Jessica M. Rothman

Within-species differences in primate social structure: evolution of plasticity and phylogenetic constraints

Primate socioecological studies have attempted to derive general frameworks using the average behavioural traits of species or genera to place them into categories. However, with the accumulation of primate studies, it is timely to place more emphasis on understanding within-species variation in social structure. In this review we have four objectives. First, we examine within-species variation in the potential determinants of social structure, including diet, demography, predation and infanticide, and document considerable variation. Second, we present case studies of within-species variation in social structure to illustrate the potential magnitude of this variation. For example, there are cases within a single interbreeding population where multi-male, uni-male, fission–fusion and monogamous groups are found. Third, by examining widespread primate lineages that occur in a variety of habitats, we note that there are differences in the magnitude of variation in social structures across different lineages and as a result we consider phylogenetic constraints on phenotypic variation in social structure. Finally, we reflect on the implications of extensive variation in social structure. We suggest that primate social structure will represent a combination of adaptation to present-day environment and phylogenetic inertia. To advance our understanding of the relative contribution of phylogeny versus ecology we propose two approaches. One approach is to compare groups in the same interbreeding population that inhabit different ecological conditions. Any differences that are found can be attributed to ecological differences, since phylogeny should not play a role within a single population. The second approach is to study distantly related species that have similar social structures to illustrate how similar ecological pressures might be operating to select for parallel social structures.

Methods in Primate Nutritional Ecology: A User’s Guide

An important goal of primatology is to identify the ecological factors that affect primate abundance, diversity, demography, and social behavior. Understanding the nutritional needs of primates is central to understanding primate ecology because adequate nutrition is a prerequisite for successful reproduction. Here, we review nutritional methods and provide practical guidelines to measure nutrient intake by primates in field settings. We begin with an assessment of how to estimate food intake by primates using behavioral observations. We then describe how to collect, prepare, and preserve food samples. Finally, we suggest appropriate nutritional assays for estimating diet nutritional quality and point to the merits and limitations of each. We hope this review will inspire primatologists to use nutritional ecology to answer many unresolved questions in primatology.

Nutritional quality of gorilla diets: consequences of age, sex, and season

We tested the effects of age, sex, and season on the nutritional strategies of a group of mountain gorillas (Gorilla beringei) in the Bwindi Impenetrable National Park, Uganda. Through observations of food intake of individual gorillas and nutritional analyses of dietary components over different seasons and environments, we estimated nutrient intake and evaluated diet adequacy. Our results suggest that the nutritional costs of reproduction and growth affect nutrient intake; growing juveniles and adult females ate more food and more protein per kilogram of metabolic body mass than did silverbacks. The diets of silverback males, adult females, and juveniles contained similar concentrations of protein, fiber, and sugar, indicating that adult females and juveniles did not select higher protein foods than silverbacks but rather consumed more dry matter to ingest more protein. Juveniles consumed more minerals (Ca, P, Mg, K, Fe, Zn, Mn, Mo) per kilogram of body mass than adult females and silverback males, and juveniles consumed diets with higher concentrations of phosphorous, iron, and zinc, indicating that the foods they ate contained higher concentrations of these minerals. Seasonally, the amount of food consumed on a dry weight basis did not vary, but with increased frugivory, dietary concentrations of protein and fiber decreased and those of water-soluble carbohydrates increased. Energy intake did not change over the year. With the exception of sodium, gorillas ate diets that exceeded human nutrient requirements. A better understanding of the relative importance of food quantity and quality for different age–sex classes provides insights into the ways in which gorillas may be limited by food resources when faced with environmental heterogeneity.

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 populations 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.

Nutritional Ecology of Entomophagy in Humans and Other Primates

Entomophagy is widespread among nonhuman primates and is common among many human communities. However, the extent and patterns of entomophagy vary substantially both in humans and nonhuman primates. Here we synthesize the literature to examine why humans and other primates eat insects and what accounts for the variation in the extent to which they do so. Variation in the availability of insects is clearly important, but less understood is the role of nutrients in entomophagy. We apply a multidimensional analytical approach, the right-angled mixture triangle, to published data on the macronutrient compositions of insects to address this. Results showed that insects eaten by humans spanned a wide range of protein-to-fat ratios but were generally nutrient dense, whereas insects with high protein-to-fat ratios were eaten by nonhuman primates. Although suggestive, our survey exposes a need for additional, standardized, data.

Fecal Bacterial Diversity in a Wild Gorilla

ABSTRACT We describe the bacterial diversity in fecal samples of a wild gorilla by use of a 16S rRNA gene clone library and terminal-restriction fragment length polymorphism (T-RFLP). Clones were classified as Firmicutes, Verrucomicrobia, Actinobacteria, Lentisphaerae, Bacteroidetes, Spirochetes, and Planctomycetes. Our data suggest that fecal populations did not change temporally, as determined by T-RFLP.

Nutritional composition of the diet of the gorilla (Gorilla beringei): a comparison between two montane habitats

The mountain gorilla (Gorilla beringei beringei) lives in two geographically separated populations, Bwindi Impenetrable National Park, Uganda and in three national parks spanning the Virunga mountain region in Rwanda, Democratic Republic of Congo, and Uganda. The altitude, climate and plant composition of these habitats differ. Our goal was to compare the diets of gorillas living in each of these habitats. The nutrients in staple foods and in the diets of individuals in a group of gorillas in Bwindi (N =12 individuals) and a group in the Virungas (N =7 individuals) were compared to determine if differences in dietary composition affected concentrations of nutrients in their diets. At both sites gorilla diets consisted primarily of herbaceous leaves, but the diet of Bwindi gorillas contained more tree leaves, fruit, pith and dry wood, and fewer stems. Despite differences in habitat and dietary composition, the nutrient concentrations in both gorilla diets were remarkably similar. On a dry matter basis, the diets and staple foods of Bwindi and Virunga gorillas contained similar concentrations of crude protein (CP), fibre (NDF) and non-structural carbohydrates (TNC). Bwindi gorillas ate diets containing 18% CP, 43% NDF and 19% TNC on a dry-matter basis, whilethedietsoftheVirungagorillascontained17%CP,41%NDFand18%TNC.Ourresultsdemonstratethatgorillas consume diets that differ by plant species and part, but contain similar concentrations of nutrients. This suggests that classifying animals by broad dietary strategy (e.g. frugivory and folivory) does not provide a reliable indicator of the nutritional quality of their diet, and that our previous assumptions about these categories should be re-evaluated.

Decaying wood is a sodium source for mountain gorillas

Like several other non-human primates, mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda consume decaying wood, an interesting but puzzling behaviour. This wood has little obvious nutritional value; it is low in protein and sugar, and high in lignin compared to other foods. We collected pieces of wood eaten and avoided by gorillas, and other foods consumed by gorillas, and measured their sodium content. Wood was substantially higher in sodium than other dietary items, and wood pieces from stumps eaten contained more sodium than those that were avoided. Wood represented only 3.9% of the wet weight food intake of gorillas, but contributed over 95% of dietary sodium, leading us to conclude that decaying wood is an important sodium source for Bwindi gorillas. Because sodium has been leached from the weathered soils characteristic of the subhumid and humid tropics, and because terrestrial plants generally do not require sodium, tropical herbivores, including gorillas, often encounter problems locating the sodium essential for their well-being. Decaying wood is an unexpected sodium source.

Nutritional contributions of insects to primate diets: implications for primate evolution.

Insects and other invertebrates form a portion of many living and extinct primate diets. We review the nutritional profiles of insects in comparison with other dietary items, and discuss insect nutrients in relation to the nutritional needs of living primates. We find that insects are incorporated into some primate diets as staple foods whereby they are the majority of food intake. They can also be incorporated as complements to other foods in the diet, providing protein in a diet otherwise dominated by gums and/or fruits, or be incorporated as supplements to likely provide an essential nutrient that is not available in the typical diet. During times when they are very abundant, such as in insect outbreaks, insects can serve as replacements to the usual foods eaten by primates. Nutritionally, insects are high in protein and fat compared with typical dietary items like fruit and vegetation. However, insects are small in size and for larger primates (>1 kg) it is usually nutritionally profitable only to consume insects when they are available in large quantities. In small quantities, they may serve to provide important vitamins and fatty acids typically unavailable in primate diets. In a brief analysis, we found that soft-bodied insects are higher in fat though similar in chitin and protein than hard-bodied insects. In the fossil record, primates can be defined as soft- or hard-bodied insect feeders based on dental morphology. The differences in the nutritional composition of insects may have implications for understanding early primate evolution and ecology.

Fiber-Bound Nitrogen in Gorilla Diets: Implications for Estimating Dietary Protein Intake of Primates

Protein is essential for living organisms, but digestibility of crude protein is poorly understood and difficult to predict. Nitrogen is used to estimate protein content because nitrogen is a component of the amino acids that comprise protein, but a substantial portion of the nitrogen in plants may be bound to fiber in an indigestible form. To estimate the amount of crude protein that is unavailable in the diets of mountain gorillas (Gorilla beringei) in Bwindi Impenetrable National Park, Uganda, foods routinely eaten were analyzed to determine the amount of nitrogen bound to the acid‐detergent fiber residue. The amount of fiber‐bound nitrogen varied among plant parts: herbaceous leaves 14.5±8.9% (reported as a percentage of crude protein on a dry matter (DM) basis), tree leaves (16.1±6.7% DM), pith/herbaceous peel (26.2±8.9% DM), fruit (34.7±17.8% DM), bark (43.8±15.6% DM), and decaying wood (85.2±14.6% DM). When crude protein and available protein intake of adult gorillas was estimated over a year, 15.1% of the dietary crude protein was indigestible. These results indicate that the proportion of fiber‐bound protein in primate diets should be considered when estimating protein intake, food selection, and food/habitat quality. Am. J. Primatol. 70:690–694, 2008.