Anatomy and dietary specialization influence sensory behaviour among sympatric primates

Abstract

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.

Keywords: colour vision; frugivory; olfaction; plant–animal interactions; platyrrhine; sensory ecology.

Figure 1.

Study species and principal diet: (a) black-handed spider monkey, Ateles geoffroyi, frugivore; (b) white-faced capuchin monkey, Cebus imitator, (frugivore–omnivore) and (c) mantled howler monkey, Alouatta palliata, (folivore–frugivore). Photo credits: Fernando Campos (a), Amanda Melin (b,c). (Online version in colour.)

Figure 2.

Boxplots of interspecific variation for (a) average monthly per cent fruit feeding (${\chi }_2^2=44.7$, p < 0.0001), (b) nasal turbinate surface area (${\chi }_2^2=15.95$, p < 0.0001), (c) thumb : index ratios (${\chi }_2^2=20.11$, p < 0.0001) and (d) density of fungiform papillae (${\chi }_2^2=23.27$, p < 0.0001). Images: (a) Ateles feeding on fruit, (b) the reconstructed left nasal turbinate (yellow) and ethmoturbinate (orange) for Cebus, (c) sketches of typical Alouatta, Ateles and Cebus hands and (d) fungiform papillae on a tongue. (Online version in colour.)

Figure 3.

Incidence rate ratio plots and statistical significance of GLMMs for the effect of primate species on investigation sequences (question 1) including (a) sniffing, (b) touch and (c) bite followed by reject. For each panel, the incidence of foraging sequences using that behaviour for Alouatta and Cebus are plotted relative to the incidence in Ateles. Ateles was arbitrarily chosen as the reference species (vertical dashed line at 1). These results include only trichromatic individuals across the three primate species. LRT statistics for each model against the null model and pairwise contrasts were reported for each panel. Photo credits: Carrie Veilleux, Amanda Melin, Fernando Campos. (Online version in colour.)