Primate population dynamics in Ngogo, Kibale National Park, Uganda, over nearly five decades.

Many anthropogenic-driven changes, such as hunting, have clear and immediate negative impacts on wild primate populations, but others, like climate change, may take generations to become evident. Thus, informed conservation plans will require decades of population monitoring. Here, we expand the duration of monitoring of the diurnal primates at Ngogo in Kibale National Park, Uganda, from 32.9 to 47 years. Over the 3531 censuses that covered 15,340 km, we encountered 2767 primate groups. Correlation analyses using blocks of 25 census walks indicate that encounters with groups of black and white colobus, blue monkeys, and baboons neither increased nor decreased significantly over time, while encounters with groups of redtail monkeys and chimpanzees marginally increased. Encounters with mangabeys and L'Hoesti monkeys increased significantly, while red colobus encounters dramatically decreased. Detailed studies of specific groups at Ngogo document changes in abundances that were not always well represented in the censuses because these groups expanded into areas away from the transect, such as nearby regenerating forest. For example, the chimpanzee population increased steadily over the last 2 + decades but this increase is not revealed by our census data because the chimpanzees expanded, mainly to the west of the transect. This highlights that extrapolating population trends to large areas based on censuses at single locations should be done with extreme caution, as forests change over time and space, and primates adapt to these changes in several ways.

The life of a naturalist.

This essay summarizes some of my findings while studying primates in the field from 1962 to 2018. Although I have studied primates throughout the tropics, I focused on Africa, primarily the Kibale Forest of Uganda. My research began in the early days of primate field studies when very little was known about the behavior and ecology of most species. Consequently, I was able to study nearly anything that could be observed under natural conditions. It was not necessary to specialize, and I opted to be a generalist. In much of my work I have attempted to understand the relationships between habitat quality, social organization, and population dynamics, emphasizing the great intraspecific variability that exists over time and between areas. Vocalizations have also long been of interest to me, starting with a description of predator-specific alarm calls and later showing how vocalizations among African monkeys appear to be evolutionarily stable. As my field experience progressed, I became increasingly involved with the conservation of tropical rain forests. In the last part of this essay I offer my thoughts on current trends in field primatology and some advice to the next generation of field biologists, stressing the importance of being a naturalist.

Facial and genital lesions in baboons (Papio anubis) of Kibale National Park, Uganda.

We describe and document with digital images two adult male baboons (Papio anubis) from the Kibale National Park, Uganda who were infected with some kind of disease having clinical signs suggestive of Treponema pallidum. One of these males was missing his premaxilla, part of the maxilla, upper incisors, canines, and possibly the first premolars. The condition of his scrotum was not seen. The other adult male had prominent inflammation of his scrotum and, to a lesser extent, his penis. Otherwise, both males appeared normal and healthy and were apparently well integrated into the same social group. These observations suggest that an earlier report of an adult female baboon living in the same area who was missing her entire premaxilla and nose and most of her maxilla may have been suffering from a similar infection, rather than a congenital disorder, as previously speculated. If these lesions were due to T. pallidum infections, then this disease has a greater geographical distribution among non-human primates than previously known.

Long-term declines in nutritional quality of tropical leaves.

Global change is affecting plant and animal populations and many of the changes are likely subtle and difficult to detect. Based on greenhouse experiments, changes in temperature and rainfall, along with elevated CO2, are expected to impact the nutritional quality of leaves. Here, we show a decline in the quality of tree leaves 15 and 30 years after two previous studies in an undisturbed area of tropical forest in Kibale National Park, Uganda. After 30 years in a sample of multiple individuals of ten tree species, the mature leaves of all but one species increased in fiber concentrations, with a mean increase of 10%; tagged individuals of one species increased 13% in fiber. After 15 years, in eight tree species the fiber of young leaves increased 15%, and protein decreased 6%. Like many folivores, Kibale colobus monkeys select leaves with a high protein-to-fiber ratio, so for these folivores declining leaf quality could have a major impact. Comparisons among African and Asian forests show a strong correlation between colobine biomass and the protein-to-fiber ratio of the mature leaves from common tree species. Although this model, predicts a 31% decline in monkey abundance for Kibale, we have not yet seen these declines.

Healthy baboon with no upper jaw or nose: an extreme case of adaptability in the Kibale National Park, Uganda.

We describe and document with digital images an adult female baboon (Papio anubis) from the Kibale National Park, Uganda, who was missing all but the basal part of her upper jaw and nose, i.e., no premaxilla and very little of the maxilla and nasal bones. She appeared otherwise healthy, well integrated into a social group, and apparently reproducing, based on the fact that she was grooming a juvenile who suckled from her and that she appeared to be pregnant. Her extreme deformity raises numerous questions and demonstrates the highly adaptable capabilities of wild baboons.

Understanding long-term primate community dynamics: implications of forest change.

Understanding the causes of population declines often involves comprehending a complex set of interactions linking environmental and biotic changes, which in combination overwhelm a population's ability to persist. To understand these relationships, especially for long-lived large mammals, long-term data are required, but rarely available. Here we use 26-36 years of population and habitat data to determine the potential causes of group density changes for five species of primates in Kibale National Park, Uganda, in areas that were disturbed to varying intensities in the late 1960s. We calculated group density from line transect data and quantified changes in habitat structure (cumulative diameter at breast height [dbh] and food availability [cumulative dbh of food trees]) for each primate species, and for one species, we evaluated change in food nutritional quality. We found that mangabeys and black-and-white colobus group density increased, blue monkeys declined, and redtails and red colobus were stable in all areas. For blue monkeys and mangabeys, there were no significant changes in food availability over time, yet their group density changed. For redtails, neither group density measures nor food availability changed over time. For black-and-white colobus, a decrease in food availability over time in the unlogged forest surprisingly coincided with an increase in group density. Finally, while red colobus food availability and quality increased over time in the heavily logged area, their group density was stable in all areas. We suggest that these populations are in nonequilibrium states. If such states occur frequently, it suggests that large protected areas will be required to protect species so that declines in some areas can be compensated for by increases in adjacent areas with different histories.

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.