Academic journal article Cognitive, Affective and Behavioral Neuroscience

Response to Bitter Substances in Primates: Roles of Diet Tendency and Weaning Age

Academic journal article Cognitive, Affective and Behavioral Neuroscience

Response to Bitter Substances in Primates: Roles of Diet Tendency and Weaning Age

Article excerpt

Published online: 28 May 2013

© Psychonomic Society, Inc. 2013

Abstract In primates, the perception of bitter taste may be an essential mechanism for avoiding the ingestion of bitter, and often toxic, substances. Bitterness sensitivity varies across the different primate species and, for bitter thioure substances (e.g., phenylthiocarbamide-PTC), within species. Primates respond to bitterness by displaying aversive affective reactions, and whether these serve for conspecifics as information on the taste of food is still unclear. The aim of this study was to investigate the response to two bitter substances (quinine and PTC) in 11 primate species (N = 29 individuals) hosted at the Ménagerie du Jardin des Plantes, in relation to their main diet tendency and weaning age. We tested primate reactions to bitterness with a two-bottle method. The study individuals showed a strong aversion to bitter taste, minimizing consumption of both bitter solutions. All of the individuals were PTC-taster phenotypes, but the degrees of sensitivity to PTC varied among the individuals. Across-species comparisons revealed that whereas the degree of frugivory of the species had a negative effect on the consumption of bitter solutions by the individuals, a later weaning age seems to be a better predictor for the occurrence of aversive affective reactions. Although the low sample size does not allow for excluding interindividual variability, our results support the hypothesis that affective reactions to bitterness may be trustworthy information for conspecifics during the learning process. Thus, the evolution of the appropriate perceiver systems to convert affective displays into true affective signals could be a shared trait among human and nonhuman primates.

Keywords Flavor perception . Bitterness . Sweet taste . Facial expressions . Diet .Weaning age . Primates

Introduction

Flavor perception is one of the most important sensory attributes that leads to animal food choices (Simmen & Hladik, 1998). The perception of the global flavor of food is a complex buildup of gustatory signals designated by the synergic effect of the perception of the biophysical taste by chemoreceptors and of the olfactory, tactile, visual, and thermal perceptions that trigger the neural trigeminal pathways (Hladik & Simmen, 1996). Consumption and appreciation of food are then elaborated at the brain level by the convergence of such gustative signals and by the psychosensory responses of the limbic system (Holley, 2006). In addition to the five main tastes traditionally described in humans (i.e., sweet, bitter, salty, acid, and umami), it is still debated whether animals, including humans, can perceive a gustative continuum of flavors that can be embedded within only these main categories (Pasquet, Hladik, & Tarnaud, 2011).

Perception of bitter substances

Coevolution between plants and their predators has shaped the evolution of flavor perception in animals, including humans (Hladik, 1993; Hladik & Simmen, 1996). Plants developed poisonous secondary metabolites that to humans often have bitter (e.g., alkaloids) or astringent (e.g., tannins) tastes, deterring herbivores from their consumption (Gilles et al., 2006). The ability of mammals to detect even traces of such substances in food allows for the regulation of toxin ingestion and the avoidance of poisoning, conferring important survival advantages throughout evolution (Glendinning, 1994; Steiner & Glaser, 1984). Food neophobia (unwillingness to ingest unfamiliar foods) is a behavioral response that generally prevents the ingestion of large amounts of novel food,minimizing the danger of plant toxicity (e.g., Agostini & Visalberghi, 2005). In humans, food neophobia correlates positively with the perception and sensitivity of taste (Anliker, Bartoshuk, Ferris, & Hooks, 1991). Given the essential role of perception of toxic substances for animal survival, primates show strong aversion to bitterness and astringency from the first days of their lives (Sclafani, 1995; Tepper et al. …

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