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.     

Primate population dynamics: variation in abundance over space and time

The rapid disappearance of tropical forests, the potential impacts of climate change, and the increasing threats of bushmeat hunting to wildlife, makes it imperative that we understand wildlife population dynamics. With long-lived animals this requires extensive, long-term data, but such data is often lacking. Here we present longitudinal data documenting changes in primate abundance over 45 years at eight sites in Kibale National Park, Uganda. Complex patterns of change in primate abundance were dependent on site, sampling year, and species, but all species, except blue monkeys, colonized regenerating forest, indicating that park-wide populations are increasing. At two paired sites, we found that while the primate populations in the regenerating forests had increased from nothing to a substantial size, there was little evidence of a decline in the source populations in old-growth forest, with the possible exception of mangabeys at one of the paired sites. Censuses conducted in logged forest since 1970 demonstrated that for all species, except black-and-white colobus, the encounter rate was higher in the old-growth and lightly-logged forest than in heavily-logged forest. Black-and-white colobus generally showed the opposite trend and were most common in the heavily-logged forest in all but the first year of monitoring after logging, when they were most common in the lightly-logged forest. Overall, except for blue monkey populations which are declining, primate populations in Kibale National Park are growing; in fact the endangered red colobus populations have an annual growth rate of 3%. These finding present a positive conservation message and indicate that the Uganda Wildlife Authority is being effective in managing its biodiversity; however, with constant poaching pressure and changes such as the exponential growth of elephant populations that could cause forest degradation, continued monitoring and modification of conservation plans are needed.     

Giardia sp. and Cryptosporidium sp. infections in primates in fragmented and undisturbed forest in western Uganda

In June 2005, we collected 115 fecal samples from wild primates in western Uganda and examined them for Cryptosporidium sp. and Giardia sp. with the use of immunofluorescent antibody (IFA) detection. We sampled primates from an undisturbed forest in Kibale National Park and from 3 highly disturbed forest fragments outside the park. Of disturbed forest samples, red colobus (Pilocolobus tephrosceles) and red-tailed guenons (Cercopithecus ascanius) harbored species of Cryptosporidium or Giardia, but black-and-white colobus (Colobus guereza) did not. All primate samples from undisturbed forest were negative for both parasites. Seven of 35 (20%) red colobus and 1 of 20 red-tailed guenons (5%) from forest fragments were infected with either Cryptosporidium sp. or Giardia sp. The presence of Cryptosporidium and Giardia species in primates living in forest fragments, but not in primates in undisturbed forest, suggests that habitat disturbance may play a role in transmission or persistence of these pathogens.     

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.     

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.     

Habitat alteration and the conservation of African primates: case study of Kibale National Park, Uganda

Tropical forests and the animals they support are being threatened by accelerating rates of forest conversion and degradation. In a continually fluctuating sociopolitical world, it is often impossible to protect areas from such conversion until the political environment is suitable to pursue conservation goals, by which time, the forests have often been converted to other uses. This reality suggests a need for inquiry into which primate species can persist after different types of disturbances and how quickly primate communities can recover from disturbance. Here we examine the persistence of primate populations in disturbed habitats by providing a case study of patterns of primate abundance in areas of Kibale National Park (766 km2), Uganda, that have been modified by different types and intensities of human activities, primarily commercial logging and agricultural clearing. Distributional surveys at 24 sites and detailed line-transect censuses at six sites demonstrate that primate populations in Kibale are often high and suggest that patterns of population change associated with disturbance are complex. Analysis of the land use coverage of Kibale reveals that abandoned farms (10.3%) and degraded forest (8.7%) now cover 146 km2. Unfortunately, we do not know what proportion of the farms were established on areas that were forest versus grassland. However, if the areas that are now abandoned farms were all once forested, this means that 79 km2 of forest has been lost. Based on density estimates from nearby sites, this would represent a loss of 52,612 monkeys and 200 chimpanzees. Populations would also have been affected by the degradation of the 66 km2 (8.7%) of forest. These estimates of the potential reductions in the primate populations that could have resulted from forest clearing and degradation illustrate the importance of protecting land. A review of the literature illustrates that the biomass of primates found within Kibale is very high in comparison to other locations and thus illustrates the importance of Kibale to regional conservation.     

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.     

Density Estimation of the Endangered Udzungwa Red Colobus (Procolobus gordonorum) and Other Arboreal Primates in the Udzungwa Mountains Using Systematic Distance Sampling

Estimates of population density and abundance are essential for the assessment of nonhuman primate conservation status, especially in view of increasing threats. We undertook the most extensive systematic primate survey yet of the Udzungwa Mountains of Tanzania, an outstanding region for primate endemism and conservation in Africa. We used distance sampling to survey three arboreal monkey species, including the endangered and endemic Udzungwa red colobus (Procolobus gordonorum). Overall, we encountered 306 primate clusters over 287 km walked along 162 line transects. We found the lowest cluster densities for both red colobus and Angolan colobus (Colobus angolensis; 0.8 clusters/km²) in the least protected forest (Uzungwa Scarp Forest Reserve, US), while we found the highest densities (3.2 and 2.6 clusters/km² for red colobus; 3.2 and 2.7 clusters/km²for Angolan colobus) in two large and protected forests in the national park. Unexpectedly, Magombera, a small forest surrounded by plantations, had the highest densities of red colobus (5.0 clusters/km²), most likely a saturation effect due to the rapid shrinking of the forest. In contrast, Sykes’ monkey (Cercopithecus mitis monoides/moloneyi) had more similar densities across forests (3.1–6.6 clusters/km²), including US, suggesting greater resilience to disturbance in this species. For the endemic red colobus monkey, we estimated an abundance of 45–50,000 individuals across all forests, representing ca. 80% of the global population. Though this is a relatively high abundance, the increasing threats in some of the Udzungwa forests are of continued concern for the long-term survival of red colobus and other primates in the area.     

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.     

Primate population dynamics over 32.9 years at Ngogo, Kibale National Park, Uganda

We present census data for eight primate species spanning 32.9 years along the same transect at Ngogo, Kibale National Park, Uganda, demonstrating major changes in the composition of the primate community. Correlated with an estimated decline of ～89% in the red colobus population was an increase in encounter rates with chimpanzee parties. Our data, along with the unusually high rates of predation by chimpanzees on red colobus at Ngogo and the fact that the chimpanzee community at Ngogo is the largest ever recorded, support the conclusion that the red colobus decline was caused primarily by chimpanzee predation. This seems to be the first documented case of predation by one nonhuman primate causing the population decline in another. We evaluated disease and interspecific competition as other possible causes of the red colobus decline, but judged them to be relatively insignificant compared with predation by chimpanzees. Notable changes in encounter rates with other primate species may have resulted from forest expansion. Those for mangabeys, redtails, and black and white colobus increased significantly. Encounter rates increased for l'Hoest's monkeys too, but the increased sightings may have been an artifact of increased habituation. Sightings of blue monkey and baboon groups declined. There was no significant change in encounter rates for all species combined. The Ngogo primate community seemed to be in a nonequilibrium state, changing from one dominated by two species, a folivore (red colobus) and a frugivorous omnivore (redtails), to one dominated by three species of frugivorous omnivores (redtails, mangabeys, and chimpanzees). This study demonstrates the importance of long-term monitoring in understanding population dynamics and the role of intrinsic variables in shaping the species composition of a community.     

Primate Community Dynamics in Old Growth Forest over 23.5 Years at Ngogo,Kibale National Park,Uganda: Implications for Conservation and Census Methods

Few data exist regarding long-term changes in primate populations in old-growth, tropical forests. In the absence of this information, it is unclear how to assess population trends efficiently and economically. We addressed these problems by conducting line-transect censuses 23.5 years apart at the Ngogo study area in Kibale National Park, Uganda. We conducted additional censuses over short time intervals to determine the degree to which the temporal distribution of censuses affected estimates of primate numbers. Results indicate that two species, blue monkeys and red colobus, may have experienced significant reductions over the past 23.5 years at Ngogo. In contrast, five other species, baboons, black-and-white colobus, chimpanzees, mangabeys, and red-tailed guenons, have not changed in relative abundance. Additional findings indicate that different observers may vary significantly in their estimates of sighting distances of animals during censuses, thus rendering the use of measures of absolute densities problematic. Moreover, censuses conducted over short periods produce biased estimates of primate numbers. These results provide guidelines for the use of line-transect censuses and underscore the importance of protecting large blocks of forests for primate conservation.     

Population Declines of Colobus in Western Uganda and Conservation Value of Forest Fragments

The processes of habitat loss and fragmentation are probably the most important threats to biodiversity. It is critical that we understand the conservation value of fragments, because they may represent opportunities to make important conservation gains, particularly for species whose ranges are not in a protected area. However, our ability to understand the value of fragments for primates is limited by the fact that researchers have conducted many studies in protected areas, which do not represent most fragments, and studies are typically short term. Here we determine the long-term survival probability of red (Procolobus pennantii) and black-and-white colobus (Colobus guereza) inhabiting forest fragments outside of Kibale National Park, Uganda. Local communities use the fragments primarily for subsistence agriculture and fuelwood. We surveyed primate populations 3 times over 8 yr, made a total inventory of all trees 2 times, contrasted behavior of groups inhabiting 1 fragment with groups in the continuous forest, and judged the conservation value of the fragments by quantifying patterns of forest use by local people. Of the 20 fragments surveyed, 16 supported resident populations of colobus in 1995, 2 were cleared in 2000, and an additional 2 fragments were cleared by 2003. In 1995 we counted 165 black-and-white colobus, whereas in 2000 and 2003, we counted 119 and 75 individuals, respectively. Seven fragments supported red colobus in 1995, 11 in 2000, and 9 in 2003. In 2000 we counted 159 red colobus, while in 2003, we saw 145 individuals. For both species, activity patterns in continuous forest were similar to those in a fragment, with the exception that individuals in the fragment rested more. Colobus in the fragment ate more mature leaves than colobus in the continuous forest did. Fragments supported all the fuelwood needs of an average of 32 people who lived immediately adjacent to them, and partially supported families up to 3 farms away (ca. 400 m), representing 576 people. Intensive harvesting for fuelwood occurred when neighboring households engaged in beer brewing (an average of 9.6% of the households), gin distilling (8.8%), or charcoal production (14.5%). Overall, between 2000 and 2003, the average density of trees declined by 14 trees/ha (range = 0–60 trees/ha). If current rates of clearing continue, the probability that the fragments will continue to support colobus populations is low.     

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.     

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.     

Vegetative predictors of primate abundance: utility and limitations of a fine-scale analysis

Determining ecological predictors of primate abundance is important for both theoretical and applied conservation management. For forest primates, research has focused on comparisons of primate abundance and vegetation in different forest blocks or forest compartments with different management histories. However, great variation in primate abundance often occurs within single forests, especially in mountainous areas or in areas with habitat mosaics due to past disturbance. Here we assess, for the first time, the usefulness and limitations of small-scale, within-transect analysis of vegetative parameters as predictors of primate abundance in a very heterogeneous forest habitat in the Udzungwa Mountains of Tanzania. Relative abundance of four species of diurnal primates was recorded over a period of 2.5 years by walking three census transects 48 times each. Tree size, density, species composition, and food plants were measured along the same census lines. The fine-scale relationship between primate abundance and vegetative variables was analyzed through generalized linear modeling applied to 58 segments of these three census lines. Each segment was 200 m in length. For all four primate species, we found significant associations between their abundance and selected vegetative variables. The abundance of the endemic and endangered Udzungwa red colobus Procolobus gordonorum was positively related to mean basal area of large trees (diameter at breast height greater than 20 cm) and to the species richness of their food plants. Considering the very great variation in primate abundance that was recorded among segments of the census lines, our approach proved useful in predicting the relationship between primate abundance and small-scale habitat differences. The main limitation of this study, however, was the relatively low-predictive power of the models for some species, especially the Angolan colobus Colobus angolensis. We discuss the potential reasons for this problem and suggest possible improvements for future studies.     

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.     

Long-term dynamics of wild primate populations across forests with contrasting protection in Tanzania

Anthropogenic activities driving tropical forests' loss imperil global biodiversity and provision of ecosystem services. In this context, systematic monitoring programs evaluating wildlife trends are essential. Non-human primates are relevant conservation targets since they represent vital components of tropical forests by serving as pollinators and seed dispersers. Here, we present primate group counts data collected over 19 years in a primate hotspot in Tanzania. We analyzed data with a hierarchical dynamic model accounting for imperfect detection that estimates local group abundance and temporal rates of change, to assess whether habitat protection explained trends of the arboreal and diurnal Peters' Angola colobus (Colobus angolensis palliatus), Udzungwa red colobus (Piliocolobus gordonorum), and Tanzania Sykes' monkey (Cercopithecus mitis subsp. moloneyi). We targeted populations occurring in two forest blocks with contrasting protection regimes, with one block impacted by targeted poaching of the two Colobus species. We found that these latter species were much less abundant in the more human impacted forest, underwent a rapid decline, and subsequently remained at low abundance and without signs of recovery once this forest was granted greater protection. Instead, Sykes' abundance did not differ between forests, and improved protection was associated with a slight increase in abundance. Age class composition for social groups of both Colobus species differed between forests, indicating altered births and survivorship rates in the impacted forest. Results suggest that targeted hunting can prevent recovery for several years and even after increased habitat protection. Our approach appears valuable to monitor population dynamics over the long term, highlighting species-specific variations in both vulnerability to anthropogenic disturbance and recovery patterns in primate populations.     

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.     

Butterfly Community Composition Across a Successional Gradient in a Human‐disturbed Afro‐tropical Rain Forest

Knowledge of the recovery of insect communities after forest disturbance in tropical Africa is very limited. Here, fruit‐feeding butterflies in a tropical rain forest at Kibale National Park, Uganda, were used as a model system to uncover how, and how fast, insect communities recover after forest disturbance. We trapped butterflies monthly along a successional gradient for one year. Traps were placed in intact primary forest compartments, heavily logged forest compartments with and without arboricide treatment approximately 43 years ago, and in conifer‐clearcut compartments, ranging from 9 to 19 years of age. The species richness, total abundance, diversity, dominance, and similarity of the community composition of butterflies in the eight compartments were compared with uni‐ and multivariate statistics. A total of 16,728 individuals representing 88 species were trapped during the study. Butterfly species richness, abundance, and diversity did not show an increasing trend along the successional gradient but species richness and abundance peaked at intermediate stages. There was monthly variation in species richness, abundance, diversity and composition. Butterfly community structure differed significantly among the eight successional stages and only a marginal directional change along the successional gradient emerged. The greatest number of indicator species and intact forest interior specialists were found in one of the primary forests. Our results show that forest disturbance has a long‐term impact on the recovery of butterfly species composition, emphasizing the value of intact primary forests for butterfly conservation.     

Primate DNA suggests long‐term stability of an African rainforest

Red colobus monkeys, due to their sensitivity to environmental change, are indicator species of the overall health of their tropical rainforest habitats. As a result of habitat loss and overhunting, they are among the most endangered primates in the world, with very few viable populations remaining. Traditionally, extant indicator species have been used to signify the conditions of their current habitats, but they have also been employed to track past environmental conditions by detecting previous population fluctuations. Kibale National Park (KNP) in Uganda harbors the only remaining unthreatened large population of red colobus. We used microsatellite DNA to evaluate the historical demography of these red colobus and, therefore, the long‐term stability of their habitat. We find that the red colobus population throughout KNP has been stable for at least ~40,000 years. We interpret this result as evidence of long‐term forest stability because a change in the available habitat or population movement would have elicited a corresponding change in population size. We conclude that the forest of what is now Kibale National Park may have served as a Late Pleistocene refuge for many East African species.