investigation of inter‐specific interactions around tropical nut trees

Carrion scavenging is a well‐studied phenomenon, but virtually nothing is known about scavenging on plant material, especially on remnants of cracked nuts. Just like meat, the insides of hard‐shelled nuts are high in energetic value, and both foods are difficult to acquire. In the Taï forest, chimpanzees (Pan troglodytes) and red river hogs (Potamochoerus porcus) crack nuts by using tools or strong jaws, respectively. In this study, previously collected non‐invasive camera trap data were used to investigate scavenging by sooty mangabeys (Cercocebus atys), two species of Guinea fowl (Agelestres meleagrides; Guttera verreauxi), and squirrels (Scrunidae spp.) on the nut remnants cracked by chimpanzees and red river hogs. We investigated how scavengers located nut remnants, by analyzing their visiting behavior in relation to known nut‐cracking events. Furthermore, since mangabeys are infrequently preyed upon by chimpanzees, we investigated whether they perceive an increase in predation risk when approaching nut remnants. In total, 190 nut‐cracking events were observed in four different areas of Taï National Park, Ivory Coast. We could confirm that mangabeys scavenged on the nuts cracked by chimpanzees and hogs and that this enabled them to access food source that would not be accessible otherwise. We furthermore found that mangabeys, but not the other species, were more likely to visit nut‐cracking sites after nut‐cracking activities than before, and discuss the potential strategies that the monkeys could have used to locate nut remnants. In addition, mangabeys showed elevated levels of vigilance at the chimpanzee nut‐cracking sites compared with other foraging sites, suggesting that they perceived elevated danger at these sites. Scavenging on remnants of cracked nuts is a hitherto understudied type of foraging behavior that could be widespread in nature and increases the complexity of community ecology in tropical rainforests.     

Allogrooming behavior inCercocebus torquatus: The case for the hygienic functional hypothesis

The hygienic functional hypothesis of allogrooming behavior was examined in two captive groups (N=9 andN=8) of white-crowned mangabeys (Cercocebus torquatus lunulatus) by analyzing: (1) the corporal distribution of manipulation type according to hair density, and (2) the corporal distribution of allogrooming according to presence of wounds. In both groups the sites with higher hair density received more bouts of Superficial Grooming, which implies a tactile screening of a fragment of the body surface. Only one group tended to emit more allogrooming on the body sites when they were wounded. In the other group, however, the number of wounds was very small and the wounds concentrated predominantly on those sites which were accessible to the subject itself. Thus, our results may be consistent with the hygienic functional hypothesis of allogrooming behavior in general and with the sanitary one in particular.     

Hardness of cercopithecine foods: implications for the critical function of enamel thickness in exploiting fallback foods

We evaluate the hardness of foods consumed by sympatric Cercopithecus ascanius (redtail guenons) and Lophocebus albigena (grey-cheeked mangabeys), and consider how selection might operate to influence foraging adaptations. Since L. albigena has among the thickest dental enamel in extant primates and is commonly referred to as a hard-object consumer, we predicted that their diet would be harder than that of the guenon. Data on diet and food hardness (as measured by resistance to puncture and crushing) were collected between June-October of 1997 at Kibale National Park, Uganda, and were compared to similar data collected in Kibale between 1991-1994. Contrary to what we predicted, there was no difference in dietary hardness when the puncture resistance of all fruit consumed by the two species was compared (31 tree species in both study periods). However, in June-October 1997, L. albigena exploited a diet more resistant to puncture and crushing than C. ascanius. This difference is largely explained by the higher percentage of bark and seeds consumed by the L. albigena during this period. We suggest that it is the difference in the mechanical properties of fallback foods during critical periods that may have served as the selective pressure for thick enamel in L. albigena.     

Associations between the drill (Mandrillus leucophaeus) and sympatric monkeys in Korup National Park,Cameroon

Studies of polyspecific associations among African forest primates have primarily focused on arboreal Cercopithecus and Procolobus/Colobus species. We examined the association frequency of the terrestrial drill (Mandrillus leucophaeus) with six sympatric monkey species in Korup National Park, Cameroon, testing reports that Mandrillus associations are infrequent and transient. We conducted 3,284 km of trail walks for 12 months (February–June 2006; July 2007 to January 2008), recording species composition in 612 primate clusters. Using a Markov chain Monte Carlo test, we compared the observed frequency of dyadic associations against null models of “no association.” A novel conservative statistical approach which addresses possible dependence of observations close in time was also used, further strengthening confidence in our findings. Drills associated with all monkeys throughout the study period, and were with at least one other species (range 1–5) in half of the encounters. The association frequency of drills with red‐capped mangabeys (Cercocebus torquatus) was greater than expected by chance, which is interesting given the morphological adaptation of the Mandrillus‐Cercocebus clade for the exploitation of the same dietary niche, hard seeds. The difference we observed in the use of forest strata by drills and mangabeys may reflect a strategy to reduce food competition while in association. The nature and duration of observed drill associations varied. Although some associations seemed to be chance encounters, others lasted for hours with the involved species foraging together. Am. J. Primatol. 73:127–134, 2011. © 2010 Wiley‐Liss, Inc.     

Threats to observers,keepers, visitors,and others by zoo mangabeys (Cercocebus galeritus chrysogaster)

The facial threats of ten captive golden-bellied mangabeys (Cercocebus galeritus chrysogaster) were categorized by object threatened. Adult males threatened more than did females except when the object was a nonhuman primate in a neighboring cage. Juvenile mangabeys threatened mainly in play within their own enclosures. Keepers and observers did not differ in frequency of being threatened by the mangabeys. Adult female mangabeys seemed more concerned with neighboring cages of nonhuman primates than were the juveniles and the males. Human visitors to the enclosures received by far the most threats of any targets, certainly far more than the observers and keepers. They were treated like interlopers. Keepers were treated like familiar conspecifics, observers like familiar neighbors. The implications of these findings for captive management of primates and for observational methods in behavioral primatology are discussed.     

Lag period for phototropism inPilobolus crystallinus sporangiophores

The lag period for the second positive curvature was examined inPilobolus crystallinus sporangiophores. The lag period for curvature development was 20–30 min at lower fluence rates than 6.32 nmol/m²s but greatly extended at higher fluence rates. When a 20-min symmetrical irradiation with blue light was applied before a 20-min unilateral blue light irradiation, sporangiophores bent as much as those unilaterally and continuously irradiated for 40 min. However, when a 20-min unilateral irradiation was followed by a 20-min symmetrical irradiation, sporangiophores did not show any curvature. That is, the reaction during the first 20 min of the lag period is independent of light direction. This light-direction-independent lag period is considered to be the duration required for adaptation. The lag period for phototropism was also extended when fluence rate was reduced after the start of irradiation. These results suggested that an adaptation process is involved in phototropism ofPilobolus.