Decoding the Plant Metabolome: A Metabolomics Approach to Guereza (Colobus guereza) Feeding Ecology in Kibale National Park, Uganda

Author

Emma Grace Thurau, CUNY Graduate CenterFollow

Date of Degree

6-2025

Document Type

Doctoral Dissertation

Degree Name

Doctor of Philosophy

Program

Anthropology

Advisor

Jessica Rothman

Committee Members

Damon Little

Ryan Raaum

Brian Sedio

Subject Categories

Behavior and Ethology | Biological and Physical Anthropology | Other Ecology and Evolutionary Biology

Keywords

primates, metabolomics, chemical ecology, primatology

Abstract

Plant metabolites, an elusive and diverse group of plant chemicals, represent a complex chemical interplay between plants and herbivores. Plants contain essential nutrients necessary for herbivore survival, yet herbivore consumption results in negative fitness consequences to a plant. This relationship has triggered a coevolutionary arms race in which plants have evolved chemical defenses to prevent herbivore consumption and herbivores, in response, have evolved their own counter-adaptations. This arms race has led to the diverse numbers of herbivores and plants observed today; therefore, these plant metabolites act as a signature of evolution through their influence on herbivore adaptations. Plant metabolites are particularly influential on primates, as primates inhabit tropical rainforests marked by high amounts of chemical diversity due to the presence of many different species of herbivores. Investigations of plant metabolites can provide insights into how these metabolites have shaped primate evolution.

In this dissertation, I integrated metabolomic and nutritional approaches to investigate the mechanisms by which a leaf-eating colobine can detect metabolites in their habitat and the ways in which these metabolites affect their feeding behavior. This dissertation draws on 120 days of focal follows of four study groups of adult guerezas or black-and-white colobus monkeys (Colobus guereza), along with 36 days of plant collection at the Kanyawara site in Kibale National Park, Uganda. Data were obtained from both nutritional and metabolite analyses of 223 plant samples and color analyses of 73 samples.

I first characterized the relationship between plant color and its metabolome. Plant color (spectral wavelengths representing greenness, redness and blueness) was associated with many metabolite classes with redness exhibiting the strongest relationship, especially for classes of alkaloids and terpenoids. Young leaves other than Celtis gomphophylla exhibited a significant number of metabolites associated with color across all pathways, whereas young leaves of C. gomphophylla and more specifically mature leaves of C. gomphophylla exhibited fewer significant relationships between color and classes of metabolites. Similarly, nutrients, including fiber and protein, were correlated with plant color (as measured as proportion of greenness, redness and blueness). These findings suggest that plant color can act as an important indicator of plant metabolomic makeup particularly in young leaves, and that trichromats such as guerezas may be able to use these indicators to select their foods.

Second, I determined if guereza food selection is related to plant color. I measured selection across three comparisons: young versus mature leaves of C. gomphophylla (between plant parts), young leaves of selected versus avoided C. gomphophylla (within species) and young leaves of selected versus avoided species other than C. gomphophylla (among species). Guerezas appear to be able to biologically distinguish young versus mature leaves of C. gomphophylla, as well distinguish differences within species using color, but not among species, which might be driven by the high variation in colors in the species dataset. These findings offer support for the use of trichromatic vision in the detection of metabolites and nutrients in young versus mature leaves.

Third, I describe the metabolite make-up of foods within guereza habitat and investigate how these metabolites are related to food selection. Leaves within Kibale are characterized by low amounts of primary metabolites (2,610; primarily fatty acids) and high amounts of secondary metabolites (8,324; primarily terpenoids). Guereza food selection was characterized using differential expression, metabolite diversity, and machine-learning approaches. The differential metabolite expression analysis suggests that young and mature leaves exhibit large differences. Young leaves were characterized by greater expression of both the primary and secondary metabolites, such as shikimates and phenylpropanoids. Terpenoids were expressed at higher levels in mature leaves in comparison to young leaves. Within species and among species comparisons, also exhibited differences in differential expression, but to a lesser extent. Young and mature leaves exhibited distinct differences in metabolite diversity, with young leaves generally exhibiting greater primary metabolite diversity, while the secondary metabolite diversity results were more mixed. Metabolite diversity did not appear to differ within species, suggesting that other factors may be important for food selection within species. Among species, selected leaves exhibited lesser polyketide, shikimates and phenylpropanoid, and terpenoid diversity when compared to avoided species. Nutritionally, young leaves were generally more nutritionally dense than mature leaves with young leaves associated with protein and energy and mature leaves with fiber. Generally, guereza among species selection was related to protein selection and fiber avoidance. Regarding C. gomphophylla selection, tannins were negatively related to selection, whereas alkaloids exhibited mixed results. C. gomphophylla exhibited high chemical diversity in both primary and secondary metabolites, meaning they are consuming highly chemically defended but nutritionally dense food, and that nutritional supplementation or adaptation to secondary metabolites may aid them in their consumption.

Guerezas through color vision can detect and select based on the plant metabolites present in their habitat and their selection appears to be driven by both metabolites and nutrients. This dissertation characterized the diet of a widespread colobine species and how diet selection relates to plant chemistry, adding to the large body of literature describing the impact of plant chemistry on primate behavior. This dissertation used new approaches in plant metabolomics integrated with existing methods to further our understanding of how plants have affected the evolution of primate traits in terms of vision and behavior and, therefore, provides a new framework to understand plant chemistry and primate behavior.

Recommended Citation

Thurau, Emma Grace, "Decoding the Plant Metabolome: A Metabolomics Approach to Guereza (Colobus guereza) Feeding Ecology in Kibale National Park, Uganda" (2025). CUNY Academic Works.
https://academicworks.cuny.edu/gc_etds/6283