Joanna E. Lambert

Primate digestion: Interactions among anatomy, physiology, and feeding ecology

Food is vital for life. It provides nutrients for growth, maintenance, and reproduction, and is the source of energy that drives the chemical reactions occurring in every cell.1,2 However, most food, as it is initially procured, is not in a form suitable for use; it must first be broken down so that it can be transported through cell membranes.1 The breaking down of food molecules via a system of both mechanical and chemical processes so that they are of use to the body is called digestion.2,3

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. Am. J. Primatol. 50:169–185, 2000.

Seed handling in chimpanzees (Pan troglodytes) and redtail monkeys (Cercopithecus ascanius): Implications for understanding hominoid and cercopithecine fruit-processing strategies and seed dispersal

Primates are confronted with an array of constraints in feeding on fruit, including the removal of adhesive, energy-rich pulp from seeds. In this paper, I discuss how primates meet this challenge and present data on the fruit-processing and seed-handling behavior of chimpanzees and redtail monkeys in Kibale National Park, Uganda. These data are then related to these species services as seed dispersers. Particular attention was paid to the methods by which primates removed pulp from seeds, the density of seed clumps that they deposited (by spitting, dropping, or defecating) to the forest floor, and the distance seeds were moved from parent trees. Distance and density differences in chimpanzee and redtail seed dispersal resulted from distinct fruit-processing and seed-handling methods. It was observed, in general, that redtail monkeys engaged in fine oral processing and were seed spitters: most seeds were dispersed in close proximity to parent trees (84% of spat seeds < 10 m of parent tree), and deposited singly (100% seeds spat singly). In contrast, chimpanzees were coarse fruit processors and seed swallowers: seeds were defecated in denser clumps (e.g., a mean of 149 large seeds/dung sample and hundreds of small seeds/dung sample), far from parent trees. I evaluate the factors that shape patterns of fruit processing in hominoids and cercopithecines, and argue that the observed seed handling differences can be attributed to differences in digestive retention times, oral anatomy, and alternative mechanisms by which to avoid the cost of seed ballast.

Impending extinction crisis of the world's primates: why primates matter

Impending extinction of the world’s primates due to human activities; immediate global attention is needed to reverse the trend. Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cultures, and religions of many societies and offer unique insights into human evolution, biology, behavior, and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats—mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture, large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the world’s primates and the costs of their loss to ecosystem health and human society is imperative.

Variation in the Diets of Cercopithecus Species: Differences within Forests, among Forests, and across Species

Dietary data have been used to address numerous theoretical issues, yet we have little understanding of dietary flexibility in primates. Previous comparative research has either explicitly or implicitly assumed that the closer the phylogenetic proximity between two taxa, or the spatial proximity between two populations of the same taxon, the more similar their diets will be. We examine such assumptions by making dietary comparisons among arboreal Cercopithecus species at the intergroup, interdemic, interpopulational, and interspecific levels. Our analyses reveal considerable variation and sometimes the magnitude of the variation of particular contrasts is unexpected. We conclude that dietary flexibility blurs our traditional trophic assessment of primate species. Thus, a study of the diet of a single group, in a specific habitat, at one point in time may not be representative of the species as a whole. This flexibility suggests that a profitable avenue of future research is quantifying the degree of flexibility that different primate lineages have in their digestive strategies.

Thirty years of research in Kibale National Park, Uganda, reveals a complex picture for conservation

Kibale National Park, Uganda, has a rich and abundant primate community and a complicated history of anthropogenic disturbance. Moreover, it has been the focus of over 30 yr of research and has received considerable attention from nongovernmental and governmental conservation organizations. As a result, Kibale serves as a valuable case study with which to evaluate the factors that regulate primate population density and the challenges of deriving generalizations for conservation. We review the impact of logging and forest fragmentation on primate population density and trace the efficacy of various conservation strategies. A 28-yr comparison of primate abundance in logged and unlogged forests and a 10-yr study of forest dynamics showed that primate recovery in logged areas is generally slow or not occurring at all for some species, which is likely driven by the fact that the forest is not recovering as expected. No primate species characteristic predicted their ability to live in forest fragments around Kibale. While a nutritional model was useful to predict the abundance of colobus in forest fragments outside of Kibale, a 5-yr study revealed that human land-use practices are more fundamentally shaping population dynamics. We evaluate data on primate abundance in light of Milton’s protein/fiber model to predict colobine biomass. We demonstrate that while the model can predict colobus biomass in pristine habitats, the 2 colobus species respond differently to disturbance. We offer suggestions for future conservation research and consider strategies to conserve forested national parks based on experiences gained over 30 yr.

Red-Tailed Guenons (Cercopithecus ascanius) and Strychnos mitis: Evidence for Plant Benefits Beyond Seed Dispersal

I report data collected on red-tailed guenon (Cercopithecus ascanius schmidti) fruit processing behaviors between June 1993 and April 1994. Red-tailed guenons consumed the fruit of Strychnos mitis in 542 of 2,930 fruit-eating events (FEEs). The monkeys spat out cleaned seeds of Strychnos mitis in a majority of these records (477/542; 88%); seeds were occasionally swallowed whole, but only when pulp was unripe (69/542; 12%). In 83% of the FEEs on Strychnos, the red-tailed guenons spat out seeds within 10 m of the removal site; they typically stayed in the same tree while processing fruit, and in 56% of the FEEs, they moved <1 m before spitting seeds. I monitored spat seeds to evaluate the impact of monkey fruit processing on seed fate. Results indicate that 83% of seeds spat out by the red-tailed guenons germinated, while only 12% of unprocessed seeds survived to germination (p < 0.01). Of the processed seeds that germinated, 60% survived to germination and seedling establishment, while only 5% of unprocessed seeds survived to seedling establishment (p < 0.01). Unprocessed seeds were also more likely to be attacked by seed predators (p < 0.01) and fungus (p < 0.01). Although there is generally high mortality in seeds/seedlings, mature trees of Strychnos mitis are found in groves of adults, under which dense populations of seedlings and saplings can occur. These data suggest that Strychnos mitis does not conform to expectations of the Janzen-Connell model of seed escape from parent trees. Instead, I suggest that by removing pulp, a process that results in a reduction of fungal pathogen attack, red-tailed guenons positively effect the seed survivorship of Strychnos mitis. Although this effect has been observed in pulp-cleaning ant species, it is a hitherto undescribed effect of primates on their fruit resources.

Digestive Retention Times in Forest Guenons (Cercopithecus spp.) with Reference to Chimpanzees (Pan troglodytes)

Because the length of time food is maintained in the gut influences fermentation rates and its overall digestibility, information on digestive passage rates is critical to explain the overall feeding and foraging strategy of a species. I present results from digestive passage experiments conducted on captive Cercopithecus ascanius, C. mitis, C. neglectus, Miopithecus talapoin, and Pan troglodytes. I recorded several measures of digestive passage time, including transit time (time of first marker appearance; TT), mean retention time of markers (MRT), and time of last appearance of a marker (TLA). I conducted 4 trials on each of the 10 subjects. A trial consists of the administration of 20, non-toxic colored plastic markers. Overall, the 5 species varied in digestive times (p < 0.01), but there is no difference between Cercopithecus neglectus and Pan troglodytes (p = 0.131) or between C. mitis and C. ascanius (p = 0.661). When the effect of body size is removed (by computing the ratio y/x, where x = body mass, and y = MRT), Pan troglodytes exhibits a low ratio, suggesting relatively slow retention times in the 4 cercopithecines. My findings and other published digestive passage rates suggest that lengthy digestive retention times may be characteristic of cercopithecines. These data may help to interpret how the smaller-bodied guenons are able to consume a higher percentage of fiber than that of chimpanzees, a specialized frugivore. Small body size, in combination with long digestive passage times may be an adaptation on the part of Cercopithecus species to consume a high fiber diet, while maintaining a greater capacity to detoxify secondary metabolites.

Primate and Dung Beetle Communities in Secondary Growth Rain Forests: Implications for Conservation of Seed Dispersal Systems

Conservation efforts are often aimed at one or a few species. However, habitat sustainability relies on ecological interactions among species, such as seed dispersal. Thus, a community-scale conservation strategy may be more valuable in some settings. We describe communities of primary (primates) and secondary (dung beetles) seed dispersers from 5 sites in the Brazilian Amazon. We estimate community biomass of these taxa and, using multivariate ordination, examine the potential for natural reforestation at each site, given the communities of seed dispersers present. Since disturbed habitat is increasingly common and increasingly the focus of conservation efforts, we also examine differences among seed disperser communities between primary forest and secondary growth at each site. Analyses of faunal biomass in different localities and habitats indicate that secondary growth receives nearly as much use by primates as primary forest; given the dominant groups of dung beetles in secondary growth, disturbed habitat should show a pattern of seed burial that is clumped and deep. Areas with high biomass of Alouatta spp. and the large nocturnal dung beetle species may have the greatest potential for natural reforestation of secondary growth particularly for large seeded species. The data suggest that knowledge of the biomass of primary and secondary dispersing fauna facilitates predictions for the likelihood of disturbed habitat to regenerate and comparisons of sites in broader geographical areas e.g., Neotropical vs. Paleotropical forests.

The evolution of stomach acidity and its relevance to the human microbiome

Gastric acidity is likely a key factor shaping the diversity and composition of microbial communities found in the vertebrate gut. We conducted a systematic review to test the hypothesis that a key role of the vertebrate stomach is to maintain the gut microbial community by filtering out novel microbial taxa before they pass into the intestines. We propose that species feeding either on carrion or on organisms that are close phylogenetic relatives should require the most restrictive filter (measured as high stomach acidity) as protection from foreign microbes. Conversely, species feeding on a lower trophic level or on food that is distantly related to them (e.g. herbivores) should require the least restrictive filter, as the risk of pathogen exposure is lower. Comparisons of stomach acidity across trophic groups in mammal and bird taxa show that scavengers and carnivores have significantly higher stomach acidities compared to herbivores or carnivores feeding on phylogenetically distant prey such as insects or fish. In addition, we find when stomach acidity varies within species either naturally (with age) or in treatments such as bariatric surgery, the effects on gut bacterial pathogens and communities are in line with our hypothesis that the stomach acts as an ecological filter. Together these results highlight the importance of including measurements of gastric pH when investigating gut microbial dynamics within and across species.