Anatomy and dietary specialization influence sensory behaviour among sympatric primates.

Senses form the interface between animals and environments, and provide a window into the ecology of past and present species. However, research on sensory behaviours by wild frugivores is sparse. Here, we examine fruit assessment by three sympatric primates (Alouatta palliata, Ateles geoffroyi and Cebus imitator) to test the hypothesis that dietary and sensory specialization shape foraging behaviours. Ateles and Cebus groups are comprised of dichromats and trichromats, while all Alouatta are trichomats. We use anatomical proxies to examine smell, taste and manual touch, and opsin genotyping to assess colour vision. We find that the frugivorous spider monkeys (Ateles geoffroyi) sniff fruits most often, omnivorous capuchins (Cebus imitator), the species with the highest manual dexterity, use manual touch most often, and that main olfactory bulb volume is a better predictor of sniffing behaviour than nasal turbinate surface area. We also identify an interaction between colour vision phenotype and use of other senses. Controlling for species, dichromats sniff and bite fruits more often than trichromats, and trichromats use manual touch to evaluate cryptic fruits more often than dichromats. Our findings reveal new relationships among dietary specialization, anatomical variation and foraging behaviour, and promote understanding of sensory system evolution.

Non-visual senses in fruit selection by the mantled howler monkey (Alouatta palliata).

There is extensive knowledge about the visual system and the implications of the evolution of trichromatic color vision in howler monkeys (genus Alouatta) related to food selection; however, information about the other sensory systems is limited. In this study we assessed the use of touch, sniffing, and taste in fruit evaluation by 20 adult mantled howler monkeys (Alouatta palliata) on Agaltepec Island, Mexico. During 9 months of observation, we recorded the frequency that each monkey used touch, sniffing, and taste in evaluating cryptic fruits (that remain green during their ripening process) and conspicuous fruits (with red, yellow, or orange colorations when they are ripe). Sucrose content and hardness measurements were made to establish the degree of ripeness of the fruits. We found that mantled howler monkeys used long behavioral sequences during conspicuous fruit investigations. Sniffing was used infrequently, but significantly more often in the evaluation of conspicuous-ripe and unripe fruits compared to cryptic-ripe and unripe fruits. During the evaluation of cryptic-ripe fruits, mantled howler monkeys increased the use of touch compared to evaluating cryptic-unripe fruits. We did not find significant differences in the use of taste in the evaluation of cryptic and conspicuous fruits (both ripe and unripe). Our results suggest that the non-visual senses play an essential role in fruit selection by howler monkeys, with differences in the behavioral strategy according to the fruit's conspicuity. The multimodal signals of ripe and unripe fruits allow the howler monkeys to assess their palatability before being consumed.

Visual detection and fruit selection by the mantled howler monkey (Alouatta palliata).

Howler monkeys (platyrrhini) have evolved routine trichromatic color vision independently from catarrhines, which presents an opportunity to test hypotheses concerning the adaptive value of distinguishing reddish from greenish hues. A longstanding hypothesis posits that trichromacy aids in the efficient detection of reddish-ripe fruits, which could be an advantage for the detection of the nutritional content of the fruit, such as sugars. In the present study, we assessed fruit visual conspicuity and selection based on color and sucrose content by wild mantled howler monkeys (Alouatta palliata) on Agaltepec Island, Mexico. We used colorimetry to classify dietary fruits as cryptic (greenish) or conspicuous (reddish) against their background leaves. Species-specific color models indicate that trichromatic howler monkeys should be more efficient in discriminating the conspicuous ripe fruits from leaves compared to detecting cryptic ripe fruits from leaves. We found howler monkeys consume more cryptic fruits compared to conspicuous fruits, and that they consume more unripe fruits than ripe fruits. The consumption (acceptance) of fruit was independent of sucrose content, and thus this disaccharide may not play an essential role in mantled howler food selection. Our findings suggest that routine trichromatic color vision may aid in the detection and discrimination of conspicuously colored fruits, but that the final decision whether to accept or reject a fruit probably involves the use of other senses in addition to vision.