Plant secondary metabolites and primate food choices: A meta‐analysis and future directions

Abstract

The role of plant secondary metabolites (PSMs) in shaping the feeding decisions, habitat suitability, and reproductive success of herbivorous mammals has been a major theme in ecology for decades. Although primatologists were among the first to test these ideas, studies of PSMs in the feeding ecology of non-human primates have lagged in recent years, leading to a recent call for primatologists to reconnect with phytochemists to advance our understanding of the primate nutrition. To further this case, we present a formal meta-analysis of diet choice in response to PSMs based on field studies on wild primates. Our analysis of 155 measurements of primate feeding response to PSMs is drawn from 53 studies across 43 primate species which focussed primarily on the effect of three classes of PSMs tannins, phenolics, and alkaloids. We found a small but significant effect of PSMs on the diet choice of wild primates, which was largely driven by the finding that colobine primates showed a moderate aversion to condensed tannins. Conversely, there was no evidence that PSMs had a significant deterrent effect on food choices of non-colobine primates when all were combined into a single group. Furthermore, within the colobine primates, no other PSMs influenced feeding choices and we found no evidence that foregut anatomy significantly affected food choice with respect to PSMs. We suggest that methodological improvements related to experimental approaches and the adoption of new techniques including metabolomics are needed to advance our understanding of primate diet choice.

Hyper-specialized primates possess a reduced suite of xenobiotic-metabolizing cytochrome P450 genes

“…A lingering question remains as to what compounds, or families of compounds, are leading to the evolutionary expansions and contractions on display in this study. However, there is currently a clear disconnect in the literature that inhibits any discussion between those who have precise knowledge of P450 substrate compounds (e.g., Guengerich 2015) and those who perform phytochemical assays on foods of wild primates (e.g., Eppley et al 2017;Thurau et al 2021;Windley et al 2022). The disconnect arises from differing levels of scale on which each of these two groups operates: pharmacologists often use precise molecules (e.g., benzo[a]pyrene, aflatoxin B1) in their experiments and parlance, while phytochemists and primatologists speak in the more general terms of compound families (e.g., alkaloids, condensed tannins).…”

Plant Diversity in the Diet of Costa Rican Primates in Contrasting Habitats: A Meta-Analysis

“…Second, an eclectic diet can help dilute the potential negative effects of plant secondary metabolites (PSMs) present in many leaves and fruits that NHPs and many other herbivores ingest [96][97][98][99]. Young and mature leaves of important plant species present in the diet of CR-NHPs, such as Samanea saman, Enterolobium ciclocarpum, Spondias mombin, and Bursera simaruba, contain a variable amount of condensed tannins and phenols throughout the year [100].…”

Go for Lipids! Food Preferences and Nutrient Composition in Zoo-Housed White-Faced Sakis, Pithecia pithecia

“…However, numerous studies demonstrate that animals do not choose their food randomly, but instead are highly selective feeders in order to maximize their intake of critical nutrients (e.g., Chivers, 1998;Ganzhorn et al, 2017;Illius & Gordon, 1990;Raubenheimer & Rothman, 2013). It is commonly agreed that the food choices of primates and other mammals are primarily determined by the nutritional and/ or toxic content of a specific plant or animal (Barton & Whiten, 1994;Windley et al, 2022) as well as by its relative temporal and spatial availability (Leighton, 1993;Trapanese et al, 2019). High concentrations of plant secondary compounds such as tannins, phenolics, or alkaloids which inhibit the digestion of proteins and polysaccharides or are even toxic, are sometimes avoided and, accordingly, correlate negatively with food choices in primates (Belovsky & Schmitz, 1994;Glander, 1982;Windley et al, 2022).…”

“…It is commonly agreed that the food choices of primates and other mammals are primarily determined by the nutritional and/ or toxic content of a specific plant or animal (Barton & Whiten, 1994;Windley et al, 2022) as well as by its relative temporal and spatial availability (Leighton, 1993;Trapanese et al, 2019). High concentrations of plant secondary compounds such as tannins, phenolics, or alkaloids which inhibit the digestion of proteins and polysaccharides or are even toxic, are sometimes avoided and, accordingly, correlate negatively with food choices in primates (Belovsky & Schmitz, 1994;Glander, 1982;Windley et al, 2022). High concentrations of nutritionally valuable compounds such as carbohydrates, proteins, and lipids which provide metabolic energy, or of certain critical minerals or vitamins, in contrast, should be expected to correlate positively with food choice (Lambert & Rothman, 2015;Simpson et al, 2004).…”