The potential interplay between the glandular microbiome and scent marking behavior in owl monkeys (<i>Aotus nancymaae</i>)

Abstract

In mammals, scent marking behavior is a pervasive form of chemical communication that regulates social interactions within and between groups. Glandular microbiota consist of bacterial communities capable of producing chemical cues used in olfactory communication. Despite countless studies on scent marking in primates, few have examined the microbiota associated with glandular secretions. Nancy Ma's owl monkeys (Aotus nancymaae) are nocturnal, socially monogamous primates that frequently scent mark using their subcaudal glands. Previous analyses revealed that unique chemical signatures of Aotus may convey information about sex and age. We used positive reinforcement to sample the subcaudal glands of 23 captive owl monkeys to describe their glandular microbiomes and examine how patterns in these bacterial communities vary with age, sex, rearing environment and/or social group (pair identity). We coupled these analyses with behavioral observations to examine patterns in their scent marking behavior. We isolated 31 bacterial species from Phyla Firmicutes, Proteobacteria, and Actinobacteria, consistent with the dermal and glandular microbiomes of other primates. Several bacterial taxa we identified produce volatile organic compounds, which may contribute to olfactory communication. These bacterial communities are best predicted by an interaction between sex, rearing environment and pair identity rather than any of these variables alone. Within mated pairs of A. nancymaae, males and females scent mark their nest boxes at similar frequencies. In some pairs, rates of scent marking by males and females fluctuated over time in a similar manner. Pairs that had been together longer tended to exhibit the greatest similarities in their rates of scent marking. Together, these findings suggest that scent marking behavior and close social interactions with pair mates in Aotus may influence bacterial transmission and their glandular microbiomes. Chemical communication, including coordinated scent marking, may play a role in strengthening pair bonds, signaling pair status and/or in mate guarding in this socially monogamous primate.