Maressa Takahashi
Ph.D. 2018
The nutritional ecology of adult female blue monkeys in Kakamega Forest, Kenya
Dissertation abstract
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 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 a
more fruit (by percentage of diet and absolute kcal) when fruit was
more available. In contrast, subjects ate less 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.
Read Maressa's blog: https://projectbluemonkey.wordpress.com/
Publications from the dissertation:
Takahashi, M.Q., Rothman, J., Raubenheimer, D., Cords, M. 2019. Dietary
generalists and nutritional specialists: feeding strategies of adult
female blue monkeys (Cercopithecus mitis) in the Kakamega Forest,
Kenya. Amer. J. Primatol. in press.
After graduation, Maressa relocated to Switzerland, she she works in medical administration.
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