Trichromacy increases fruit intake rates of wild capuchins (Cebus capucinus imitator)

Abstract

Intraspecific color vision variation is prevalent among nearly all diurnal monkeys in the neotropics and is seemingly a textbook case of balancing selection acting to maintain genetic polymorphism. Clear foraging advantages to monkeys with trichromatic vision over those with dichromatic "red-green colorblind" vision have been observed in captive studies; however, evidence of trichromatic advantage during close-range foraging has been surprisingly scarce in field studies, perhaps as a result of small sample sizes and strong impacts of environmental or individual variation on foraging performance. To robustly test the effects of color vision type on foraging efficiency in the wild, we conducted an extensive study of dichromatic and trichromatic white-faced capuchin monkeys (Cebus capucinus imitator), controlling for plant-level and monkey-level variables that may affect fruit intake rates. Over the course of 14 months, we collected behavioral data from 72 monkeys in Sector Santa Rosa, Costa Rica. We analyzed 19,043 fruit feeding events within 1,602 foraging bouts across 27 plant species. We find that plant species, color conspicuity category, and monkey age class significantly impact intake rates, while sex does not. When plant species and age are controlled for, we observe that trichromats have higher intake rates than dichromats for plant species with conspicuously colored fruits. This study provides clear evidence of trichromatic advantage in close-range fruit feeding in wild monkeys. Taken together with previous reports of dichromatic advantage for finding cryptic foods, our results illuminate an important aspect of balancing selection maintaining primate opsin polymorphism.

Keywords: color vision; frugivory; opsin genes; platyrrhine; sensory ecology.

Fig. 1.

Juvenile white-faced capuchins forage for the fruit of Allophylus occidentalis (A and B) and a katydid insect (C and D). Images simulate capuchin trichromacy (A and C; λ_max 532 and 561) and dichromacy (C and D; λ_max 532), using customized software (31), demonstrating the increased difficulty of visually discerning the ripe fruits, but not the leaf-camouflaged insect.

Fig. 2.

Fruit intake rates [mean, ±SE (bold lines) and 95% confidence intervals (dashed lines)] are plotted as least-squares (LS) means for dichromatic and trichromatic monkeys.

Fig. S1.

Fruit intake rates [mean ±SE (bold lines) and 95% confidence intervals (dashed lines)] of different age classes are plotted as least-squares (LS) means for mature (≥6 y), large immature (≥3 y), and small immature (<3 y) monkeys. Negative values reflect log-transformation of data before analysis.

Fig. 3.

Fruit intake rates (fruits eaten/second) of dichromatic and trichromatic wild capuchin monkeys across different plant species and fruit conspicuity categories of fruits consumed in Sector Santa Rosa, Costa Rica.