Wild Bornean orangutans experience muscle catabolism during episodes of fruit scarcity

Caitlin A O’Connell,Daniel J Naumenko,Rebecca S A Brittain,Sri Suci Utami Atmoko,Erin R Vogel,Andrea L Digiorgio,Alexa D Ugarte

doi:10.1038/s41598-021-89186-4

Abstract

Pronounced temporal and spatial variation in the availability of food resources can produce energetic deficits in organisms. Fruit-dependent Bornean orangutans face extreme variation in fruit availability and experience negative energy and protein balance during episodes of fruit scarcity. We evaluate the possibility that orangutans of different sexes and ages catabolize muscle tissue when the availability of fruit is low. We assess variation in muscle mass by examining the relationship between urinary creatinine and specific gravity and use the residuals as a non-invasive measure of estimated lean body mass (ELBM). Despite orangutans having a suite of adaptations to buffer them from fruit scarcity and associated caloric deficits, ELBM was lower during low fruit periods in all age-sex classes. As predicted, adult male orangutans had higher ELBM than adult females and immatures. Contrary to expectation, flanged and unflanged males did not differ significantly in ELBM. These findings highlight the precarity of orangutan health in the face of rapid environmental change and add to a growing body of evidence that orangutans are characterized by unique metabolic traits shaped by their unpredictable forest environment.

Highlights

Pronounced temporal and spatial variation in the availability of food resources can produce energetic deficits in organisms
To detect changes in muscle mass, we measured the concentration of creatinine and the specific gravity of each urine sample
Episodes of fruit scarcity were associated with lower estimated lean body mass (ELBM) ( F(5.094) = 13.6, p < 0.001); this lower estimated muscle mass measured during periods of fruit scarcity was consistent across all age-sex classes (Figs. 1, 2)

Summary

Introduction

Pronounced temporal and spatial variation in the availability of food resources can produce energetic deficits in organisms. Orangutans display a notable tendency to become obese[15–17], and it has been argued that a propensity for storing fat during periods of fruit abundance which is catabolized during lean periods sets orangutans apart from the other great apes[18] Despite this suite of adaptations to their challenging environment, low fruit periods are associated with declining ovarian hormone production, lower conception rates[18,19], negative energy balance20, ketosis[9], and negative protein balance[21,22] in orangutans. Previous research has indicated that prolonged periods of low fruit availability on Borneo are associated with increased levels of δ15N in orangutan urine, indicating that somatic catabolism, or tissue wasting, was beginning to occur[22] Despite their enhanced tendency for fat storage[15–18,23], orangutan fat reserves may not be sufficient and instead they may catabolize functional body tissues for energy. The variation in creatinine that is unexplained by the variation in specific gravity represents an estimate of lean body mass[25,26]

Methods

Results

Conclusion