Black Colobus Research Articles

Contrasts in Livelihoods and Protein Intake between Commercial and Subsistence Bushmeat Hunters in Two Villages on Bioko Island, Equatorial Guinea

Across West and Central Africa, wildlife provides a source of food and income. We investigated the relation between bushmeat hunting and household wealth and protein consumption in 2 rural communities in Bioko Island, Equatorial Guinea. One village was dedicated to commercial hunting, the other trapped game primarily for food. We tested whether commercial-hunter households were nutritionally advantaged over subsistence-hunter households due to their higher income from the bushmeat trade and greater access to wild-animal protein. We conducted bushmeat-offtake surveys in both villages (captures by hunters and carcasses arriving to each village). Mammals (including threatened primates: black colobus [Colobus satanas], Preussi's guenon [Allochrocebus preussi], and russet-eared guenon [Cercopithecus erythrotis]), birds, and reptiles were hunted. The blue duiker (Philantomba monticola), giant pouched rat (Cricetomys emini), and brush-tailed porcupine (Atherurus africanus) contributed almost all the animal biomass hunted, consumed, or sold in both villages. Monkeys and Ogilbyi's duikers (Cephalophus ogilbyi) were hunted only by commercial hunters. Commercial hunters generated a mean of US$2000/year from bushmeat sales. Households with commercial hunters were on average wealthier, generated more income, spent more money on nonessential goods, and bought more products they did not grow. By contrast, households with subsistence hunters spent less on market items, spent more on essential products, and grew more of their own food. Despite these differences, average consumption of vegetable protein and domestic meat and bushmeat protein did not differ between villages. Our results highlight the importance of understanding the socioeconomic and nutritional context of commercial and subsistence bushmeat hunting to correctly interpret ways of reducing their effects on threatened species and to enable the sustainable offtake of more productive taxa.

The market for bushmeat: Colobus Satanas on Bioko Island

Species conservation is an important issue worldwide. The market for monkeys consumed as food on Bioko Island, Equatorial Guinea, is modeled as a bargaining game. The bargaining set-up leads to the conclusion that black colobus are being over-hunted. Using daily data an empirical density is fit to the price–quantity pairs resulting from exchange between buyers and retailers. The density provides support for the bargaining model. Quantile regressions are also fit to the data. The median quantile indicates buyers have greater bargaining power than retailers. Knowing who has bargaining power aids in the design of policy to reduce bushmeat hunting. Strategic elasticities are constructed from the quantiles. Given the harvest rate of monkeys and the elasticity estimates, the monkeys of Bioko Island are under considerable pressure.

Impact of Gun-Hunting on Diurnal Primates in Continental Equatorial Guinea

Bushmeat hunting is threatening wildlife populations across west-central Africa, and now poses a greater threat to primates than habitat loss or degradation does in some areas. However, species vary in their abilities to withstand hunting, either because hunters target them differentially or they vary in their vulnerability to a given level of hunting. We studied the impact of current levels of gun-hunting on diurnal primate species in the little-studied Monte Mitra area of Monte Alen National Park, continental Equatorial Guinea. Most bushmeat is currently trapped, but gun-hunting is increasing as shotguns become more available and affordable, allowing targeting of arboreal as well as terrestrial prey. We collected data over 15-mo, via hunter interviews, gun-hunter follows, an offtake survey recording 9374 individuals, and primate surveys covering 408 km of line transects in 2 sites with differing gun-hunting histories. Inside the park, where gun-hunting pressure was recent and light, we found high primate diversity, density, and biomass, with black colobus (Colobus satanas) particularly abundant at 57 individuals/km2. However, around the village, where gun-hunting was longer-established, though other species such as the guenons still persisted (albeit at lower densities), Colobus satanas were virtually absent. Being slow and large-bodied, Colobus satanas are preferred and susceptible prey, and an early indicator of overhunting. Monte Alen National Park is currently an important stronghold for primates, particularly Colobus satanas, but regulation of the trade and enforcement of hunting bans in the park are urgently needed to safeguard their future and that of other vulnerable species.

Population status of black and white colobus monkeys (Colobus guereza) in Kakamega Forest, Kenya: are they really on the decline?

Eastern black and white colobus monkeys, or guerezas (Colobus guereza), are among the few primate species that have traditionally been regarded as not being adversely affected by habitat degradation. This view was recently challenged by von Hippel et al. (2000) who, using data from short-term censuses in 1992 and 1998, reported a striking decline in guereza density over a six-year period of light to moderate habitat degradation at Isecheno study site in the Kakamega Forest, Kenya. In this paper, I present evidence from my own more intensive study during the same period that suggests that the guereza population at Isecheno is actually quite robust and may in fact be increasing. I provide evidence to suggest that the census methods adopted by von Hippel and his colleagues are prone to overestimating density and that the decline in guereza density that they reported probably did not occur. My study suggests that brief censuses based on group counts over a given area, even when conducted by multiple observers, are not sufficient for accurately determining primate distributions and densities in rainforest environments. Data on animal distribution and density play a critical role in the development of conservation strategies and it is therefore important that these data be relatively accurate if biologists are to make informed conservation decisions.

Distribution, population density, and status of sympatric cercopithecids in the Campo-Ma'an area, Southwestern Cameroon.

A study on species composition, distribution, and population density of cercopithecids in the Campo-Ma'an area, Southwestern Cameroon, was undertaken from December 1997 until August 2000. A total of 665.5 km of line transects was used for the census. Thirteen diurnal primate species including five endangered species (Gorilla g. gorilla, Pan troglodytes, Mandrillus sphinx, Colobus satanas, Cercocebus torquatus) were recorded in the Campo Forest, the greatest part of which is a logging concession. Cercopithecus nictitans (1.43 groups/km2), C. cephus (1.13 groups/km2), C. pogonias (0.81 groups/km2), and C. torquatus (0.51 groups/km2) occurred at medium frequencies compared to figures from other Central African study sites. Mandrill densities estimated (0.27 groups/km2) show that the area is very important for the conservation of this rare species. Guenon densities found inside areas with a high level of human activities did not differ significantly from densities estimated in areas with a lower level of human activities. C. torquatus densities were significantly higher in the areas with a low level of human disturbance and encounter rates with Lophocebus albigena also indicate a preference of less disturbed areas. Mangabeys are thus likely to be adversely affected by human activities in the area. In the Ma'an Forest, which has not been logged yet, ten species were confirmed. The population densities of two guenons (C. nictitans and C. cephus) were estimated to be twice as high in the unlogged forest area as compared to the logged forest of Campo. Other species are rarer in the Ma'an Forest than in the Campo Forest. Although mangabeys are adversely affected by human activities, the results still indicate that selective logging may be compatible with the conservation of cercopithecids, if a reduced damage logging concept and antipoaching measures are implemented. Increased hunting activities following logging operations will definitely have a negative longterm impact on primate populations in the Campo-Ma'an area if no further, more effective conservation measures will regulate wildlife use in future.

Estimating primate densities using home range and line transect methods: A comparative test with the black colobus monkeyColobus satanas.

The line transect method is one of the main methods used to estimate primate densities. Several protocols have been proposed to analyze the data recorded under this method but none of them have been widely accepted since there is a considerable controversy about their respective accuracy. In this study, densities of the black colobus monkeyColobus satanas calculated using eight different protocols were compared with the actual density given by the home range method. Rates of polyspecific associations were also compared. The two most accurate estimates of group density (under- or overestimation <10%) were yielded by the protocol that used the maximum transect-to-animal distance and by that of using a fixed distance of 100 m. These protocols, however, underestimated individual density because counts performed from transects underestimated by 23% the average group size. The six other protocols overestimated group density by 20-195%. Factors that could explain these overestimation were discussed. Because histogram of sighting frequency showed several classes of distances with no records and because groups have been detected as far as 160 m, we suggested that the uneven topography of the study site increased the variability of the sighting distances. Combined with a relatively low number of sightings (n=23), this did not allow to identify a sharp detection distance. Rates of polyspecific association found with the two methods were similar. We recommend to investigate the influence of the topography for bias in density estimates when using the line transect method.

Population decline of the black and white colobus monkey (Colobus guereza) in the Kakamega Forest, Kenya

Groups of black and white colobus monkeys, or guerezas (Colobus guereza), in a study site in the Kakamega Forest, Kenya, have declined in number from 18 groups in 1992 to 12 groups in 1998. This decline occurred largely in the eastern half of the study site, and was not offset by an increase in group size. The western half of the study site has areas next to buildings, on the edge of the forest, where guerezas supplement their diet with soil, and it has more human foot traffic which might reduce predation levels; these factors might be partially responsible for holding the number of guereza groups in the western half steady while forest degradation takes its toll on guerezas in the eastern half. This decline in guerezas is of particular concern since it took place in an area of forest that has not decreased in size and because guerezas are among the least sensitive primates to forest degradation.

Seminomadic ranging in a population of black colobus (Colobus satanas) in Gabon and its ecological correlates

We observed ranging patterns in a black colobus population in the Foret des Abeilles, Central Gabon. We compared the results with those for two other populations (Lope Reserve in Central Gabon, Douala-Edea in coastal Cameroun) in order to estimate the extent of specific variability in population structure and ranging behavior and to identify ecological factors influencing interpopulation differences. The mean number of monkeys in a group is 17, and all groups had a multimale structure. Home ranges were large, and the fact that they continued to increase with increasing number of observations indicated that the monkeys did not frequently resample their habitat. Ranging patterns varied according to the staple food consumed: distances travelled daily increased with increasing seed intake and decreased with increasing leaf intake. The ranging patterns of groups of Colobus satanas are seminomadic. Up to 6 or 7 groups shared the same space, and two group ranges could overlap by as much as 65–75%. Comparisons with the two populations previously studied showed that group size and group structure are broadly similar. At all three sites, black colobus were mainly seed eaters and ate large amounts of leaves in the season of fruit shortage. In the Foret des Abeilles, however, group home ranges were much larger than at other sites, and this population had the lowest density. This is correlated with vegetation composition and with harshness of the main dry season. This colobus population appears limited by both recurring food shortage in the dry season and episodic periods of seed shortage resulting from irregular fruiting of the dominant family Caesalpiniaceae. Their seminomadic ranging would constitute the least costly strategy to cope with the low carrying capacity of their habitat.

Fragmented living: Behavioural ecology of primates in a forest fragment in the Lopé Reserve, Gabon

A 17-month study was made of the primates using a 9-ha "island" of forest, surrounded by savanna, in the northern part of the Lopé Reserve, Gabon. One group ofCercopithecus cephus (plus a young maleCercopithecus nictitans who was in permanent association with them) were resident in the fragment and groups of five other species of primates made visits during 127 days of observation:Pan troglodytes, 15 visits;Cercocebus albigena, 10;Colobus satanas, 3;Cercopithecus nictitans, 2;C. pogonias, 1. Visits were also made by lone males of three species,C. nictitans, Cercocebus albigena, andMandrillus sphinx. The eighth species of diurnal primate present at Lopé,Gorilla g. gorilla, did not visit the fragment during the study. Compared to conspecific groups in neighbouring continuous forest, primates in the fragment ate less fruit, seeds and flowers and more insects and leaves. The local population density of primates resident in the fragment was equivalent to that of the neighbouring continuous forest where all eight species occur, despite the diversity and abundance of fruit being less in the fragment. The costs imposed on the resident group by the reduced diversity and availability of preferred fruit foods appeared to be offset by a number of benefits that increased individual feeding efficiency for monkeys residing within a single fragment. These included lower travel costs, reduced feeding competition between individuals through group fission, and excellent knowledge of the location and quality of food resources in the small home range. It is also possible that the overall negative impact of inter-specific feeding competition was lower in fragments than in continuous forest and that micro-habitat differences resulted in an increased availability of palatable insect and leaf fallback foods in the fragment.

Population size of the black colobus monkey Colobus satanas and the impact of logging in the Lopé Reserve, Central Gabon

The black colobus monkey Colobus satanas is a threatened species from the central African forests suspected to be vulnerable to habitat disturbance and thus thought to be mainly restricted to primary forest. A survey was carried out in 1995–1996 to estimate the density of black colobus in the primary forest of the Lopé Reserve, central Gabon. Combined with the available data on density in the logged part of the reserve, a population of ca. 55,900 colobus was estimated for the whole reserve. No significant differences were found between densities in logged and unlogged forests. Using data on the logging activity that occurred in the reserve, this result was mainly explained by a low rate of extraction (1–2 trees ha −1) which did not induce a major change in the forest composition and structure. This suggests that hunting is currently a more important threat to the survival of the species than habitat disturbance. The Lopé Reserve is of prime importance for the conservation of this species since it holds the largest population of black colobus known in any protected area.

Adaptation au milieu naturel d’un jeune Cercopithecus solatus élevé à la main

After his mother had been killed when he was 5 months old, Mbaya, a young C. solatus, was raised at the Makande field station with the intention of reintroducing him later in his natural environment. Therefore, he was allowed to accompany research workers in the forest and he was free to choose his food and movements. He did not get food poisoning and he soon found his bearings. He developed social contacts with other primates he met. Although he was attracted by the forest, he never went there alone during this 22-month study. He showed obvious interest in wild troops of C. solatus, particularly in young group members. These C. solatus first showed rejection reactions, then tolerated him. Mbaya stayed longer and longer with three different troops of C. solatus (up to 6 days), and with a solitary adult male for a maximum of 12 days. However, he never integrated a troop definitively. In spite of their total permissiveness, Mbaya mixed with troops of Colobus satanas only for short durations (less than 2 hours), often during feeding and always at heights below 15 meters. This study suggests that 1) the young C. solatus had acquired species recognition during the first 5 months of his life ; 2) a few months with humans was sufficient to make his return to the natural environment difficult.

The primate community of the Lopé Reserve, Gabon: diets, responses to fruit scarcity, and effects on biomass.

The diets of all diurnal primates (Gorilla g. gorilla, Pan t. troglodytes, Mandrillus sphinx, Colobus satanas, Cercocebus albigena, Cercopithecus nictitans, C. pogonias, C. cephus) in the Lópe Reserve, central Gabon, are described from qualitative and quantitative data collected over 10 years. A total of 397 foods were recorded, of which 91% were from plants. The diet of seven of the eight species were numerically dominated by fruit, the exception being Colobus satanas with a diet dominated by seeds. When proportion of feeding time was examined, fruit remained the dominant food class for six species, while Cercocebus albigena, like the black colobus, spent most time feeding on seeds. The number of foods recorded per species ranged from 46-220, but dietary breadth of the four species that have not been subjects of detailed study was certainly underestimated. Almost half of the foods (46%) were eaten by only one species, and only four (1%) were recorded for all eight species. At Lópe, fruit is scarce for 2-3 months during the annual dry season, and fruit crop failures can prolong this period of scarcity to as many as 8 months in some years. When fruit is scarce, the diets of all the species changed to include more nonfruit foods, but chimpanzees and the three species of guenons maintained a fruit dominated diet. The total biomass of the Lópe primate community is 374 kg/km2, which is low compared to other sites in tropical Africa. Within the Lópe community, biomass correlates negativity with degree of frugivory, suggesting that fruit availability may be critical, but this does not explain the low total biomass compared to other sites. Neither floristic diversity nor the composition of the primate community at Lópe can account for the biomass. While historical events such as climate-induced changes in forrest cover, disease, or impact of human activities cannot be ruled out, we conclude that the most likely explanation of low primate biomass is the occurrence of an ecological "catastrophe" in the fairly recent past from which populations have not yet recovered. We believe that the most likely scenario was climate-mediated disturbance of flowering of important fruit food species. Prolonged fruit scarcity would have caused mortalities and affected the most frugivorous species more severely.

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.

Mapping homology between human and black and white colobine monkey chromosomes by fluorescent in situ hybridization.

We used in situ hybridization of chromosome specific DNA probes ("chromosome painting") of all human chromosomes to establish homologies between the human and the white and black colobus (Colobus guereza 2n = 44). The 24 human paints gave 31 signals on the autosomes (haploid male chromosomes homologus to human 14 and 15, 21 and 22, form colobine chromosomes 6 and 16, respectively. Reciprocal translocations were found between human chromosomes 1 and 10, 1 and 17, as well as 3 and 19. The alternating hybridization signals between human 3 and 19 on Colobus chromosome 12 show that in this case a reciprocal translocation was followed by a pericentric inversion. The hybridization data show that in spite of the same diploid number and similar Fundamental Numbers, the black and white colobine monkey differs from Presbytis cristata, an Asian colobine, by 6 reciprocal translocations. Comparisons with the hybridization patterns in other primates show that some Asian colobines have a more derived karyotype with respect to African colobines, macaques, great apes, and humans. Chromosome painting also clearly shows that similarities in diploid number and chromosome morphology both between colobines and gibbons are due to convergence.

Do black colobus in mixed-species groups benefit from increased foraging efficiency?

Seed-eating in the African colobines varies according to species and site. Because seeds are more palatable than leaves, seed-eating is considered to result from a positive choice by colobines. A year-long study of the diet of Colobus satanas in Central Gabon confirmed that this species eats a significant amount of seeds. Furthermore, despite large variations in fruit availability, this amount consistently increases when colobines feed in mixed-species troops including frugivorous cercopithecines and mangabeys. Our results show that colobines benefit when feeding in mixed troops and suggest that polyspecific associations are an adaptive strategy that could have positive effects on colobine populations, especially during the period of fruit shortage.

Primates in Gabon – current status and distribution

This paper examines the current status and distribution of primates in Gabon on the basis of data collected in the field between 1985 and 1988. There are at least 19 and possibly 21 species of primates definitely present in Gabon, making it one of the richest countries in the world for primates. Most of the species are still widespread and one, the sun-tailed guenon, is endemic. Hunting and habitat destruction are the main threats to the country's primates. The major problem at the moment is the opening up of previously inaccessible areas by logging companies and the Trans Gabon railway, which leads to an increase in hunting pressure. Several species are threatened; the mandrill/drill, the black colobus, and the sun-tailed guenon need special conservation measures. Suggestions for action are made and several new reserves have recently been proposed.

Diet of the northern bearded saki (Chiropotes satanas chiropotes): A neotropical seed predator.

Data on the diet of Chiropotes satanas chiropotes, the northern bearded saki, has been collected during several years of primate field observations in the Raleighvallen-Voltzberg Reserve in Suriname. This species feeds predominantly on immature seeds and ripe fruit, mainly the former. Chiropotes is especially fond of the members of the Brazil nut family, Lecythidaceae, and other species with exceptionally hard or tough seed pods. Concomitantly, Chiropotes shows striking dental and gnathic adaptations that facilitate opening and ingesting these well-protected food items. Seed predation in the Old World colobine, Colobus satanas, has been discussed primarily as a strategy for survival in forests characterized by leaves with low nutrient content and high toxicity; however, it now appears that arboreal seed predation is a relatively widespread primate dietary strategy found among higher primate species in a variety of forest types on three continents. It is yet another way of "making a living" in a tropical rain forest.

Un primate granivore : le Colobe noir dans la forêt du Gabon ; potentialité d’évolution du comportement alimentaire

This paper presents preliminary data on the feeding strategy of the Black colobus, Colobus satanas, in central Gabon. The study was conducted in the Réserve de la Lopé, using frequency method and systematic monthly samples to quantify the diet on one focal group of monkeys. The Black colobus feeds predominantly on immature seeds, unlike most of its folivorous relatives, while the consumption of young leaves is second in importance. Despite considerable variation in resource availability, seeds always dominate in the monthly diet. An increase in young leaf consumption was associated with an abundance of flush leaves, but also a reduction in seed availability ; a subsequent seasonal peak of flush leaves showed rm increase in their contribution to the diet, as seeds were also commonly available. Mature leaves were rarely eaten, and their occurence in the diet could explain some aspects of concomitant geophagy. Seasonal variation in diet and resources is compared with that of other primates of North-East Gabon : availability of foliage also partly influences consumption, but the dependence largely on fruit pulp and lack of seeds in the diet contrasts sharply with Black colobus. A similar biomass of Cercopithecidae is found in North-East Gabon where colobus are absent, and Lopé where one might have expected a larger biomass if the Black colobus had been a true folivore. Folivorous and frugivorous dietary strategies are contrasted on the basis of energetically economical vs expensive feeding. The Colobinae tend towards economical feeding strategies with their specialized digestive apparatus, but C. satanas represents a contrast, favoring an expensive seed-eating strategy. A hypothetical mechanism for the behavioural regulation of these strategies is discussed, based on conditioning principles. With such behavioural flexibility, we suggest that seed-eating by Black colobus may be a positive choice rather than a result of selective pressures against folivory.

Ranging behaviour of a group of black Colobus (Colobus satanas) in the Douala-Edea Reserve, Cameroon.

Data are presented from an 11-month study of the ranging movements of a group of Colobus satanas in a rain forest on the coast of Cameroon. Discussion centers on correlations between seasonal variation in ranging behaviour and seasonal variation in food availability, diet composition and diversity, and weather conditions. The data support the hypothesis that the scarcity of nutrient-rich, highly digestible leaves in this site has led to a feeding strategy based on seeds, which are characterised by high nutritive quality and occurrence in large clumps, allowing monotonous feeding and low expenditure of energy in ranging movements.

Food selection by black colobus monkeys (Colobus satanas) in relation to plant chemistry*

Black colobus monkeys (Golobus salanas) in the Douala-Edea Reserve, a rain-forest on the coast of Cameroon, have been shown to avoid young and mature leaves of most of the common plants in their habitat and to feed disproportionately heavily on leaves of rare plants. The proportion of leaves in the diet was low compared to most colobines studied, and the monkeys spent over half their feeding time eating seeds. Patterns of food selection were analysed in relation to distribution of nutrients, digestion–inhibitors and toxins in the vegetation. Colobw satanas select food items that are rich in mineral nutrients and nitrogen and low in content of the general digestion-inhibitors, lignin and tannin. They achieve this in the following ways: (i) by feeding preferentially on young leaves, which have higher nutrient content and lower contents of digestion-inhibitors than mature leaves; (ii) by eating those mature leaves with highest nument content relative to content of digestion-inhibitors; and (iii) by eating seeds, which are sources of readily available energy and which, as an item class, are less rich in digestion-inhibitors. Seeds at Douala-Edea appear to contain Ins nitrogen than leaves and C. satanas selects those seeds with highest nitrogen content. It is suggested that seed-feeding may be facilitated by the ability of the forestomach flora of these ruminant-like monkeys to detoxify some of the secondary compounds contained in seeds. Avoidance of most unused young and mature leaf items is correlated with a low nutrienudigestion-inhibitor ratio; avoidance of most unused seeds could be accounted for by their low nitrogen contents. Most items whose avoidance could not be explained in terms of these major constraints on food selection possess secondary compounds likely to be toxic. It is proposed that relative importance of digestion-inhibitors, low nutrient content and toxins as constraints on food selection by generalist herbivores will vary greatly among forests with different nutrient and secondary chemistry profiles.