Theses Doctoral

The Nutritional Ecology of Adult Female Blue Monkeys, Cercopithecus mitis, in the Kakamega Forest, Kenya

Takahashi, Maressa

The search for food and adequate nutrition determines much of an animal's behavior, as it must ingest the macronutrients, micronutrients, and water needed for growth, reproduction and body maintenance. These macro- and micronutrients are found in varying proportions and concentrations in different foods. A generalist consumer, such as many primates, faces the challenge of choosing the right combination of foods that confers adequate and balanced nutrition. Diet selection is further complicated and constrained by antifeedants, as well as digestive morphology and physiological limitations. Nutritional ecology is the study of the connected relationships between an organism, its nutrient needs (determined by physiological state), its diet selection, and the foraging behavior it uses within a specific food environment. Additionally, these relationships are complex and changeable since the nutrient needs of a consumer change over time and food resources (including the nutritional composition) vary spatiotemporally. Published data on primate nutritional ecology are limited, with most investigations of nutritional needs stemming from captive populations and few field studies. To contribute to the body of knowledge of nutritional ecology in natural populations, I examined the nutritional ecology of wild adult female blue monkeys, Cercopithecus mitis. I used the geometric framework (GF) to quantify nutritional patterns, as it allows simultaneous examination of multiple nutrients that may be driving foraging behavior and patterns of food intake.
Blue monkeys are known to be generalist feeders, with flexible feeding behavior. The population I studied inhabits the Kakamega Forest, western Kenya. This forest has a history of variable human modification on a small scale, and offered a unique opportunity to examine environmental factors (e.g. degree of human-modification of forest type, food availability), social factors (dominance rank), and physiological factors (reproductive demand) that may alter blue monkey nutritional strategies.
From January and September 2015, a team of field assistants and I collected behavioral data from 3 study groups, intensively sampling 24 adult females that varied in dominance rank and reproductive condition. I used all-day focal follows to quantify feeding behavior, which allowed me to assess diet selection and nutrient intake on a daily basis. I also monitored subjects' daily movement. To assess food availability, I quantified vegetative differences among major habitat types within each group's home range and monitored biweekly changes in plant production of fruits and young leaves, which were major constituents of the plant-based diet. I collected >300 food samples, as well as fecal samples, and analyzed them for macro-nutritional content using wet chemistry and near-infrared spectroscopy techniques. I combined data to examine patterns in diet and nutritional strategy on different scales: patterns across subjects, between groups and within the population as a whole, patterns in the diet on the food composition level versus nutrient intake level, and patterns in nutrient intake on a daily basis versus a long term basis (i.e. over the course of the study period). Additionally, I evaluated factors that might affect variation in nutritional strategies, including a female's reproductive condition, dominance rank, habitat use, and degree of frugivory or folivory in daily intake, as well as food availability in the environment.
Kakamega blue monkeys ate a broad diet of over 445 food items (species-specific plant parts and insect morphotypes). Fruit was preferred food, and particular species-specific fruits constituted the majority of important food items (i.e., those contributing >1% of total caloric intake by group); many fruits were highly selected (i.e. eaten more than expected based on availability). Many species-specific young leaves also were important food items, though they were eaten in proportion to their availability, or even less often. Regardless of whether group diet was characterized by time spent feeding or by calories, fruit remained the largest constituent and young leaves the second largest. A subject's daily path length was negatively related to proportion of fruit in the diet (by kcal) because females focused feeding in particular trees when important fruits ripened and thus traveled less. Daily path length was not related to group size, probably because females spread out when foraging to avoid within-group scramble competition over food. Group differences in the food composition of diets likely reflected habitat differences in food distribution. Comparison of the population's diet to data from previous studies showed that as study groups moved into new areas and habitats, they capitalized on new food resources, reinforcing the idea that blue monkey are flexible feeders. During this study, subjects adjusted their diet in response to food availability in the environment, consuming more fruit (by percentage of diet and absolute kcal) when fruit was more available. In contrast, subjects ate fewer young leaves (by absolute kcal) when either fruit or young leaves were more available, suggesting that young leaves served as fallback food. At the level of nutrient intake, it was also true that females consumed significantly more structural carbohydrates when fruit availability was low. Despite their diverse diets and changes related to food availability, females actively regulated food intake to converge daily on a similar nutrient intake (grand mean of 637 kcal, with 108 kcal from protein, 149 kcal from lipid, 88 kcal from structural carbohydrates, and 293 kcal from non-structural carbohydrates, N=24). Thus, considering a multidimensional nutritional niche, I characterized their feeding behavior at two levels: they were both food composition generalists and nutrient intake specialists.
Blue monkeys showed a nutritional strategy on two different temporal scales: 1) daily protein prioritization and 2) long term non-protein energy (NPE; i.e. lipid + carbohydrate energy) to available protein (P) balancing. On a daily basis, protein intake (by kcal) showed the least amount of variation (by coefficient of variation) and subjects consumed similar amounts of protein, regardless of potential influences from environmental, social or physiological factors. Females allowed more variation in daily ratio of non-protein energy to protein (NPE:P), taking advantage of high NPE foods like fruit. They allowed higher NPE:P ratios when fruit was a larger proportion of their diet and when they spent less time in near-natural forest. There was no evidence that reproductive demand or dominance rank affected protein intake or NPE:P balance. Dominance rank also did not predict deviation (absolute or directional) from mean protein intake or mean NPE:P ratio. On a long term basis (i.e. over the 8 months of data collection), all subjects tightly balanced cumulative NPE:P intake, regardless of dominance rank. This long-term pattern in all 24 subjects suggests that it a species-typical strategy. However, lower ranking females ate more unique food items per day than higher ranking females. Varying daily dietary breadth may allow females to cope with social constraints while feeding, such that dominance rank had no effect on nutritional strategies. Further, the prevalence of NPE:P balancing in most nutritional ecology studies of primates suggests that the diversity of feeding strategies within this order of mammals may have evolved to allow them to adhere to that particular nutrient balance, though the rule of compromise (e.g. protein versus NPE prioritization) and the exact ratio balanced may differ by population or species.
Blue monkeys regularly used human-modified habitats and ate considerable amounts of the non-natural foods found there (and elsewhere in the forest). Non-natural foods were directly derived from humans or human activity (e.g. via scavenging from trash) and exotic (non-native) plants, generally introduced inadvertently or for silviculture. Subjects incorporated a substantial amount of non-natural foods into their diets, with approximately a third of their daily calories derived from non-natural foods. Subjects in the group with the most access to human-modified habitat used non-natural foods the most extensively. Further, subjects in two groups showed clear preference for human-modified habitat while members of the third group used habitat types in proportion to their occurrence in the home range. Human-modified habitat, and the non-natural foods found within, may have been readily used because many non-natural foods provided similar access to nutritional space as natural foods. Some non-natural foods, like oil palm fruit and ugali (cooked maize flour), represented energetically dense food resources, which also proved attractive. Regardless of whether subjects fed primarily on natural or non-natural foods, they consumed similar amounts of daily protein. This prioritization of protein, coupled with the fact that females had higher NPE:P ratios when feeding mostly on non-natural foods, indicated that blue monkeys capitalized on non-natural resources to increase NPE intake as long as they were able to consume a threshold amount of protein. What remains unclear though, is whether there are adaptive advantages associated with the ability to consume diets of variable NPE:P ratios.
Overall, blue monkeys in Kakamega Forest are very flexible feeders, perhaps to a greater degree than previously acknowledged. Subjects were able to consume a diverse diet of hundreds of species-specific food items, to shift their diet in response to changes in food availability, to capitalize on food resources found in different habitat types, to take advantage of non-natural food resources, and to tolerate a wide range of NPE:P ratios in daily diets. Further, on a nutritional level, they successfully navigated potential stressors from the physiological demands of reproduction and dominance rank to adhere to a particular nutritional strategy. Flexible behavior, such as spreading out during feeding or varying dietary breadth, indicates how blue monkeys may use particular feeding strategies to arrive at a common nutrient intake target. Despite daily fluctuations in NPE:P ratio that varied with environmental and dietary factors, all subjects were able to consume a consistent daily amount of protein and prioritized its intake above all other nutritional components. Finally, their tight adherence to long term NPE:P balancing suggested that they followed a nutritional strategy that operated on both daily and longer timescales.
Primates are increasingly threatened from habitat loss, degradation and other human-disturbances. There is growing awareness that some species, like blue monkeys, may be able to persist in regenerating human-modified landscapes, where they regularly and readily use non-natural food resources. More species- and habitat-specific nutritional studies are needed to predict population-level responses to varying degrees of habitat alteration. The data generated may help us assess the potential value of human-modified habitats that may require protection, as these habitats may contribute to the persistence of primate populations around the globe, especially in novel ecosystems.


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More About This Work

Academic Units
Ecology, Evolution, and Environmental Biology
Thesis Advisors
Cords, Marina
Ph.D., Columbia University
Published Here
April 13, 2018