Dissertations, Theses, and Capstone Projects

Date of Degree

2-2025

Document Type

Dissertation

Degree Name

Ph.D.

Program

Anthropology

Advisor

Andrea L. Baden

Committee Members

Jessica M. Rothman

Stephanie B. Levy

James P. Higham

Subject Categories

Biological and Physical Anthropology

Keywords

behavioral ecology, nutritional ecology, metabolism, physiology

Abstract

Nutrition and, increasingly, microbiota are recognized in shaping all aspects of animal behavioral ecology and physiology. Since diet and nutrition shape not only animal physiology but also gut microbiota, and these microbiota serve as suppliers of and competitors to host nutrition, this raises questions of how these complex nutritional and microbial environments synergistically affect animal physiology. Examining this nutrition-gut microbiome-host physiology axis has immense potential to unveil how these intricate relationships contribute to animals’ responses to environmental change at multiple scales. Most of what we know about primate responses to environmental change is based upon studies examining one or few behavioral and/or physiological factors. Moreover, what we know about the gut microbiome’s role is largely based on studies of specialist folivores because of their reliance on microbial fermentation of fibrous foods. Specialist frugivores, however, have been little studied but are also likely to rely upon gut microbiota to facilitate nutrient acquisition, despite their short and simple gastrointestinal tracts. Fruit-specialists are particularly vulnerable to the effects of environmental change, at both seasonal and habitat levels. To better predict how these primates respond to environmental change as well as implemented conservation measures, we need to understand the synergistic effects of multiple drivers of these responses. As such, the nutrition-gut microbiome-host physiology axis warrants further study in primate taxa, particularly in fruit-specialists. Thus, this dissertation integrates behavior, nutrition, gut microbiome, metagenomics, and energetics to examine the responses of a dietary specialist to environmental variation in Madagascar.

In Chapter 1, I briefly review relevant literature on primate nutrition, gut microbiome (GM), metagenomics and metabolomics, and physiology, introduce the nutrition-gut microbiota-host physiology axis approach, and discuss ruffed lemurs as an ideal taxon in which to apply this approach to better understand responses of these integrated systems to environmental variation.

In Chapter 2, I characterize the nutritional strategy of Varecia living in a primary forest habitat. I found this population to show seasonal variation in nutrient balancing, particularly shifts in NPE:AP (nonprotein energy-to-available protein) which varied from 12.6:1 in the fruit-abundant season to 9.6:1 in the fruit-lean season. Overall, they prioritized maintaining a constant AP intake and maximized NPE during times of high fruit-availability, within this constraint. However, seasonal shifts in NPE intakes resulted in significant energy shortfalls during fruit‐lean seasons, which may be important factor in their purported sensitivity to habitat disturbance.

In Chapter 3, using 16S sequencing data, I examine responses of the Varecia GM to variation in climate, diet and nutrient intakes. I found substantial intra- and inter- individual variation in GM composition. Bayesian mixed models revealed that both climate (temperature, rainfall) and nutrition (NDF: fibers, TNC: non-structural carbohydrates) significantly impacted GM alpha diversity, and in addition to fat intake, degree of frugivory and diet diversity, both also drove changes in microbial differential abundances, with changes to each predictor comprising a unique microbial signature. These results indicate that despite its rapid gut transit times, this fruit-specialist maintains a diverse GM which responds dynamically to changes in diet and nutrient intakes.

In Chapter 4, I validate two non-invasive energetic biomarkers, urinary C-peptide (uCP) and urinary total triiodothyronine (uTT3), using captive Varecia at the Duke Lemur Center. I experimentally manipulated the diet of five individuals across a 4‐week period, including a 2-week calorie‐restriction. I successfully measured uCP and uTT3 in frozen urine using commercial enzyme-linked immunosorbent assay kits and found that both biomarkers were excreted at significantly lower concentrations during calorie‐restriction. I successfully recovered positively correlated uCP, but not uTT3, levels from filter paper when compared with frozen control samples. These uCP results allowed for the non-invasive measurement of energetic condition in wild Varecia for Chapters 5 and 6.

In Chapter 5, I examine the behavioral ecology and flexibility of Varecia in response to habitat quality by comparing data collected in primary and secondary forests. I found significant variation in food availability between sites, as well as correlated responses in diet composition and diversity, activity budgets, range use, and group dynamics. While fission-fusion group dynamics were ubiquitous, lemurs in the secondary forest lived in larger, more stable groups, exploited larger home ranges, and traveled shorter daily distances than those in the primary forest, patterns that can be explained by differences in food availability, floristic diversity, and population density. These results demonstrated divergent behavioral strategies in primary and secondary forests, yet these behavioral differences only partially explained the differences in energetic outcomes between the two populations.

In Chapter 6, I take an integrative approach to examine the nutrition-gut microbiome-host physiology axis of Varecia to characterize nutritional and metabolic flexibility in this fruit-specialist in these same two populations. I found that nutrient balancing was remarkably similar across sites, though secondary forest animals consumed fewer calories. The GM was moderately different across sites, with secondary forest animals characterized by lower alpha diversity and differential beta dissimilarity. Though metagenomic functional potential was reduced in the secondary forest animals, Bayesian mixed models revealed that KEGG functional pathway abundances for nutrient metabolism negatively correlated with their respective nutrient intakes. Moreover, energetics outcomes showed limited differences across sites, and variation in energy balance was significantly predicted by KEGG functional pathway abundances. These findings indicate substantial metabolic buffering by the GM. These results demonstrate that metabolic flexibility facilitated by GM plasticity plays a pivotal role in enabling fruit-specialists to maintain energetic status under variable environmental conditions, even in environments characterized by fruit-limitation.

In Chapter 7, I summarize and contextualize the main conclusions of this dissertation and provide suggestions for applications of these results and future directions for research.

Download

Share

COinS