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It is not well understood how primates combine olfactory and visual cues in their natural behaviour, especially during feeding. In this study we conducted field observations of a group of wild, frugivorous black-handed spider monkeys, Ateles geoffroyi (Platyrrhini), consisting of both dichromats (N = 11) and trichromats (N = 9) in Santa Rosa National Park, Costa Rica. We focused on the fruit foraging behaviour, for which involvement of vision has been well studied. We examined how often the monkeys inspected fruits by sniffing them during their fruit feeding attempts (i.e. sniffing index). We found that both dichromats and trichromats sniffed the visually cryptic fruit species more often than the conspicuous species, with the sniffing index being negatively correlated with the luminance and blue–yellow contrasts of fruits to background leaves. Furthermore, the sniffing index was negatively correlated with the proportion of fruits eaten (versus rejected) following a foraging attempt in both dichromats and trichromats. These results suggest that monkeys use olfaction for discrimination between edible and inedible fruits when vision alone is insufficient to evaluate the quality of fruits, showing the first documentation of interplay between vision and olfaction in primate feeding behaviour under natural conditions.

Unlike most eutherian mammals, which have dichromatic (two-colour) vision, most platyrrhine primate species have polymorphic colour vision. This unique characteristic is enabled via multiple alleles for a midto long-wavelength-sensitive (M/LWS), single-locus opsin gene on the X chromosome. In combination with the autosomal opsin common to most vertebrates, this arrangement provides heterozygous females with trichromatic (three-colour) vision, whereas homozygous females and males are dichromats. Trichromatic vision enables visual differentiation among longer-wavelength colours, such as red, orange, yellow and green. Currently, many researchers attribute the evolution and maintenance of polymorphic colour vision to trichromat (¼ heterozygote) advantage. However, dichromacy may be more suited for achromatic tasks, such as penetrating colour camouflage, especially under low-light conditions. We evaluated whether dichromatic capuchin monkeys (Cebus capucinus) were more efficient than trichromatic monkeys at capturing camouflaged and noncamouflaged insects. Through faecal DNA analysis, we determined the genotypes of the M/LWS opsins for 34 capuchins in two groups inhabiting Santa Rosa National Park, Costa Rica. Dichromatic monkeys were more efficient at detecting camouflaged, surface-dwelling insects, especially under conditions of low ambient light. However, unexpectedly, trichromats were more efficient in extracting embedded, noncamouflaged insects from substrates. To our knowledge, this is the first study to document a foraging advantage to dichromatic monkeys in the wild. Our findings show that there is a lack of heterozygote advantage in foraging for surface-dwelling insects and therefore indicate that this mechanism may not be the sole driving force maintaining polymorphic colour vision in this population.