Effects of Forest Fragmentation on the Abundance of <Emphasis Type="Italic">Colobus angolensis palliatus</Emphasis> in Kenya’s Coastal Forests

We documented the occurrence and abundance patterns of Angola black-and-white colobus (Colobus angolensis palliatus) in 46 coastal forest fragments ranging from 1 ha to >1400 ha in the Kwale District, Kenya. In field surveys conducted in 2001, we also recorded forest spatial, structural, resource, and disturbance characteristics to determine the effects of habitat quality and fragmentation and the factors most critical to the continued survival of the little-known species. We tested 13 hypotheses to explain variation in patch occupancy and abundance patterns of Colobus angolensis palliatus in relation to habitat attributes. Minimal adequate models indicated that the occurrence of colobus in forest fragments is positively associated with fragment area and canopy cover, whereas the density of colobus in occupied fragments is attributable to forest area, the proportion of forest change over the previous 12 yr, and the basal area of 14 major food trees. Large-scale illegal extraction of major colobus food trees in the District for human resource use, in both protected and unprotected forests, together with ongoing forest clearance and modification, are the major threats to Colobus angolensis palliatus in Kenya.     

Forest fragmentation, the decline of an endangered primate, and changes in host-parasite interactions relative to an unfragmented forest

Forest fragmentation may alter host-parasite interactions in ways that contribute to host population declines. We tested this prediction by examining parasite infections and the abundance of infective helminths in 20 forest fragments and in unfragmented forest in Kibale National Park, Uganda. Over 4 years, the endangered red colobus (Procolobus rufomitratus) declined by 20% in fragments, whereas the black-and-white colobus (Colobus guereza) in fragments and populations of both colobines in unfragmented forest remained relatively stable. Seven nematodes (Strongyloides fulleborni, Strongyloides stercoralis, Oesophagostomum sp., an unidentified strongyle, Trichuris sp., Ascaris sp., and Colobenterobius sp.), one cestode (Bertiella sp.), and three protozoans (Entamoeba coli, Entamoeba histolytica/dispar, and Giardia sp.) were detected. Infection prevalence and the magnitude of multiple infections were greater for red colobus in fragmented than in unfragmented forest, but these parameters did not differ between forests for black-and-white colobus. Infective-stage colobus parasites occurred at higher densities in fragmented compared with unfragmented forest, demonstrating greater infection risk for fragmented populations. There was little evidence that the nature of the infection was related to the size of the fragment, the density of the host, or the nature of the infection in the other colobine, despite the fact that many of the parasites are considered generalists. This study suggests that forest fragmentation can alter host-parasite dynamics and demonstrates that such changes can correspond with changes in host population size in forest fragments.     

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.     

Parasite prevalence and richness in sympatric colobines: effects of host density

Factors that influence proximity and the number and duration of contacts among individuals can influence parasite transmission among hosts, and thus parasite prevalence and species richness are expected to increase with increasing host density. To examine this prediction we took advantage of a unique situation. Following the clearing of a forest fragment that supported red colobus (Piliocolobus tephrosceles) and black-and-white colobus (Colobus guereza), the animals moved into a neighboring fragment that we had been monitoring for a number of years and for which we had described the primate parasite community. After the animals immigrated into the fragment, the colobus populations more than doubled and colobus density became almost twice that found in Kibale National Park, Uganda. Despite this increase in host density, the richness of the parasite community did not increase. However, in both colobus species the prevalence of Trichuris sp., the only commonly occurring gastrointestinal parasite, increased. Over the next 5 years the prevalence and intensity of infection of Trichuris sp. in red colobus declined and their population numbers slowly increased. In contrast, the prevalence and intensity of infection of Trichuris sp. increased in black-and-white colobus and remained high following the immigration, and their population size declined. While Trichuris sp. infections are typically asymptomatic, we consider it a possibility that they contributed to the decline of the black-and-white colobus, and that the red colobus may be serving as a reservoir for Trichuris, thereby increasing the infection risk for black-and-white colobus.     

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.     

Life on the edge: gastrointestinal parasites from the forest edge and interior primate groups

Humans are responsible for massive changes to primate habitats, and one unanticipated consequence of these alterations may be changes in host-parasite interactions. Edges are a ubiquitous aspect of human disturbance to forest landscapes. Here we examine how changes associated with the creation of edges in Kibale National Park, Uganda, alter the parasite community that is supported by two species of African colobines: the endangered red colobus (Piliocolobus tephrosceles) and the black-and-white colobus (Colobus guereza). An analysis of 822 fecal samples from edge and forest interior groups revealed no difference in the richness of parasite communities (i.e., the number of parasite species recovered from the host's fecal sample). However, for both species the proportion of individuals with multiple infections was greater in edge than forest interior groups. The prevalence of specific parasites also varied between edge and forest interior groups. Oesophagostomum sp., a potentially deleterious parasite, was 7.4 times more prevalent in red colobus on the edge than in those in the forest interior, and Entamoeba coli was four times more prevalent in red colobus on the edge than in animals from the forest interior. Environmental contamination with parasites (measured as parasite eggs/gm feces) by red colobus from the edge and forest interior differed in a similar fashion to prevalence for red colobus, but it did not differ for black-and-white colobus. For example, egg counts of Oesophagostomum sp. were 10 times higher in red colobus from the edge than in those from the interior. The less severe infections in the black-and-white colobus relative to the red colobus may reflect the fact that black-and-white colobus raid agricultural crops while red colobus do not. This nutritional gain may facilitate a more effective immune response to parasites by the black-and-white colobus. The fact that animals on the edge are likely not nutritionally stressed raises an intriguing question as to what facilitates the elevated infections in edge animals. We speculate that interactions with humans may be linked to the observed patterns of infections, and hence that understanding the ecology of infectious diseases in nonhuman primates is of paramount importance for conservation and potentially for human-health planning.     

Group Size Dynamics over 15+ Years in an African Forest Primate Community

Group size affects many aspects of the ecology and social organization of animals. We investigated group size stability for five primate species in Kibale National Park, Uganda from 1996 to 2011 at three nested spatial scales. Survey data indicated that group sizes did not change for most species, with the exception of red colobus monkeys (Procolobus rufomitratus), in which group size increased at all spatial scales. Mangabey (Lophocebus albigena) group size increased in old‐growth forest, but the sample size and increase were small. To augment this survey data, we collected several years of demographic data on three habituated groups of redtail monkeys (Cercopithecus ascanius), eight groups of black‐and‐white colobus (Colobus guereza), and one red colobus group. The red colobus group increased from 59 to 104 individuals, while redtail monkey and black‐and‐white colobus group sizes were stable, mirroring our survey results. To understand mechanisms behind group size changes in red colobus versus stability in other primates, we monitored forest dynamics at two spatial scales between 1990 and 2013, considered changes in predator population, and explored evidence of disease dynamics. The cumulative size of all trees and red colobus food trees increased over 24 yr, suggesting that changing food availability was driving group size changes for red colobus, while predation and disease played lesser roles. Overall, our results and evidence of changing primate densities suggest that the Kibale primate community is in a non‐equilibrium state. We suggest future conservation and management efforts take this into consideration.     

Predicting folivorous primate abundance: validation of a nutritional model

Understanding the determinants of animal abundance has become more vital as ecologists are increasingly asked to apply their knowledge to the construction of informed management plans. However, there are few general models are available to explain variation in abundance. Some notable exceptions are studies of folivorous primates, in which the protein-to-fiber ratio of foods has been shown to predict biomass. Here we examine the generality of Milton's [American Naturalist 114:363-378, 1979] protein/fiber model by providing a detailed analysis of diet selection in black-and-white colobus monkeys (Colobus guereza), and applying the model to populations shown to be stable; an assumption not previously examined. Based on observations of two groups of black-and-white colobus in Kibale National Park, Uganda, and one group in a forest fragment, we documented that the animals selected young leaves that had more protein, were more digestible, and had a higher protein-to-fiber ratio than mature leaves. The mature leaves did not differ from young leaves with respect to secondary compounds or mineral content (with the exceptions of copper and zinc). All of the colobus groups selected foods with a high protein-to-fiber ratios. However, one group also selected more digestible foods, and in another group, foraging efforts were positively related to zinc and negatively related to potassium. Previous studies that examined Milton's protein/fiber model did not demonstrate that the study populations were stable. If some populations were not at carrying capacity, then the correlations drawn between food availability and/or quality and folivore biomass may have been spurious. To address this issue, we censused a series of forest fragments in 1995 and again in 2000. We found that the populations in these fragments had declined from 165 in 1995 to 119 animals in 2000. However, based on evidence of population stability and lack of forest disturbance, we concluded that five of the original populations were stable. The biomass of these populations was related to the protein-to-fiber ratio of the fragment's trees. Combining our data with published data, we demonstrate that the protein-to-fiber ratios of mature leaves available to these folivorous primates accounted for 87% of the variance in their biomass.     

Dental sexual dimorphism and morphology in african colobus monkeys as related to diet

We considered the relationship between dental sexual dimorphism and diet in 542 specimens of olive, red, and black-and-white colobus. Using univariate statistical techniques, we examined 41 measurements of the maxillary and mandibular dentitions. The results reveal two trends of dental sexual dimorphism in black-and-white colobus wherein (i) maleColobus guereza andC. angolensis are generally larger than females throughout the dentition and (ii)C. satanas and, to a lesser degree,C. polykomos exhibit reduced sexual differences in the canine base and females are slightly larger than males in noncanine dimensions. Females of the red colobus,Procolobus (Piliocolobus) badius, are slightly larger than males in most noncanine measurements but canine sex differences are more pronounced than those of black-and-white colobus.Procolobus (Procolobus) verus, the olive colobus, is characterized by some of the largest canine sex differences, yet the sexes do not differ much in noncanine mean values. When patterns of sexual dimorphism are considered in terms of specific ecology and behavior, it is possible to relate sex differences, in part, to known dietary differences. For example, overall dental morphology and the trend of sexual differences inC. satanas andC. polykomos seem to be associated with the consumption of a diet rich in seeds. The pattern of dental sexual dimorphism inC. badius may also be influenced by dietary factors in that their patrilineal social organization could restrict female access to certain foods thereby affecting rates of attrition and creating selection pressure for larger teeth. Relatively less is known of the ecology and social organization ofP. verus but their dental sexual dimorphism is possibly less related to dietary factors than is the case for red or black-and-white colobus.     

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.     

Application of Protein-to-Fiber Ratios to Predict Colobine Abundance on Different Spatial Scales

The biomass of arboreal folivorous primates in Africa and Asia is related to an index of mature leaf quality: the ratio of protein-to-fiber concentration. Investigations have considered variation in folivore biomass and forest composition among sites separated by hundreds or thousands of km. However, large variation in folivore abundance has been documented over much smaller spatial scales. We quantify the degree to which the average protein-to-fiber ratio of mature leaves of the 20 most abundant tree species predicts the biomass of western red colobus (Piliocolobus trephosceles) and black-and-white colobus (Colobus guereza) over very small spatial scales. Four sites within Kibale National Park, Uganda, varied markedly in forest structure. Colobine biomass varied among sites from 191 to 2675 kg/km² and was related to the average protein-to-fiber ratio of mature leaves of the 20 most abundant tree species at each site. We examined the generality of the relationship between protein-to-fiber ratios and colobine abundance by adding our biomass and leaf chemistry values to previously published values to produce 9 comparable sites. At these locations, colobine biomass varied from 84 to 2675 kg/km² (mean biomass among sites = 910 kg/km²), and mean protein/fiber ratios varied from 0.167 to 0.577. Colobine biomass was related to the protein-to-fiber ratios of mature leaves (R ² = 0.616, P = 0.012).     

Do food availability,parasitism, and stress have synergistic effects on red colobus populations living in forest fragments?

Identifying factors that influence animal density is a fundamental goal in ecology that has taken on new importance with the need to develop informed management plans. This is particularly the case for primates as the tropical forest that supports many species is being rapidly converted. We use a system of forest fragments adjacent to Kibale National Park, Uganda, to examine if food availability and parasite infections have synergistic affects on red colobus (Piliocolobus tephrosceles) abundance. Given that the size of primate populations can often respond slowly to environmental changes, we also examined how these factors influenced cortisol levels. To meet these objectives, we monitored gastrointestinal parasites, evaluated fecal cortisol levels, and determined changes in food availability by conducting complete tree inventories in eight fragments in 2000 and 2003. Red colobus populations declined by an average of 21% among the fragments; however, population change ranged from a 25% increase to a 57% decline. The cumulative basal area of food trees declined by an average of 29.5%; however, forest change was highly variable (a 2% gain to a 71% decline). We found that nematode prevalence averaged 58% among fragments (range 29-83%). The change in colobus population size was correlated both with food availability and a number of indices of parasite infections. A path analysis suggests that change in food availability has a strong direct effect on population size, but it also has an indirect effect via parasite infections.     

Population size and density of Colobus vellerosus at the Boabeng-Fiema Monkey Sanctuary and surrounding forest fragments in Ghana

The Boabeng-Fiema Monkey Sanctuary (BFMS) is inhabited by a growing population of Ursine colobus (Colobus vellerosus), a species that is listed as vulnerable. Smaller, degraded forest fragments that surround the BFMS also contain C. vellerosus and may provide an important habitat for the monkeys. Our objectives were to 1) determine the current population size and density of C. vellerosus at BFMS and in five surrounding fragments, 2) examine the differences in demographics between the fragments and BFMS, and 3) determine whether a relationship exists between population density and fragment size and isolation distance from BFMS. The census was a complete count and was conducted for 1 month (July 2003) by S.W. and trained research assistants. Seven census routes were walked simultaneously on 13 days. The 2003 population estimate of C. vellerosus at BFMS was 217-241 individuals (15 groups), a slight increase from the 2000 census. Numbers in the fragments (58-62, six groups) have remained stable since 1997, when the only other census of these fragments was conducted. Mean group size did not differ between the fragments and BFMS. Larger fragments had larger numbers of colobus, but there was no relationship between fragment size and colobus density. Isolation distance had no effect on population density. Our data suggest that colobus probably travel between fragments. Conservation efforts should focus on treating the small forests and their connecting areas as a single conservation unit.     

The status ofColobus polykomos dollmani Schwarz

The two West African black-and-white colobus taxa,Colobus polykomos andC. vellerosus, are distinct species. A supposedly intermediate subspecies,C. polykomos dollmani, is actually a hybrid swarm, in whichC. vellerosus genes greatly predominate. We propose a hypothesis to explain this situation.     

Comparison of habitat quality and diet of Colobus vellerosus in forest fragments in Ghana

The forest fragments surrounding the Boabeng-Fiema Monkey Sanctuary (BFMS) in central Ghana shelter small populations of Colobus vellerosus. Little is known about these populations or the ability of the fragments to support them, despite the fact that these fragments represent potentially important habitat for the colobus in this region. We compared the diet of three groups of C. vellerosus in the fragments to two groups in BFMS. We also examined the differences in plant species composition and food abundance among fragments. The study took place from June to November 2003. Dietary data were collected using scan sampling. Plant species composition and food abundance were evaluated using tree plots and large tree surveys. As in BFMS groups, leaves constituted the highest proportion of the diet of fragment groups, yet the colobus in fragments fed on more lianas than did those in BFMS. Over 50% of all species observed eaten by colobus in the fragments were not consumed in BFMS groups during the same season. Food abundance was similar between fragments and BFMS, although species composition differed. There was no relationship between the density of colobus and the density of food trees or percentage of food species, suggesting that other factors may be influencing the number of colobus present. This study highlights the broad dietary range of C. vellerosus, which may be a factor allowing its survival in these fragments.     

Cross-species handling of colobine infants

At Tiwai Island, Sierra Leone, several instances of red colobus (Procolobus badius) adults handling white infants of black-and-white colobus monkeys (Colobus polykomos) were observed. These observations are described and their significance is discussed.     

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.     

Gastrointestinal parasites of the colobus monkeys of Uganda

From August 1997 to July 2003, we collected 2,103 fecal samples from free-ranging individuals of the 3 colobus monkey species of Uganda-the endangered red colobus (Piliocolobus tephrosceles), the eastern black-and-white colobus (Colobus guereza), and the Angolan black-and-white colobus (C. angolensis)--to identify and determine the prevalence of gastrointestinal parasites. Helminth eggs, larvae, and protozoan cysts were isolated by sodium nitrate flotation and fecal sedimentation. Coprocultures facilitated identification of helminths. Seven nematodes (Strongyloides fulleborni, S. stercoralis, Oesophagostomum sp., an unidentified strongyle, Trichuris sp., Ascaris sp., and Colobenterobius sp.), 1 cestode (Bertiella sp.), 1 trematode (Dicrocoeliidae), and 3 protozoans (Entamoeba coli, E. histolytica, and Giardia lamblia) were detected. Seasonal patterns of infection were not apparent for any parasite species infecting colobus monkeys. Prevalence of S. fulleborni was higher in adult male compared to adult female red colobus, but prevalence did not differ for any other shared parasite species between age and sex classes.     

The Angola black-and-white colobus (Colobus angolensis palliatus) in Kenya: historical range contraction and current conservation status

The Angola black-and-white colobus (Colobus angolensis palliatus) is a flagship species for Kenya's coastal forests, a global biodiversity hotspot and a region for "priority" conservation investment. This study provides the first evaluation of colobus distribution, status, and current threats within its Kenyan range: the southern coastal District of Kwale. Line transect and sweep count surveys were carried out between July and November of 2001, covering 25,514 ha of coastal forest within 124 forest fragments. A total of 55 colobus populations were located, with total Kenyan C. a. palliatus population estimates ranging between 3,100 and 5,000 individuals (560-900 groups). The Shimba Hills National Reserve protects both the largest forest and largest colobus population in the District. A total of 3,000 ha of coastal forest (12%) still remain unprotected and provide critical habitat for over 17% of the national colobus population. The Diani and Shimoni forests in particular, are highlighted as key habitat for future colobus (and coastal forest) conservation initiatives. Local semistructured interviews and archival research into the historical distribution of the taxon in North Coast Kenya confirmed its occurrence (and subsequent range contraction) in the Kilifi District, with the last sightings occurring in the Arabuko Sokoke Forest in 1979. Differences in the settlement distribution, associated habitat loss and hunting preferences of the nine coastal tribes (Mijikenda) may explain why colobus have disappeared from the north coast, but persist in the south.     

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.