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Response to bitter substances in primates: Roles of diet tendency and weaning age

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.

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Author Note

This research was financially supported by a National Agency for Research (ANR) SAFAPE awarded to S.K. The second and third authors contributed equally to the study. We are grateful to M.S.J., the director of the Ménagerie du Jardin des Plantes, for permission to conduct this study. We thank the ATM 16 (Action Transversale du Museum national d’Histoire naturelle) and the project “JC SAFAPE” of the ANR for funding this research. We greatly thank all primate zookeepers for their help, patience, and advice throughout the study. We are grateful to B. Simmen, M. O. Monneuse, and A. Sjöstrand for their help and valuable discussions during the establishment of the study protocol. Finally, we deeply thank A. C. Gruner, M. Hladik, and A. Sjöstrand for their suggestions and corrections for improving the manuscript.

Author information

Correspondence to Shelly Masi.

Additional information

N. Asselain and L. Robelin contributed equally to this study.

Electronic supplementary materials

Below is the link to the electronic supplementary material.

Adult female of Cercocebus atys lunulatus gaping in response of quinine solution (WMV 1.57 mb)

Adult female of Lophocebus aterrimus displaying tongue protrusion down in responseto PTC solution. (WMV 1.88 mb)

Adult female of Lophocebus aterrimus displaying rhythmic tongue protrusion in response to fruit juice. (WMV 2.74 mb)

Adult male of Cercopithecus neglectus lip smacking in response to fruit juice. (WMV 2.16 mb)

Adult male of Cercocebus chrysogaster grimacing in response to PTC solution. (WMV 3.69 mb)

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Adult female of Cercocebus atys lunulatus gaping in response of quinine solution (WMV 1.57 mb)

SI 2

Adult female of Lophocebus aterrimus displaying tongue protrusion down in responseto PTC solution. (WMV 1.88 mb)

SI 3

Adult female of Lophocebus aterrimus displaying rhythmic tongue protrusion in response to fruit juice. (WMV 2.74 mb)

SI 4

Adult male of Cercopithecus neglectus lip smacking in response to fruit juice. (WMV 2.16 mb)

SI 5

Adult male of Cercocebus chrysogaster grimacing in response to PTC solution. (WMV 3.69 mb)

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Masi, S., Asselain, N., Robelin, L. et al. Response to bitter substances in primates: Roles of diet tendency and weaning age. Cogn Affect Behav Neurosci 13, 916–929 (2013) doi:10.3758/s13415-013-0171-9

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Keywords

  • Flavor perception
  • Bitterness
  • Sweet taste
  • Facial expressions
  • Diet
  • Weaning age
  • Primates