Fruit scent and observer colour vision shape food-selection strategies in wild capuchin monkeys

Abstract

The senses play critical roles in helping animals evaluate foods, including fruits that can change both in colour and scent during ripening to attract frugivores. Although numerous studies have assessed the impact of colour on fruit selection, comparatively little is known about fruit scent and how olfactory and visual data are integrated during foraging. We combine 25 months of behavioural data on 75 wild, white-faced capuchins (Cebus imitator) with measurements of fruit colours and scents from 18 dietary plant species. We show that frequency of fruit-directed olfactory behaviour is positively correlated with increases in the volume of fruit odours produced during ripening. Monkeys with red-green colour blindness sniffed fruits more often, indicating that increased reliance on olfaction is a behavioural strategy that mitigates decreased capacity to detect red-green colour contrast. These results demonstrate a complex interaction among fruit traits, sensory capacities and foraging strategies, which help explain variation in primate behaviour.

Fig. 1

Variation in fruit sniffing behaviour by white-faced capuchins for 18 plant species. Box plots of fruit investigation sequences (N = 15,160) by individual white-faced capuchin monkeys that included at least 1 sniffing event. Medians (bar) are plotted along with upper and lower quartiles (box perimeters), and whiskers stretching to the first data point within 1.5 interquartile ranges of the box. Points beyond the whiskers are plotted as individual symbols. Source data are provided as a Source Data file. Photo credit for fruit images: AD Melin

Fig. 2

Ripe fruit olfactory conspicuity and monkey sniffing behaviour. a Chemical dissimilarity between conspecific ripe and unripe fruits calculated as Bray–Curtis dissimilarities based on the relative amounts of VOCs. b Scent increase ratio: total amount of scent emitted by an individual ripe fruit divided by the total amount of scent emitted by a conspecific unripe fruit. Each boxplot is overlaid on the raw data, jittered horizontally. Bars over boxes provide significance in a glmm (see Methods). ns, p > 0.05; *p < 0.05. Source data are provided as a Source Data file

Fig. 3

Sniffing behaviour and primate colour vision type plotted with red–green contrast between unripe and ripe fruits. Each dot represents an individual monkey–plant species combination. Data points were binomially classified as to whether that monkey was ever observed sniffing the fruits of that plant species and are vertically and horizontally jittered in each quadrant. Darker red dots represent a larger red–green chromatic contrast between ripe and unripe fruits in the visual space of a trichromatic capuchin monkey. Dichromatic monkeys sniffed fruits significantly more often than trichromatic monkeys did, regardless of red–green contrast, glmm: p < 0.01. Source data are provided as a Source Data file

Fig. 4

Correlation between fruit visual and olfactory changes with ripeness. Scatterplots showing three measures of colour distance between unripe and ripe fruits: a red–green contrast, b yellow–blue contrast, c luminance contrast against the Bray–Curtis chemical dissimilarity index, and against the log scent increase ratio (d–f). (Pearson’s correlation, ripe–unripe chemical dissimilarity: −0.05, 0.07 and 0.17, respectively; scent increase ratio: 0.07, −0.1 and −0.04). Source data are provided as a Source Data file