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Reproductive parameters and life-history variables in captive golden-bellied mangabeys (Cercocebus agilis chrysogaster).

An understanding of the reproductive physiology of captive primates is vital for their successful management. We report on reproductive parameters and life-history variables collected at the Sacramento Zoo for five female golden-bellied mangabeys (Cercocebus agilis chrysogaster) over a 7-year period. For each female, we collected data on their sexual skins, menses, gestation, and other pregnancy-related factors, such as postconception bleeding and swelling. We used these data to estimate life-history variables, such as age at onset of estrus, menses, and conception, as well as the duration of intervals between births, and between parturition and the resumption of cycling. Cercocebus agilis chrysogaster is comparable to other Cercocebus species in terms of reproductive parameters, although variability is exhibited within and among female subjects. In some cases, it appears that stressful incidents altered cycle length or halted cycling altogether. We suggest the use of husbandry practices that include consistent data collection to enhance regularity in reproductive cycles, and maximize captive breeding success for this rare species.

Animal Husbandry↗

Isolation and characterization of simian immunodeficiency virus from African white-crowned mangabey monkeys (Cercocebus torquatus lunulatus).

Forty-eight of 236 sera from seven species of African non-human primates in Kenya, including those of white-crowned mangabey monkeys (Cercocebus torquatus lunulatus) had antibodies to simian immunodeficiency viruses (SIVs). Isolates of simian lentivirus were obtained from seropositive white-crowned mangabey monkeys which are indigenous in West Africa. This virus, designated as SIVWCM, appeared morphologically similar to HIV by electron microscopy, showed Mg(2+)-dependent reverse transcriptase activity, and induced cytopathic effects in human CD4-positive cells. Western blotting analysis revealed that env products of SIVWCM cross-reacted with those of SIVAGM more strongly than with those of HIV-1 and SIVMAC, and clear hybridization bands were detected with an SIVAGM probe. For comparison of the virus sequence with those of other primate lentiviruses, part of the pol gene and the long terminal repeats (LTRs) were amplified and cloned. Sequencing showed that SIVWCM isolates were closely related to SIVAGM isolates. This study suggested that SIVAGM from the Cercopithecus genus and SIVWCM from the Cercocebus genus may be members of an SIV group that is genetically distinct from the SIV from a sooty mangabey monkey (SIVSMM) of the genus Cercocebus, to which the white-crowned mangabey monkey also belongs.

Animals↗

Does allogrooming serve a hygienic function in Cercocebus torquatus lunulatus?

To test the hygienic functional hypothesis of allogrooming in the white-crowned mangabey (Cercocebus torquatus lunulatus), we analyzed the distribution of such behavior over the body surface in the individuals of two captive groups of this species (N = 9 and N = 8). To sample the data, we used focal animal sampling and continuous recording. Before analyzing the data, we measured a representative subject in order to calculate the body surface area occupied by each site, defined accessibility rigorously (distinguishing among three categories of sites: easy to reach, difficult to reach, and inaccessible), and tested empirically the classification proposed. To determine whether allogrooming was likely to concentrate on the body sites with accessibility problems, we ran three successive analyses, each of with was increasingly specific: grouping types of sites, analyzing each site separately, and analyzing each subject's reception profile. The results obtained show that in both groups inaccessible sites received more allogrooming than predicted by their actual surface area; sites that were difficult to reach received an amount of allogrooming proportional to the body surface area they occupied, and those easy to reach received less allogrooming than expected. This complementarity between the distribution of auto- and allogrooming is consistent with the hygienic functional hypothesis of allogrooming. However, not all inaccessible sides nor those difficult-to-reach were allogroomed equally: Allogrooming concentrated primarily on dorsal and caudal regions, whose care is incompatible with a ventral/ventral orientation between groomer and groomee. The strong distributional selectivity of allogrooming and the interindividual variability in preferred allogrooming sites suggest that the hygienic functional hypothesis cannot fully account for all the aspects of the corporal distribution of such behavior. Thus, in support of the multifunctional nature of allogrooming, we conclude that there must be more than cleaning involved in Cercocebus torquatus lunulatus' allogrooming.

Animals↗

Molecular epidemiology of simian T-lymphotropic virus (STLV) in wild-caught monkeys and apes from Cameroon: a new STLV-1, related to human T-lymphotropic virus subtype F, in a Cercocebus agilis.

A serological survey for human T-lymphotropic virus (HTLV)/simian T-lymphotropic virus (STLV) antibodies was performed in 102 wild-caught monkeys and apes from 15 (sub)species originating from Cameroon. Two animals (a Mandrillus sphinx and a Cercocebus agilis) exhibited a complete HTLV-1 seroreactivity pattern while two others lacked either the p24 (a Mandrillus sphinx) or the MTA-1/gp46 bands (a Pan troglodytes). Sequence comparison and phylogenetic analyses, using a 522 bp env gene fragment and the complete LTR, indicated that the two mandrill STLV strains belonged to the HTLV/STLV subtype D clade while the chimpanzee strain clustered in the HTLV/STLV subtype B clade. The Cercocebus agilis STLV strain, the first one found in this species, was closely related to the two HTLV/STLV subtype F strains. Such data indicate that the African biodiversity of STLV-1 in the wild is far from being known and reinforces the hypothesis of interspecies transmission of STLV-1 from monkeys and apes to humans leading to the present day distribution of HTLV-1 in African inhabitants.

Animals↗

Simian T-cell leukemia virus (STLV) infection in wild primate populations in Cameroon: evidence for dual STLV type 1 and type 3 infection in agile mangabeys (Cercocebus agilis).

Three types of human T-cell leukemia virus (HTLV)-simian T-cell leukemia virus (STLV) (collectively called primate T-cell leukemia viruses [PTLVs]) have been characterized, with evidence for zoonotic origin from primates for HTLV type 1 (HTLV-1) and HTLV-2 in Africa. To assess human exposure to STLVs in western Central Africa, we screened for STLV infection in primates hunted in the rain forests of Cameroon. Blood was obtained from 524 animals representing 18 different species. All the animals were wild caught between 1999 and 2002; 328 animals were sampled as bush meat and 196 were pets. Overall, 59 (11.2%) of the primates had antibodies cross-reacting with HTLV-1 and/or HTLV-2 antigens; HTLV-1 infection was confirmed in 37 animals, HTLV-2 infection was confirmed in 9, dual HTLV-1 and HTLV-2 infection was confirmed in 10, and results for 3 animals were indeterminate. Prevalences of infection were significantly lower in pets than in bush meat, 1.5 versus 17.0%, respectively. Discriminatory PCRs identified STLV-1, STLV-3, and STLV-1 and STLV-3 in HTLV-1-, HTLV-2-, and HTLV-1- and HTLV-2-cross-reactive samples, respectively. We identified for the first time STLV-1 sequences in mustached monkeys (Cercopithecus cephus), talapoins (Miopithecus ogouensis), and gorillas (Gorilla gorilla) and confirmed STLV-1 infection in mandrills, African green monkeys, agile mangabeys, and crested mona and greater spot-nosed monkeys. STLV-1 long terminal repeat (LTR) and env sequences revealed that the strains belonged to different PTLV-1 subtypes. A high prevalence of PTLV infection was observed among agile mangabeys (Cercocebus agilis); 89% of bush meat was infected with STLV. Cocirculation of STLV-1 and STLV-3 and STLV-1-STLV-3 coinfections were identified among the agile mangabeys. Phylogenetic analyses of partial LTR sequences indicated that the agile mangabey STLV-3 strains were more related to the STLV-3 CTO604 strain isolated from a red-capped mangabey (Cercocebus torquatus) from Cameroon than to the STLV-3 PH969 strain from an Eritrean baboon or the PPA-F3 strain from a baboon in Senegal. Our study documents for the first time that (i) a substantial proportion of wild-living monkeys in Cameroon is STLV infected, (ii) STLV-1 and STLV-3 cocirculate in the same primate species, (iii) coinfection with STLV-1 and STLV-3 occurs in agile mangabeys, and (iv) humans are exposed to different STLV-1 and STLV-3 subtypes through handling primates as bush meat.

Animals↗

Further description of blood stages of Plasmodium petersi from Cercocebus albigena monkey.

Additional information is given on the erythrocytic stages of Plasmodium petersi (Poirriez, Baccam, Dei-Cas, Brogan et Landau, 1933), which was found in a Cercocebus albigena monkey from the Central-African Republic. The first colour pictures of P. petersi are presented. In 60% of young trophozoites, the vacuole is divided into two or three parts by thin cytoplasmic streaks. In young trophozoites and almost mature schizonts, 80% of nuclei are oval or kidney-shaped; they are two-coloured; measurement of their surface area shows that it is about twice that of the nuclei of P. gonderi at the same stages. Studies using polarised light show that most of the pigment granules are elongated (spindle-shaped) and found at the periphery of old trophozoites and schizonts. P. petersi can easily be distinguished from P. gonderi and P. georgesi, the two other species found so far in Cercocebus monkeys, which are regarded as the African equivalents of the Asian macaques.

Animals↗

The banded karyotypes of Macaca fuscata compared with Cercocebus aterrimus.

The karyotypes of Macaca fuscata and Cercocebus aterrimus are compared after G, C and AgNOR banding. Although it is often assumed that the 42-chromosome monkeys (species of the genera Macaca, Papio, and Cercocebus) are identical at the chromosomal level, a number of clear and consistent differences between the karyotypes of these two taxa are described. These differences include one pericentric inversion and differences in staining intensity, particularly in centromeric and pericentromeric areas. It is probable that high resolution chromosome techniques could reveal more differences between taxa in the 42-chromosome group than are now believed to exist. It is therefore probable that karyological data could provide insight into the phylogenetic relationships in this group of Old World monkeys.

Animals↗

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).

Animals↗

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.

Animals↗

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.

Animals↗

Female sooty mangabeys (Cercocebus torquatus atys) respond differently to males depending on the male's residence status-preliminary data.

I tested the hypothesis that free-ranging female mangabeys (Cercocebus torquatus atys) differentiate between males depending on their residence status. Adult males in this species employ two group-membership strategies: they are either full-time residents or part-time residents (i.e., present for several weeks at a time, then gone for several weeks, then present again, etc.). In a playback experiment I tested whether adult females with young infants responded differently to calls of adult males that were group members during the previous mating season as compared to males that belonged to neighboring groups during the mating season or were complete strangers. Males whose calls were played were present residents, part-time residents (absent for at least 3 months), neighbors, or complete strangers. Because infanticide is a potential risk in mangabeys, I predicted that females would respond differently to males that had resided in the group when their infant was conceived than they would to those that had not been present. The females showed a clear difference in their reaction to the playbacks of vocalizations from resident and part-time resident males as opposed to nonresidents.

Acoustic Stimulation↗

Hand preference in unimanual and bimanual tasks and postural effect on manual laterality in captive red-capped mangabeys (Cercocebus torquatus torquatus).

Hand preference in 11 captive red-capped mangabeys (Cercocebus torquatus torquatus) was examined under different conditions: a free situation during spontaneous food processing, three different postural conditions (brachiating, and bipedal and tripedal standing), and a situation involving bimanual processing. Generally, individual laterality was found regardless of the task and behavior involved. However, the number of monkeys with hand preferences and the strength of the preference increased with the complexity of the tasks. The monkeys exhibited a significantly higher and positive mean manual preference index (HI) when they were hanging than when they were quadrupedal or sitting. The strength of manual preference (ABS-HI) was in turn higher when the monkeys were hanging or bipedal than when they were quadrupedal. The strength of manual preference was higher for both the bimanual and experimental tasks than for unimanual tasks and spontaneous activities. Although our sample was too small to allow us to make any generalizations concerning lateral preferences in red-capped mangabeys, we propose some hypotheses about the influence of posture stability and task complexity.

Analysis of Variance↗

Examination of increased annual range of a Tana mangabey (Cercocebus galeritus) group.

A group of Tana mangabeys (Cercocebus galeritus) has greatly expanded its annual range over three decades: from 17.25 hectares (ha) in 1974 (Homewood [1976] Ph.D. dissertation, University College London) and 18.75 ha in 1988-1989 (Kinnaird [1990a] Ph.D. dissertation, University of Florida) to 46.75 ha in 2000-2001. Utilizing 5-min mapping samples, phenological samples, vegetation data, and statistical and descriptive comparisons with previous data, three hypotheses concerning this range increase were postulated. The hypothesis with the strongest support is an increase in intragroup feeding competition, which was measured by a decrease in fruit availability per hectare and an increase in group size. Fruit biomass estimates of four species individually and of eight species combined showed significant decreases between earlier findings (Kinnaird [1990] Ph.D. dissertation, University of Florida) and this study. Group size decreased from 36 in 1974 to 17 in 1988-1989, and is now 50 individuals. There is no support for the hypotheses that the group is no longer constrained in home range size by neighboring groups or by the extent of forest cover. The changes in group and home range size are also discussed in the context of historical forest loss in the lower Tana River. The ability of the Tana mangabey to increase its home range, especially by traveling through nonforest habitat, is an important aspect of its ecological flexibility in a fragmented and threatened habitat.

Animals↗

Sooty mangabey (Cercocebus torquatus atys) IGHG and IGHA genes.

Antibodies are adaptor molecules of the immune system that link antigen recognition with the effector mechanisms responsible for antigen clearance. Several nonhuman primate species are widely used in biomedical research, especially for vaccine development and for AIDS-related studies. However, nonhuman primate antibody molecules have been characterized only partially and only in a few species. Here, we describe sooty mangabey (Cercocebus torquatus atys) IGHG and IGHA genes, which encode the heavy-chain constant region of IgG and IgA molecules, respectively. The four mangabey IGHG genes are highly homologous to the rhesus macaque and baboon IGHG genes (percent identity varies between 94.0 and 98.8, depending on the subclass), with most amino acid differences located in the hinge regions. Results obtained by real-time reverse transcription polymerase chain reaction show that the four IGHG genes are expressed at least at the mRNA level. The mangabey IGHA gene is highly homologous to the corresponding gene from rhesus macaques (percent identity ranges from 88.6 to 96.7, depending on the allele considered), the only other nonhominoid primate species for which the complete sequence of the IGHA gene is currently available. In the mangabey analyzed, two IGHA alleles are present, confirming that high levels of IGHA gene heterozygosity are present in monkey species. These results show that nonhuman primate gamma and alpha heavy chains differ from each other mostly at the level of the hinge region and that alpha sequence heterogeneity in nonhuman primate species is also present in other gamma regions. In addition, these results provide sequence information that can be used for residue frequency analysis of antibody heavy-chain constant region sequences.

Amino Acid Sequence↗

Learning to outwit a competitor in mangabeys (Cercocebus torquatus torquatus).

To investigate whether monkeys would be able to acquire the location of hidden food from the experimenter and later from an informed conspecific, a group of 7 mangabeys (Cercocebus torquatus torquatus) was tested in an experimental design comparable to Menzel's (1974) with chimpanzees. Food was hidden in the presence of particular animals. An informed young male repeatedly lost his food to a dominant male. Accordingly, the young male developed a pattern, when he alone was informed, of moving in an indirect route to the goal, which generally functioned to mislead the dominant male to the young male's advantage. When the dominant male was also informed, the young male observed the dominant male taking the food or headed straight to the remaining hidden goal. His taking an indirect route, when he alone was informed, cannot therefore be considered his expected response to a competitive situation but rather is a case of tactical deception.

Animal Communication↗

Facial growth in Cercocebus torquatus: an application of three-dimensional geometric morphometric techniques to the study of morphological variation.

This paper presents a study of 3-dimensional growth in the facial skeleton of the mangabey, Cercocebus torquatus. The pattern of facial cortical remodelling in this species is already well mapped from an earlier study. In this paper we consider the extent to which these remodelling maps relate to ontogenetic changes in size and shape of the face. This study is based on 31 facial landmarks taken from 49 adult and subadult faces. Our analysis draws on some of the tools of geometric morphometrics and we take this opportunity to describe our implementation of these tools for 3D data. The geometric analysis permits the known remodelling maps to be interpreted in the context of the general pattern of facial growth in this species. We are also able to examine sexual dimorphism in the face of this species and consider the extent to which males and females share similar ontogenetic allometries. Our findings indicate that the general pattern of size-related shape variation during facial growth is more or less identical for males and females up to eruption of the third permanent maxillary molar (M3). After this, ontogenetic allometries appear to diverge. The finding of a common growth allometry that is well approximated for younger specimens by a simple linear model is consistent with the earlier findings of a consistent pattern of facial remodelling up to M3 eruption. We consider the implications of these findings in terms of the potential for these approaches in the study of comparative growth in related species.

Animals↗