Parasitology of five primates in Mahale Mountains National Park, Tanzania

Parasitological surveillance in primates has been performed using coprological observation and identification of specimens from chimpanzees (Pan troglodytes schweinfurthii) in Mahale Mountains National Park, Tanzania (Mahale). In this study, we conducted coprological surveillance to identify the fauna of parasite infection in five primate species in Mahale: red colobus (Procolobus badius tephrosceles), red-tailed monkeys (Cercopithecus ascanius schmidti), vervet monkeys (Cercopithecus aethiops pygerythrus), yellow baboons (Papio cynocephalus), and chimpanzees. Fecal samples were examined microscopically, and parasite identification was based on the morphology of cysts, eggs, larvae, and adult worms. Three nematodes (Oesophagostomum spp., Strongyloides sp., and Trichuris sp.), Entamoeba coli, and Entamoeba spp. were found in all five primate species. The following infections were identified: Bertiella studeri was found in chimpanzees and yellow baboons; Balantidium coli was found in yellow baboons; three nematodes (Streptopharagus, Primasubulura, an undetermined genus of Spirurina) and Dicrocoeliidae gen. sp. were found in red-tailed monkeys, vervet monkeys, and yellow baboons; Chitwoodspirura sp. was newly identified in red colobus and red-tailed monkeys; Probstmayria gombensis and Troglocorys cava were newly identified in chimpanzees, together with Troglodytella abrassarti; and Enterobius sp. was newly identified in red colobus. The parasitological data reported for red colobus, vervet monkeys, and yellow baboons in Mahale are the first reports for these species.     

Suffixation influences receivers' behaviour in non-human primates

Compared to humans, non-human primates have very little control over their vocal production. Nonetheless, some primates produce various call combinations, which may partially offset their lack of acoustic flexibility. A relevant example is male Campbell''s monkeys (Cercopithecus campbelli), which give one call type (‘Krak’) to leopards, while the suffixed version of the same call stem (‘Krak-oo’) is given to unspecific danger. To test whether recipients attend to this suffixation pattern, we carried out a playback experiment in which we broadcast naturally and artificially modified suffixed and unsuffixed ‘Krak’ calls of male Campbell''s monkeys to 42 wild groups of Diana monkeys (Cercopithecus diana diana). The two species form mixed-species groups and respond to each other''s vocalizations. We analysed the vocal response of male and female Diana monkeys and overall found significantly stronger vocal responses to unsuffixed (leopard) than suffixed (unspecific danger) calls. Although the acoustic structure of the ‘Krak’ stem of the calls has some additional effects, subject responses were mainly determined by the presence or the absence of the suffix. This study indicates that suffixation is an evolved function in primate communication in contexts where adaptive responses are particularly important.     

Drinking competition in vervet monkeys

During a period of water shortage, adult female and adult male vervet monkeys (Cercopithecus aethiops) obtained water by different methods. Females drank from tree-holes within their normal home range, while males invaded the territories of neighbouring groups. Higher-ranking females had access to preferred tree-holes. The mortality rate was high in both sexes and was greater in low-ranking than in high-ranking animals.     

High Prevalences and a Wide Genetic Diversity of Simian Retroviruses in Non-human Primate Bushmeat in Rural Areas of the Democratic Republic of Congo

Like the majority of emerging infectious diseases, HIV and HTLV are of zoonotic origin. Here we assess the risk of cross-species transmissions of their simian counterparts, SIV and STLV, from non-human primates (NHP) to humans in the Democratic Republic of Congo (DRC). A total of 331 samples, derived from NHP bushmeat, were collected as dried blood spots (DBS, n = 283) or as tissue samples (n = 36) at remote forest sites mainly in northern and eastern DRC. SIV antibody prevalences in DBS were estimated with a novel high throughput immunoassay with antigens representing the actual known diversity of HIV/SIV lineages. Antibody-positive samples were confirmed by PCR and sequence analysis. Screening for STLV infection was done with universal primers in tax, and new strains were further characterized in LTR. SIV and STLV infection in tissue samples was done by PCR only. Overall, 5 and 15.4% of NHP bushmeat was infected with SIV and STLV, respectively. A new SIV lineage was identified in Allen’s swamp monkeys (Allenopithecus nigroviridis). Three new STLV-1 subtypes were identified in Allen’s swamp monkeys (Allenopithecus nigroviridis), blue monkeys (Cercopithecus mitis), red-tailed guenons (Cercopithecus ascanius schmidti) and agile mangabeys (Cercocebus agilis). SIV and STLV prevalences varied according to species and geographic region. Our study illustrates clearly, even on a small sample size from a limited number of geographic areas, that our knowledge on the genetic diversity and geographic distribution of simian retroviruses is still limited and that humans continue to be exposed to relative high proportions on infected NHP bushmeat.     

Observations on the ecology and social organization of the green monkey,Cercopithecus sabaeus,in Senegal

The green monkey,Cercopithecus sabaeus, has not been studied in its natural habitat in West Africa. This paper reports observations made during a 3-month study in Senegal. Green monkeys live in multimale groups averaging some 12 individuals. Information is given on home range size, use of habitat, daily activity patterns, diet and birth seasonality. Social organization is discussed and data are given on the relationships between age-sex classes, aggression and leadership. Inter-group relations are discussed and it is suggested that groups defend their ranges as territories. The ecology and social organization of green monkeys is compared with that of populations ofC. aethiops studied in East Africa and they are found to be similar.     

Relationships among adult females in captive vervet monkeys: Testing a model of rank-related attractiveness

Data from three captive groups of vervet monkeys (Cercopithecus aethiops sabaeus) were used to test predictions from Seyfarth's (1977) model of rank-related attractiveness. Grooming patterns among adult females were consistent with the model's predictions. There was also evidence that females compete for access to the alpha female, as would be predicted by the model. This study failed to provide evidence for reciprocal support in agonistic encounters based on proximity relationships, independent of kinship.     

Positional Behavior of Cercopithecus petaurista

I studied the positional behavior and habitat use of Cercopithecus petaurista, the lesser spot-nosed monkey, in the Ivory Coast's Taï Forest for 15 months. I compare these data with similar information collected on sympatric groups of Cercopithecus diana and C. campbelli in order to examine further the relationships between locomotion, posture, support use, stratal use, body size, diet, activity patterns and foraging behavior. Spot-nosed monkeys are predominantly quadrupedal primates that frequent the top layer of the understory during all maintenance activities. Locomotion is characteristically slow and cautious; travel takes place on branches and boughs while foraging occurs on twigs and branches. Postural behavior of Cercopithecus petaurista reflects their reliance on more ubiquitously distributed, less mobile food items. The relationship between body size, climbing, leaping and support use among Taï guenons is weak; interspecific differences are more likely functions of strata use and overall behavioral characteristics, e.g. crypticity. I also compare the locomotion and support use of Cercopithecus petaurista with that of C. ascanius from Uganda's Kibale Forest (Gebo and Chapman, 1995a) in order to assess the behavioral similarity of members of the same superspecies. Although overall support use is quite similar, the monkeys differ significantly in frequencies of quadrupedism, leaping and climbing. I present possible reasons for and implications of these differences.     

Spatial distribution of primates in a mosaic of colonizing and old growth forest at Ngogo, Kibale National Park, Uganda

Primate censuses were conducted in a mosaic of colonizing (two locations) and old-growth forests using line transect methods at the Ngogo study site, Kibale National Park, Uganda. Black and white colobus monkeys (Colobus guereza) were encountered more frequently in the colonizing forests than in the old growth forest, while chimpanzees (Pan troglodytes) were encountered more frequently in the old growth forest than in colonizing forests. Although not significant, results suggest that blue monkeys (Cercopithecus mitis) frequented colonizing forests more often than old growth forest. The encounter rates of mangabey (Lophocebus albigena), and redtail (Cercopithecus ascanius) groups were ambiguous with their density being higher in some colonizing forests but not others as compared to old-growth forest. No significant differences were detected for baboons (Papio anubis), Lhoests (Cercopithecus lhoesti), and red colobus monkeys (Piliocolobus tephroscales). The conversion of forests to farmland is one of the major problems encountered in primate conservation. This study shows that secondary forests replacing anthropogenic grasslands have the potential of supporting some primate species such as black and white colobus, redtail monkeys, and possibly blue monkeys. Therefore, such areas should not be given up but should be conserved for the benefit of primates that can survive in secondary forests; as the forests mature further, primate species that are adapted to old growth forest will colonize the area provided there is a nearby source.     

Cheek pouch use in relation to interspecific competition and predator risk for three guenon monkeys (Cercopithecus spp.)

Forest guenons (Cercopithecus spp.) are often found in polyspecific associations that may decrease predator risk while increasing interspecific competition for food. Cheek pouch use may mitigate interspecific competition and predator risk by reducing the time spent in areas of high competition/predator risk. I investigated these ideas in three forest guenons: Campbell’s monkey (Cercopithecus campbelli), spot-nosed monkey (C. petaurista), and Diana monkey (C. diana). I present 13 months of scan sample data from Taï Forest, Côte d’Ivoire, including 3,675, 3,330, and 5,689 records of cheek pouch distention, to quantify cheek pouch use, for Campbell’s, spot-nosed, and Diana monkeys, respectively. Cheek pouches are often used to hold fruit, so I first predicted that the most frugivorous species, Diana monkeys, would have the most cheek pouch distension. Spot-nosed monkeys ate the least amount of fruit over the study period and had the least distended cheek pouches, suggesting the importance of frugivory in relation to cheek pouch distension for this species. This was not a sufficient explanation for Campbell’s monkeys; Campbell’s ate fruit less than Diana monkeys, but had more distended cheek pouches, suggesting that cheek pouch use was not simply a reflection of high frugivory. From the interspecific competition hypothesis, I predicted that Campbell’s monkeys would have more distended cheek pouches than Diana and spot-nosed monkeys, and more distended cheek pouches when associated with Diana because Campbell’s monkeys have the highest potential for interspecific competition with dominant Diana monkeys. From the predator risk hypothesis, I predicted that Campbell’s would have more distended cheek pouches when not associated with highly vigilant Diana monkeys. Campbell’s monkeys had the most distended cheek pouches overall, but had more distended cheek pouches when not in association with Diana, suggesting the greater importance of predator risk rather than interspecific competition in Campbell’s cheek pouch use.     

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.     

Role of local culture,religion, and human attitudes in the conservation of sacred populations of a threatened ‘pest’ species

Indigenous belief systems and informal institutions that result in the conservation of wild species or sites exemplify biocultural conservation. The erosion of cultural beliefs and practices can have adverse, often severe, consequences for biodiversity. We explored the relationships among informal institutions, religion, and human attitudes toward sacred populations of a threatened, endemic species, Sclater’s monkey (Cercopithecus sclateri), in two communities in southeastern Nigeria. Due to habitat loss and hunting pressure across the species’ range, monkeys in these two sites live alongside people, raid farms and gardens, and are commonly viewed as pests. Using structured (n = 410) and semi-structured (n = 21) interviews, we examined factors influencing residents’ views of the monkeys, mechanisms affecting adherence to social taboos against harming monkeys, and implications for conservation. Our analyses revealed that most residents, particularly those from one community, women, and farmers, held negative opinions of the monkeys. Crop and garden raiding by monkeys had the most adverse effect on people’s attitudes. Although the adoption of Christianity weakened residents’ views regarding the no-killing taboos, continued adherence to the taboos was particularly influenced by supernatural retribution in one site and community disapproval in the other. Only one community widely conferred symbolic importance on the monkeys. Such site differences illustrate the value of local cultural understanding in conservation. Pre-intervention studies of this nature allow for the development of locally and culturally sensitive conservation programs, as well as better-informed assessments of what interventions are most likely to be effective.     

Upperlimb skeletal elements of miocene cercopithecoids from east Africa: Implications for function and taxonomy

Old collections and unpublished newly-discovered specimens of Miocene cercopithecoids studied here include humeri and proximal ulnae from Maboko (KNM MB 2, KNM MB 3, KNM MB 19, KNM MB 32, KNM MB 12038, KNM MB 12044), Nyakach (KNM NC 9824) in Kenya and from Napak (NAP V-8.85) in Uganda. This work leads to the conclusion that two different groups of monkeys may have co-existed in East Africa in the Middle Miocene. After comparison with extant cercopithecoids (Colobus polykomos, Colobus badius, Colubus angolensis, Colobus guereza, Cercopithecus aethiops, Cercopithecus ascanius, Nasalis larvatus, Presbytis entellus and severalPapio andMacaca), the fossils can be divided into two morphological groups. In the distal humerus, the shape of thetrochlea humeri and the orientation of theepicondylus medialis are distinctive; in the ulnae, the distinction is mainly based on the morphology of theincisura trochlearis. Thus, we would have a more terrestrial group and a more arboreal one. The differences (not linked with sex) are large enough to indicate a taxonomic difference (as proposed on the teeth collected to the same sites, by several authors). At this stage, we cannot assign with certainty the specimens to one taxon or the other (Victoriapithecus macinnesi orVictoriapithecus leakeyi).     

Better to Live with Allogenerics Than to Live Alone? The Case of Single Male Cercopithecus pogonias in Troops of Colobus satanas

We report the integration of single male crowned guenons (Cercopithecus pogonias) into troops of black colobus (Colobus satanas). We observed one male Cercopithecus pogonias in three troops of Colobus satanas on 30% of observation days (n = 231). Activities of single males guenons did not differ significantly from those of the colobus with which they associated. Moreover, both species performed simultaneously the same activities more often than expected by chance. Interspecific grooming occurred on several occasions. Furthermore, single male guenons spent as much in time social activities when part of a colobus troop, as they typically do when part of a conspecific group. Unlike solitary male crowned guenons, which are silent, a male that is integrated into a troop of colobus is vocal and emits social alarm calls to which colobus monkeys respond. During the single file movements of colobus troops, single male crowned guenons were integrated in the core of the troop and used the same branches at the same height with the colobus. Thus, the life of a single male crowned guenon with black colobus was social. We suggest that the main benefits that he gained is the possibility to live in a social context. Social interactions could be the key element to explain why single males Cercopithecus pogonias join troops of monkeys so different from their natal groups.     

Cooperation and competition in two forest monkeys

Putty-nosed monkeys, Cercopithecus nictitans stampflii, occurat various sites in West Africa, particularly in the transitionzone between rainforest and savannah. The species is sometimesseen in primary rainforest, although at a curiously low densitycompared with that of other monkey species. We conducted a 24-monthfield study in the tropical rainforest of Taï NationalPark, Ivory Coast, and found that putty-nosed monkeys requirean ecological niche almost identical to that of the Diana monkeys,Cercopithecus diana diana. Moreover, the niche breadth of putty-nosedmonkeys was significantly decreased in the presence of Dianamonkeys, suggesting that feeding competition with Diana monkeyskept putty-nosed monkeys from successfully colonizing a rainforesthabitat. However, contrary to the interspecies competition hypothesis,groups of both species almost completely overlapped in homeranges and formed near-permanent mixed-species associations,rather than avoiding each other. We hypothesized that Dianamonkeys tolerated immigrating putty-nosed monkeys and formedmixed-species groups with them, despite high levels of competition,because of their merit in predation defense. Direct observationsand a series of field experiments confirmed that male putty-nosedmonkeys play a vital role in defense against crowned eagles,suggesting that putty-nosed monkeys obtain access to feedingtrees by offering antipredation benefits to Diana monkeys. Wediscuss these findings in light of biological market theory.     

Influence of Chimpanzee Predation on Associations Between Red Colobus and Red-tailed Monkeys at Ngogo,Kibale National Park,Uganda

Colobines often associate with cercopithecines at various African sites. Such polyspecific associations presumably have an antipredation function. At Ngogo, Kibale National Park, Uganda, red colobus (Procolobus rufomitratus) spend considerable time in association with red-tailed monkeys (Cercopithecus ascanius), and they are also heavily hunted by chimpanzees (Pan troglodytes). I conducted behavioral observations and playback experiments to test the hypothesis that red colobus and red-tailed monkeys obtain mutual protection and predator-related benefits by associating. Despite high chimpanzee hunting pressure on red colobus and much lower hunting pressure on red-tailed monkeys, red-tailed monkeys initiate, maintain, and terminate the associations. The results suggest that rather than providing red colobus with protection against chimpanzees, the associations occur mostly because they protect red-tailed monkeys against predation by eagles.     

Enzootic simian piroplasm (Entopolypoides macaci ) in wild-caught Kenyan non-human primates

Background Three species of non‐human primates comprising African green monkeys (AGMs), (Cercopithecus aethiops, n = 89), Syke’s monkeys (Cercopithecus mitis, n = 60) and olive baboons (Papio cynocephalus anubis, n = 30), were screened for Entopolypoides macaci. Methods Observation of blood smears prepared from these animals revealed E. macaci infection rate of 42.7% in AGMs, 35% in Syke’s monkeys and 33.3% in baboons. Results Gender infection rate was 38.2% in females and 29% in males. Statistically, there was no significant difference in infection rates between the monkey species and sexes (P > 0.05). Subsequent indirect immuno fluorescent antibody test supported the morphological appearance of E. macaci observed by microscopy. Sera from infected animals reacted positively (1:625) with E. macaci antigen, but not to Babesia bigemina or B. bovis antigen at 1:125 titer. Conclusion This study has revealed high prevalence of E. macaci infection in all three widely distributed Kenyan non‐human primates. With the continued use of these animals as models for human parasitic diseases, the presence of this highly enzootic parasite should be noted.     

Interspecific interaction of the primate groups in Kibale Forest,Uganda

An ecological survey on the influence of interspecific interaction of the primates upon the distribution of their group ranges was carried out in 100 ha of the isolated forest northern outskirts of Kibale Forest in western Uganda, Africa. The study period of 105 days was from the 12th of November, 1970 to the 24th of February, 1971, including a preliminary survey of about two months. The subjects of this study are five species of primates, i.e., black and white colobus (Colobus polykomos), red colobus (Colobus badius), red tailed monkey (Cercopithecus ascanius), blue monkey (Cercopithecus mitis), and vervet monkey (Cercopithecus aethiops), which inhabited the study area. The red colobus group is thought to be the most influential of the five in the interspecific interaction.     

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.     

The recognition of social alliances by vervet monkeys

Vervet monkeys (Cercopithecus aethiops) are significantly more likely to threaten a particular individual if they have previously been involved in a fight with that individual's close kin. They thus show evidence of recognizing that certain individuals associate regularly with each other. Vervets over the age of 3 years are also significantly more likely to threaten a particular individual if that individual's close kin and their own close kin have previously been involved in a fight. It therefore seems possible that adult vervets can recognize, from experience, that certain sorts of relationships share similar characteristics, regardless of the individuals involved.     

Assessment of meaning and the detection of unreliable signals by vervet monkeys

Free-ranging vervet monkeys, Cercopithecus aethiops, who had learned to ignore playbacks of one type of call by an unreliable signaller subsequently also ignored playback of an acoustically different call by the same individual if the calls had similar referents. Such transfer did not occur if either the identity of the signaller changed or if the two calls had different referents. After repeatedly being played an intergroup call in the absence of other groups, vervets also ignored an acoustically different intergroup call given by the same individual. The monkeys did not transfer habituation, however, if the new call was given by a different individual. In tests where the referents of two calls were different, the monkeys also failed to transfer habituation across call types. Vervet monkeys who had learned to ignore an unreliable leopard alarm call did not later ignore an eagle alarm call, even when the signaller remained the same. Results suggest that vervets, like humans, process information at a semantic, and not just an acoustic, level.