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.     

The importance of well protected forests for the conservation genetics of West African colobine monkeys

In tropical forests, anthropogenic activities are major drivers of the destruction and degradation of natural habitats, causing severe biodiversity loss. African colobine monkeys (Colobinae) are mainly folivore and strictly arboreal primates that require large forests to subsist, being among the most vulnerable of all nonhuman primates. The Western red colobus Piliocolobus badius and the King colobus Colobus polykomos inhabit highly fragmented West African forests, including the Cantanhez Forests National Park (CFNP) in Guinea-Bissau. Both species are also found in the largest and best-preserved West African forest—the Taï National Park (TNP) in Ivory Coast. Colobine monkeys are hunted for bushmeat in both protected areas, but these exhibit contrasting levels of forest fragmentation, thus offering an excellent opportunity to investigate the importance of well-preserved forests for the maintenance of evolutionary potential in these arboreal primates. We estimated genetic diversity, population structure, and demographic history by using microsatellite loci and mitochondrial DNA. We then compared the genetic patterns of the colobines from TNP with the ones previously obtained for CFNP and found contrasting genetic patterns. Contrary to the colobines from CFNP that showed very low genetic diversity and a strong population decline, the populations in TNP still maintain high levels of genetic diversity and we found no clear signal of population decrease in Western red colobus and a limited decrease in King colobus. These results suggest larger and historically more stable populations in TNP compared to CFNP. We cannot exclude the possibility that the demographic effects resulting from the recent increase of bushmeat hunting are not yet detectable in TNP using genetic data. Nevertheless, the fact that the TNP colobus populations are highly genetically diverse and maintain large effective population sizes suggests that well-preserved forests are crucial for the maintenance of populations, species, and probably for the evolutionary potential in colobines.     

GeMBiD,a Geometric Morphometric Approach to the Study of Biological Diversity: An Example Study of the Red Colobus (<Emphasis Type="Italic">Procolobus</Emphasis> [<Emphasis Type="Italic">Piliocolobus</Emphasis>]) Species Complex

Determining conservation priorities requires an understanding of biological diversity in terms of both genetic variation and phenotypic difference. The phenotype is where many adaptations are expressed and thus provides the potential for future evolution, including responses to rapidly changing environments. We suggest that applying geometric morphometrics (a set of methods related to image analysis) to the study of morphological differences among closely related populations can effectively quantify phenotypic variation in poorly studied taxa, and provide an informative estimate of the degree of morphological divergence relative to their better known relatives. The approach is simple and flexible, but has proven to be powerful. As an example of a Geometric Morphometric approach to the study of Biological Diversity (GeMBiD), we provide a preliminary estimate of the morphological distinctiveness of a poorly studied red colobus monkey, the Semliki red colobus (Procolobus sp. ellioti), by using cross-validated discriminant analyses on cranial shape data and comparing chance-corrected classification accuracy in this population with that of other populations of monkeys within and outside the red colobus lineage. By fruitfully exploiting available museum collections and by developing networks of scientists who can provide information on and study material from rare populations, GeMBiD could become a useful tool for complementing genetic analyses of biodiversity.     

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.     

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

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

Dyadic associations of red Colobus and diana monkey groups in the Taï National Park, Ivory Coast

Members of the genus Colobus have been observed to associate frequently with Cercopithecus monkeys in several African sites. In the Taï National Park, Ivory Coast, one group of western red colobus was found to be in association with one particular group of diana monkeys more than could be expected by chance (Holenweg et al., 1996). We show that dyadic association is not an idiosyncrasy of these two groups, but rather a pattern that is general for our study site. All five red colobus groups we studied were closely associated with diana monkeys during more than 60% of the time. Four groups had one particular diana partner group, the fifth two different partners. Apart from the red colobus, three more primate species, the olive colobus, Campbell's monkey, and the lesser spot-nosed monkey, were also strongly attracted to diana monkeys.     

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.     

Genetic evidence for spatio‐temporal changes in the dispersal patterns of two sympatric African colobine monkeys

Western black‐and‐white colobus and Temmink's red colobus are two forest‐dependent African primates with similar ecological requirements, often found in sympatry. Their most striking difference lies in their social system: black‐and‐white colobus live in small groups with mainly male‐mediated dispersal but where females can also disperse, whereas red colobus live in larger groups with males described as philopatric. To investigate whether genetic evidence supports the reported patterns of dispersal based on observational data, we examined eight black‐and‐white and six red colobus social groups from Cantanhez National Park, Guinea‐Bissau. Microsatellite markers revealed a lack of sex‐biased dispersal for black‐and‐white colobus. Gene flow, mainly mediated by females, better explained the genetic patterns found in red colobus, with some evidence for less extensive male dispersal. In contrast to the microsatellite data, low mitochondrial diversity for the black‐and‐white colobus suggests that historical and/or long‐range male‐mediated gene flow might have been favored. In red colobus, the co‐existence of three divergent mitochondrial haplogroups suggests that the Cantanhez population contains a secondary contact zone between divergent lineages that evolved in allopatry. Female‐biased dispersal in this species may be a major factor contributing to the colonization by such differentiated mitochondrial lineages in the region. Overall, we find evidence for a spatio‐temporal change in the dispersal patterns of the colobus monkeys of Cantanhez, with mitochondrial DNA indicating dispersal by mainly a single sex and microsatellite data suggesting that recently both sexes appear to be dispersing within the population. Am J Phys Anthropol, 2013. © 2013 Wiley Periodicals, Inc.     

Conservation and Survival Adaptations of Temminck’s Red Colobus <Emphasis Type="Italic">(Procolobus badius temmincki)</Emphasis>, in Senegal

In the Fathala Forest, Saloum Delta National Park, Senegal, in 1974–1976 and 1988–2002, we studied the northernmost populations of the endangered Temminck’s red colobus (Procolobus badius temmincki). Drastic habitat changes in the last 30 yr have reduced the forests by > 50% (75% in the gallery forests used by the red colobus). The woody species diversity decreased by > 30%. Despite these changes, the red colobus population only decreased from ca. 600 to ca. 500 individuals. We examined the ecological conditions and behavioral adaptations that may have influenced survival of the population. We found that 5 major adaptations have emerged in the last 30 yr that may have influenced the survival of red colobus at Fathala: (1) frugivory, (2) terrestriality, (3) tendency to form polyspecific associations with green monkeys, (4) tendency to frequent more open habitats, and (5) use of mangrove swamps for refuge and forage. By developing these adaptations, red colobus demonstrated their ability to persist in degraded habitats of the Fathala Forest. Preserving the forest should ensure the conservation of the red colobus population there.     

Competing pressures on populations: long-term dynamics of food availability,food quality,disease, stress and animal abundance

Despite strong links between sociality and fitness that ultimately affect the size of animal populations, the particular social and ecological factors that lead to endangerment are not well understood. Here, we synthesize approximately 25 years of data and present new analyses that highlight dynamics in forest composition, food availability, the nutritional quality of food, disease, physiological stress and population size of endangered folivorous red colobus monkeys (Procolobus rufomitratus). There is a decline in the quality of leaves 15 and 30 years following two previous studies in an undisturbed area of forest. The consumption of a low-quality diet in one month was associated with higher glucocorticoid levels in the subsequent month and stress levels in groups living in degraded forest fragments where diet was poor was more than twice those in forest groups. In contrast, forest composition has changed and when red colobus food availability was weighted by the protein-to-fibre ratio, which we have shown positively predicts folivore biomass, there was an increase in the availability of high-quality trees. Despite these changing social and ecological factors, the abundance of red colobus has remained stable, possibly through a combination of increasing group size and behavioural flexibility.     

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.     

Population Sizes and Distribution of Primates in the Lower Tana River Forests,Kenya

We studied the population size and distribution of diurnal primates in the lower Tana River forests, Kenya. They are the only remaining habitats for 2 threatened primates: the Tana River red colobus (Procolobus rufomitratus) and the Tana River crested mangabey (Cercocebus galeritus galeritus). We conducted censuses in 73 forest patches from January through March 2001. We estimate population size of the red colobus to be 788 individuals in 82 groups and that of the crested mangabeys to be 2,070 individuals in 59 groups. The data suggest that over a 7-year period (1994-2001), there was an 18% increase in the crested mangabey population and a 5% decline in red colobus numbers. Further, the red colobus range has expanded both north and south, whereas that of crested mangabeys has only expanded south. Fifty-six percent of crested mangabeys and 46% of red colobus groups were inside the Tana River Primate National Reserve (TRPNR). Other primates encountered included 170 groups of Sykes' monkeys (Cercopithecus mitis), 70 groups of yellow baboons (Papio cynocephalus) and 4 groups of grivets [Chlorocebus (Cercopithecus) aethiops]. Mean group densities of the 2 endangered primates and of baboons were higher inside than outside the TRPNR, reinforcing the importance of TRPNR for their conservation. An intervention program is required to stem further decline in the red colobus population and to protect small isolated groups in forest patches outside TRPNR.     

Implications of small scale variation in ecological conditions for the diet and density of red colobus monkeys

In this 3-year investigation we documented patterns of density, diet, and activity of red colobus monkeys (Procolobus tephrosceles) in six areas in or near Kibale National Park, Uganda and related these patterns to availability of food resources. There were large differences in the density and behavior of the red colobus among the sites. For example, the red colobus at one site with a diverse plant community of more than 61 tree species, had a diet that included at least 42 species. In contrast, at a second site red colobus spent 92% of their feeding time eating from one species that dominated the tree community. The density of important red colobus food trees varied among sites from 32 trees/ha to 204 trees/ha, and red colobus density ranged from 0.70 groups/km² to 7.41 groups/km². Among sites, red colobus density was related to the cumulative DBH of important food trees, when one apparently anomalous site was excluded, and populations with more plant species in their diets tended to be those that were found at higher densities. Activity budgets of the red colobus populations varied markedly among sites. For example, feeding time ranged among sites from 29 to 55%, and traveling varied from 5 to 20%. When faced with increased foraging demands, red colobus reduced the time spent resting, while the time spent socializing remained fairly constant. Comparative socioecological studies typically contrast species separated by large geographical distances to ensure there is sufficient variation in the environment to detect behavioral responses. The marked differences in ecological conditions and red colobus behavior we documented over short geographical distances, suggests that small-scale contrasts are a useful tool to examine ecological determinants of behavior and community structure.     

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

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

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.     

Primate census and habitat evaluation in the Tana delta region, Kenya

Nineteen indigenous forest patches in the Tana River delta region, Kenya were surveyed between October and November 2000 for primates and habitat disturbance. Special emphasis was placed on the endangered Tana River red colobus (Procolobus rufomitratus Peters) and crested mangabeys (Cercocebus galeritus galeritus Peters), both of which are endemic to the region. Habitat disturbances evident in the forests included cutting of trees, harvesting of thatching material, firewood collection, dyke construction, cultivation, palm wine tapping and charcoal burning. A total of 85 groups of five primate species were counted. These comprised eighteen, ten, 22, 31 and four groups of red colobus, crested mangabey, baboons (Papio cynocephalus L.), sykes monkeys (Cercopithecus mitis Wolf) and vervet monkeys (Cercopithecus aethiops L.), respectively. A wider distribution of red colobus and crested mangabeys than was documented previously was noted, implying that they are probably more abundant than hitherto reported. It is hypothesized that extensive studies on some fauna considered endangered world‐wide would probably redefine their conservation status. Future studies in the lower Tana River region should cover the previously unsurveyed forests and focus on ways of curbing forest destruction.     

Mitochondrial relationships and divergence dates of the African colobines: evidence of Miocene origins for the living colobus monkeys

The African colobines represent a neglected area of cercopithecid systematics. Resolving the phylogenetic relationships and estimating divergence dates among the living forms will provide insight into the evolution of this group and may shed light upon the evolution of other African primates as well. This is the first molecular assessment of the evolutionary relationships among the modern colobus monkeys, which are comprised of the black-and-white, olive, and red colobus groups. Over 4,000 base pairs of mitochondrial DNA were amplified and sequenced in over 40 colobus monkey individuals incorporating representatives from all commonly recognized species. Gene trees were inferred using maximum likelihood and Bayesian inference, and penalized likelihood was employed to estimate mitochondrial divergence dates among the sampled taxa. The results are congruent with some aspects of previous phylogenetic hypotheses based on morphology and vocalizations, although the relationships among several West and Central African taxa differ to some degree. The divergence date analysis suggests that the black-and-white, olive, and red colobus had diverged from one another by the end of the Miocene, and that by the Plio-Pleistocene many of the species lineages were already present. This demonstrates that the initial extant colobus monkey diversification occurred much earlier than previously thought and was likely part of the same adaptive radiation that produced the diverse colobine taxa seen in the African Plio-Pleistocene fossil record. The lack of early members from the modern lineages in fossiliferous deposits suggests that they resided in part in the forests of Central and West Africa, which also currently harbor the highest levels of colobus monkey diversity. These forests should not be ignored in models of Plio-Pleistocene human and nonhuman primate evolution.     

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.     

Phylogenetic Patterns of Extinction Risk in the Eastern Arc Ecosystems,an African Biodiversity Hotspot

There is an urgent need to reduce drastically the rate at which biodiversity is declining worldwide. Phylogenetic methods are increasingly being recognised as providing a useful framework for predicting future losses, and guiding efforts for pre-emptive conservation actions. In this study, we used a reconstructed phylogenetic tree of angiosperm species of the Eastern Arc Mountains – an important African biodiversity hotspot – and described the distribution of extinction risk across taxonomic ranks and phylogeny. We provide evidence for both taxonomic and phylogenetic selectivity in extinction risk. However, we found that selectivity varies with IUCN extinction risk category. Vulnerable species are more closely related than expected by chance, whereas endangered and critically endangered species are not significantly clustered on the phylogeny. We suggest that the general observation for taxonomic and phylogenetic selectivity (i.e. phylogenetic signal, the tendency of closely related species to share similar traits) in extinction risks is therefore largely driven by vulnerable species, and not necessarily the most highly threatened. We also used information on altitudinal distribution and climate to generate a predictive model of at-risk species richness, and found that greater threatened species richness is found at higher altitude, allowing for more informed conservation decision making. Our results indicate that evolutionary history can help predict plant susceptibility to extinction threats in the hyper-diverse but woefully-understudied Eastern Arc Mountains, and illustrate the contribution of phylogenetic approaches in conserving African floristic biodiversity where detailed ecological and evolutionary data are often lacking.