Influence of chimpanzee predation on the red colobus population at Ngogo, Kibale National Park, Uganda

Frequent hunting of red colobus monkeys (Procolobus rufomitratus) takes place at all long-term chimpanzee (Pan troglodytes) study sites where both species are present. Red colobus are the most commonly selected prey of chimpanzees even when other monkey species are more abundant. In particular, the chimpanzee community at Ngogo, Kibale National Park, Uganda, preys heavily on red colobus monkeys: the chimpanzee hunting success rate is extremely high, and chimpanzees kill many individuals per successful hunt. Census data had suggested that the red colobus population is declining and that predation by chimpanzees may be contributing to this decline. In this paper, I address the impact of hunting on the red colobus population at Ngogo. To test the hypothesis that chimpanzee hunting is sustainable, I am using demographic data collected on red colobus monkeys over a period of 3 years, as well as fecundity and mortality data from previous studies of this species. I apply matrix models and vortex analyses using a sensitivity analysis approach to project future population development. Results show that current rates of hunting are not sustainable, but that chimpanzees are neither more “noble”, nor more “savage” than humans are, but that they also hunt to ensure maximum benefit without regard for the consequences for the prey population.     

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.     

Has Predation Shaped the Social Systems of Arboreal Primates?

I studied antipredator behavior in two species of monkeys to elucidate the role of predation in shaping the social systems of arboreal primates. I compared the responses of monkeys to auditory and visual contact with predators to response elicited by sound playback experiments using the recorded calls of predators. Changes in vigilance and aggregation persisting up to 30 min after predator encounter occurred in both cases. Measures of vigilance shed light on individual perceptions of risk, while aggregation measures—intragroup spatial cohesion and polyspecific associations—permit direct inference about the protective benefits of grouping for the monkeys. They responded to real predator encounters and simulations in similar ways. Thus, sound playbacks of predator vocalizations are effective to simulate predator proximity. Contrary to predictions, predator encounters did not lead invariably to increased cohesion within groups or to increased time spent vigilant. Moreover, behavior in polyspecific associations was no different from that in single-species groups. Only red colobus encountering chimpanzees behaved as predicted by increasing vigilance and intragroup cohesion. The red colobus social system may have developed to protect against chimpanzee attack. In contrast, red-tailed monkey encounters with raptors and chimpanzees involved no change in time spent vigilant, coupled with decreases in intragroup cohesion. I conclude that predation is not a uniform selective pressure and patterns of social behavior within groups do not predict antipredator behavior.     

The formation of red colobus-diana monkey associations under predation pressure from chimpanzees.

It is generally assumed that most primates live in monospecific or polyspecific groups because group living provides protection against predation, but hard evidence is scarce. We tested the antipredation hypothesis with observational and experimental data on mixed-species groups of red colobus (Procolobus badius) and diana monkeys (Cercopithecus diana) in the Taï National Park, Ivory Coast. Red colobus, but not diana monkeys, are frequently killed by cooperatively hunting chimpanzees. Association rates peaked during the chimpanzees'' hunting season, as a result of changes in the behaviour of the red colobus. In addition, playbacks of recordings of chimpanzee sounds induced the formation of new associations and extended the duration of existing associations. No such effects were observed in reaction to control experiments and playbacks of leopard recordings.     

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.     

Interspecific interactions between wild pygmy chimpanzees (Pan paniscus) and red colobus (Colobus badius)

Interspecific interactions accompanied by physical contacts between wild pygmy chimpanzees (Pan paniscus) and red colobus (Colobus badius) were observed on three occasions at Wamba, Republic of Zaire. In all cases, the red colobus initiated the interactions by approaching the pygmy chimpanzees. Most of the pygmy chimpanzees, which were within 5 m of the red colobus, were juveniles or infants but the adult male pygmy chimpanzees never showed any interest in the red colobus. The red colobus groomed the chimpanzees in two cases, but the latter never groomed the former. No true aggressive interactions were observed between the two species. The lack of any evidence of hunting of red colobus through longitudinal studies of the pygmy chimpanzees of Wamba, together with the present observations, suggests that red colobus are probably not targets of hunting by the pygmy chimpanzees.     

Patterns of predation by chimpanzees on red colobus monkeys in gombe national park, 1982–1991

Predatory patterns in wild chimpanzees are important evidence in the continuing debate about the role of hunting in the behavior of early hominids. Data are presented on the predator–prey ecology of red colobus monkeys (Colobus badius tephrosceles) and chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania, from 1982 through 1991. During this period chimpanzees were observed to kill 429 mammalian prey items, 350 of which were red colobus. Hunts were undertaken by chimpanzees in 71.5% of encounters with red colobus, and in 52.2% of all hunts at least one colobus was caught. Hunting occurred in all months, but its frequency peaked in the late dry season months of August and September, and was lowest in the rainy months of April and May. There was greater seasonality of hunting from 1982 to 1991 than previously reported for Gombe. Hunting success varied between 40% in the rainy season and 65% in the dry season. Sixty multiple kills of colobus were reported in which from two to seven colobus were killed. Approximately 75% of all colobus caught were immatures; juveniles were the most preyed upon age class. Adult and adolescent male chimpanzees made 89.3% of all kills; the 10.7% of kills made by adult females was an increase over the 4% figure for female kills reported in the preceding decade. Hunting showed a strong “binge” tendency, with the explanation for binges likely related to social rather than ecological factors. These results are discussed in light of earlier hunting data for Gombe chimpanzees, and compared with data from other chimpanzee field studies. © 1994 Wiley-Liss, Inc.     

Chimpanzee predation in the Mahale mountains from August 1979 to May 1982

Fifty-four episodes of predatory behavior of wild chimpanzees were recorded in Mahale, western Tanzania, from August 1979 to May 1982. The chimpanzees most frequently hunt in two seasons, during May, and from August to December. Longer-term fecal analysis indicates that predation frequency is significantly higher in the dry than in the rainy season. The seasonality of predation might be the result of the sum of various ecological factors, at least one of which is the birth season of the prey species. Most of the prey are juvenile blue duiker, bushbuck, bushpig, red colobus, and red-tailed monkeys. Sex difference is recognized in the prey selection and in the hunting method employed. Apparent local difference in the predatory behavior between Mahale and Combe chimpanzees (in Mahale,females hunt more frequently, and blue duiker is the most frequent prey) can be understood in terms of the difference either in the observation methods or in the faunal diversity and density. Other aspects of predatory behavior also are reported.     

Hunting Behavior of Chimpanzees at Ngogo,Kibale National Park,Uganda

Chimpanzees (Pan troglodytes) prey on a variety of vertebrates, mostly on red colobus (Procolobus spp.) where the two species are sympatric. Variation across population occurs in hunting frequency and success, in whether hunting is cooperative, i.e., payoffs to individual hunters increase with group size, and in the extent to which hunters coordinate their actions in space and time, and in the impact of hunting on red colobus populations. Also, hunting frequency varies over time within populations, for reasons that are unclear. We present new data on hunting by chimpanzees at Ngogo, Kibale National Park, Uganda, and combine them with earlier data (Mitani and Watts, 1999, Am. J. Phys. Anthropol. 109: 439–454) to examine hunting frequency and success, seasonality, and cooperation. The Ngogo community is the largest and has the most males of any known community. Chimpanzees there mostly hunt red colobus and are much more successful and make many more kills per hunt than at other sites; they kill 6–12% of the red colobus population annually. The number of kills and the offtake of meat per hunt increase with the number of hunters, but per capita meat intake is independent of hunting party size; this suggests that cheating occurs in large parties. Some behavioral cooperation occurs. Hunting success and estimated meat intake vary greatly among males, partly due to dominance rank effects. The high overall success rate leads to relatively high average per capita meat intake despite the large number of consumers. The frequency of hunts and of hunting patrols varies positively with the availability of ripe fruit; this is the first quantitative demonstration of a relationship between hunting frequency and the availability of other food, and implies that the chimpanzees hunt most when they can easily meet energy needs from other sources. We provide the first quantitative support for the argument that variation in canopy structure influences decisions to hunt red colobus because hunts are easier where the canopy is broken.     

Predation on mammals by chimpanzees in the montane forest of Kahuzi, Zaire

The rate of predation on mammals by chimpanzees was determined from carcasses and from fecal specimens found on fresh trails during a 16-month period in the montane forest of Kahuzi-Biega National Park, Zaire. A unit-group of semi-habituated chimpanzees, composed of 22 – 23 individuals including 8 adult or adolescent males, appeared to kill about 18 – 30 mammalian prey (16 – 28Cercopithecus monkeys) per year, if the multiple kills by chimpanzees were not considered. A juvenile l'Hoest's monkey was recorded for the first time as the prey of chimpanzees in this study. Predation occurred in the late dry and the early rainy seasons, when the diversity of ripe fruits was the highest during the year. The Kahuzi chimpanzees tended to kill mammals less frequently but to killCercopithecus monkeys more frequently than chimpanzees in other habitats. The absence of red colobus monkeys, which are the most frequent prey in Gombe, Mahale, and Tai, might be responsible for the low predation rate. However, the estimated rate of predation onCercopithecus monkeys is the highest record among various chimpanzee habitats. At least 11 – 18% of theCercopithecus population seemed to be lost annually as a result of being killed by chimpanzees. Chimpanzees may be the most important predators on these monkeys in the absence of leopards at Kahuzi. The examination of fecal samples and carcasses suggested that adult (probably male) or adolescent chimpanzees tended to eat juvenile or subadult monkeys most frequently, as is also seen for chimpanzees in Gombe, Mahale, and Tai.     

Red-tailed monkeys (Cercopithecus ascanius) hunt green pigeons (Treron calva) in the Kalinzu Forest in Uganda

Red-tailed monkeys (Cercopithecus ascanius) were observed hunting green pigeons (Treron calva) in the Kalinzu Forest in Uganda. During 2 h 39 min, I observed two cases of successful hunting and one case of unsuccessful hunting in a Ficus saussureana tree. Red-tailed monkeys stalked the pigeons until they were within 2–3 m, and then jumped and caught them. In both successful cases, blue monkeys (C. mitis) ran to the hunting site from adjacent trees in order to poach the prey, and the red-tailed monkeys fled. One of these red-tailed monkeys dropped the pigeon while fleeing, and the blue monkey climbed down from the tree to search for it. This is the first record of cercopithecoid monkeys hunting birds that are outside of the nest and moving freely, and also the first record of red-tailed monkeys hunting vertebrates. However rare it may be, the repeated hunting attempts using similar techniques and the immediate attempt of blue monkeys to poach the prey suggest that this type of hunting was not a one-time event that happened by chance. Blue monkeys and an adult chimpanzee (Pan troglodytes schweinfurthii) in and around the fig tree did not attempt to hunt. The hunting of volant birds may be enabled by the small body size and the quick movements of red-tailed monkeys.     

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.     

Coping with Forest Fragmentation: The Primates of Kibale National Park,Uganda

A goal of conservation biology is to determine which types of species are most susceptible to habitat disturbance and which types of disturbed habitats can support particular species. We studied 20 forest fragments outside of Kibale National Park, Uganda, to address this question. At each patch, we determined the presence of primate species, tree species composition, patch size, and distance to nearest patch. We collected demographic, behavioral, and dietary data for Abyssinian black-and-white colobus (Colobus guereza). Black-and-white colobus and red-tailed guenons (Cercopithecus ascanius) were in almost all fragments; Pennant's red colobus (Procolobus pennantii) and chimpanzees (Pan troglodytes) were in some fragments; and blue monkeys (Cercopithecus mitis) and gray-cheeked mangabeys (Lophocebus albigena) were absent from all fragments. No species characteristics—home range, body size, group size, or degree of frugivory—predicted the ability of species to live in patches. No characteristics of patches—area, distance to the nearest patch, distance to Kibale, or number of food trees present—predicted the presence of a particular species in a patch, but distance to Kibale may have influenced presence of red colobus. Black-and-white colobus group size was significantly smaller in the forest patches than in the continuous forest of Kibale. For a group of black-and-white colobus in one patch, food plant species and home range size were very different from those of a group within Kibale. However, their activity budget and plant parts eaten were quite similar to those of the Kibale group. The lack of strong predictive variables as well as differences between other studies of fragmentation and ours caution against making generalizations about primate responses to fragmentation.     

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.     

Feeding habits of chimpanzees (Pan troglodytes), red-tail monkeys (Cercopithecus ascanius schmidti) and blue monkeys (Cercopithecus mitis stuhlmanii) on figs in Budongo Forest Reserve, Uganda

Feeding habits of chimpanzees, red‐tail and blue monkeys on figs (Ficus) were studied in compartment N3 of Budongo Forest Reserve, western Uganda, from September 1997 to March 1998. The aim was to examine the spatial and temporal foraging habits of chimpanzees, red‐tail monkeys and blue monkeys on figs in the forest reserve. Both scan and focal sampling methods were used to assess the foraging habits of the primates. It was found that the primates fed on emerging leaves of Ficus mucuso Ficalho, F. varifolia Warb. and F. exasperata Vahl. They also preferred ripe fruits to emerging, young and unripe fruits. The primates spent 78% of the morning eating fruits and leaves and inhabited fig trees with fruits for about 4 h. Fig trees with ripe fruits attracted larger numbers of primate groups. It is concluded that information on the feeding habits of chimpanzees and monkeys is required in order to have a clear understanding of the social behaviour and pattern of movement of the primates and to assist in predicting the likely impacts of poor forest management, forest degradation and loss of food resources on their populations.     

Group size in folivorous primates: ecological constraints and the possible influence of social factors

The ecological-constraints model assumes that food items occur in depletable patches and proposes that an increase in group size leads to increased day range due to more rapid patch depletion. Smaller groups become advantageous when an increase in travel costs is not repaid by an increase in energy gained or some other fitness advantage. On the other hand, we also know that group size can be influenced by social factors. Here we contrast the diet and group size of red colobus (Procolobus badius) and black-and-white colobus (Colobus guereza) in Kibale National Park, Uganda to consider how ecological and social factors are affecting their group sizes. Subsequently, we examine whether the insights gained from this detailed comparison can provide an understanding of why the social organization and group size of mantled howlers (Alouatta palliata) and black howlers (A. pigra) differ. Two groups of red colobus and two groups of black-and-white colobus were studied over 10 months. Red colobus groups were larger (48 and 24) than black-and-white colobus groups (9 and 6). The two groups of red colobus overlap home ranges with the two groups of black-and-white colobus; 75% and 95% of their home ranges were within red colobuss home range. There was a great deal of similarity in the plant parts eaten by the two species and both species fed primarily on young leaves (red colobus 70%, black-and-white colobus 76%). In terms of the actual species consumed, again there was a great deal of similarity between species. The average dietary overlap among months for the two neighboring groups of red colobus was 37.3%, while the dietary overlap between the red colobus and the black-and-white colobus group that had its home range almost entirely within the home range of the red colobus groups averaged 43.2% among months. If ecological conditions were responsible for the difference in group size between the two colobine species, one would expect the density of food trees to be lower in the home ranges of the black-and-white colobus monkeys, since they have the smaller group size. We found the opposite to be true. Both black-and-white colobus groups had more food trees and the cumulative size of those trees was greater than those in the red colobuss home ranges. We quantify how these differences parallel differences in mantled and black howlers. The average group size for mantled howlers was 12.9 individuals, and for black howlers it was 5.3 individuals. We explore possible social constraints, such as infanticide, that prevent black-and-white colobus and black howlers from living in large groups.This revised version was published online in April 2005 with corrections to the cover date of the issue.     

Monkey Abundance and Social Structure in Two High-Elevation Forest Reserves in the Udzungwa Mountains of Tanzania

The effects of human activity on population and social structure are a pantropical concern for primate conservation. We compare census data and social group counts from two forests in the Udzungwa Mountains, Tanzania. The main aim is to relate differences within and between the forests to current theory on the effect of human disturbance on primate abundance and group size. The survey reveals the presence of the restricted-range red colobus, Procolobus gordonorum, in New Dabaga/Ulangambi Forest Reserve (NDUFR). The primate community of NDUFR is impoverished compared to that in Ndundulu forest. Red colobus and black-and-white colobus (Colobus angolensis palliatus) abundance and group size are lowest in NDUFR. Fission-fusion of red colobus social groups may be occurring in previously logged areas of both forests. Our observations are consistent with current theory on the effect of habitat degradation and hunting on primates, but the relative effects of the 2 factors could not be differentiated. We pooled the results with previous data to show that abundance of red colobus in the Udzungwa Mountains is lowest at high elevations. Low red colobus group sizes appear to be related to human activity rather than elevation. Black-and-white colobus and Sykes monkeys (Cercopithecus mitis) show no relationship with elevation. Future studies will require more detailed information on vegetation, diet and ranging patterns to interpret fully intraspecific variation in population demography and social structure in the Udzungwa Mountains.     

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 note on the ecology of the red-colobus monkeys (Colobus badius tephrosceles) living in the Mahali Mountains

Red-colobus monkeys of the Mahali Mountains utilize many vegetation types; although their main habitat is composed of forest vegetation (gallery forest and montane forest), they sometimes penetrate into even theMiombo woodland.Red-colobus monkeys mainly live on leaves of trees, but sometimes eat flowers, fruits, and barks. Most of the plant leaves which the chimpanzees eat have proved to be delicacies to colobus monkeys also. Colobus monkeys live in compact bisexual groups, ranging from 30 to 50 in size. No solitary male has so far been observed.A colobus group living in the gallery forest moved 100 to 200 meters daily within its welldocumented home range. The home ranges of groups do not seem to overlap each other extensively.Their natural enemies are leopards, birds of prey and probably chimpanzees. The Tongwe inhabitants avail themselves of the colobus coat as part of their native bellows (mufuba) and some pagan inhabitants kill them for their meat.The research was financed by the Scientific Research Fund of the Ministry of Education and in part by the Wenner-Gren Foundation. This report is a part of the results of the Kyoto University Africa Primatological Expedition.     

Red colobus as prey: the leaping habits of five sympatric Old World monkeys

This study explored the leaping habits of five sympatric Old World monkeys (Colobus badius, Colobus guereza, Cercopithecus ascanius, Cercopithecus mitis and Cercocebus albigena) in an attempt to determine why chimpanzees prefer to hunt red colobus. We videotaped the leaps of the monkeys for 3 months in Uganda's Kibale National Park. Data were collected on leap preparation time as well as several other variables of the leaps. The leap preparation time of red colobus was found to be about double that of the other species studied. This difference is a likely reason why red colobus represent the preferred prey of chimpanzees. The hypothesis that red colobus spend more time in isolated trees than do other species was not supported.