A call-to-action to assist in efforts to protect owl monkeys (Aotus spp.).

The majority of the 11 species of owl monkeys (Aotus spp.) have declining populations or are listed as data deficient. Deforestation due to agriculture, development, or logging poses threats to owl monkeys throughout their range. In some areas, Aotus are hunted for bushmeat or trapped for the wildlife trade. In Colombia, the country with the greatest number of Aotus species, owl monkeys are also threatened by civil unrest. To help combat these challenges, nonprofit organizations and field researchers in habitat countries have successfully implemented a variety of conservation projects such as censusing and monitoring owl monkey populations, establishing protected areas, reforesting degraded areas, filing lawsuits to protect wild populations, helping law enforcement with environmental regulation, and promoting environmental education. We highlight some of the conservation successes and suggest actions people around the world can take to contribute to these important efforts.

The importance of auditory, olfactory, and visual cues for insect foraging in owl monkeys (Aotus nancymaae).

Nocturnal mammals have unique sensory adaptations to facilitate foraging at night. Owl monkeys (Aotus spp.) are pair-living nocturnal platyrrhines adept at capturing insect prey under low-light conditions. Owl monkeys use acoustic and chemical cues in intraspecific communication and use olfaction to detect fruit as they forage. We conducted an experiment to determine which cues (auditory, olfactory, and visual) Aotus nancymaae rely upon when foraging for insects. We scored the behavior of 23 captive owl monkeys during a series of trials in which monkeys were provided sensory boxes with insect cues either present (experimental box) or absent (control box). Each cue was tested alone and in combination with all other cues (multimodal cues). We used generalized linear mixed models to determine which cues elicited the greatest behavioral response. Owl monkeys approached and spent more time near experimental boxes than control boxes. Male owl monkeys were quicker than their female partners to approach the sensory boxes, suggesting that males may be less neophobic than females. The owl monkeys exhibited behaviors associated with olfaction and foraging (e.g., sneezing, trilling) during trials with multimodal cues and when only olfactory cues were present. When only visual or auditory cues were present, owl monkeys exhibited fewer foraging-related behaviors. After approaching a sensory box, however, they often touched boxes containing visual cues. A. nancymaae may rely on olfactory cues at night to detect a food source from several meters away and then rely more on visual cues once they are closer to the food source. Their use of sensory cues during insect foraging differs from nocturnal strepsirrhines, possibly reflecting physiological constraints associated with phylogeny, given that owl monkeys evolved nocturnality secondarily from a more recent diurnal ancestor.

The potential interplay between the glandular microbiome and scent marking behavior in owl monkeys (Aotus nancymaae).

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.

Allogrooming in Male-Female Pairs of Captive Owl Monkeys (Aotus nancymaae).

Owl monkeys (Aotus spp.) are socially monogamous, yet allogrooming is reported to be rare. Because Aotus are nocturnal and arboreal, allogrooming is difficult to observe in natural settings. We observed 21 male-female pairs of captive Aotus nancymaae during 2 nonconsecutive study periods in order to describe the details of allogrooming between mates (partner grooming). We found that grooming bouts are brief and consist of tugging the hair or skin with flexed fingers and/or the mouth. Males groomed females most often, and their rates of partner grooming were negatively related to age. Partner grooming occurred regardless of mating behavior. Camera trap data revealed that the rate of partner grooming (1.50 bouts/h) is greater than that recorded from our direct observations in the early evenings (0.51 bouts/h, in 2013; 0.37 bouts/h in 2003) given that most bouts occurred later in the night. A positive relationship between the rates of the parents' partner grooming and those of their offspring later in life suggests intergenerational transmission. This relationship is influenced by the fathers' rates of partner grooming. We conclude that allogrooming in Aotus is a normal part of their behavioral repertoire that likely serves social functions similar to those in other pair-bonded primates.

Hormonal monitoring of reproductive status in monogamous wild female owl monkeys (Aotus azarai) of the Argentinean Chaco.

The Neotropical owl monkeys (Aotus spp.) are a good model for evaluating the hypothesis that monogamy may arise if female reproductive cycles limit the mating potential of males. To evaluate this hypothesis, we first needed to assess the feasibility of using fecal sampling for monitoring the reproductive status of females. We collected fecal samples (n = 242, from 7 females) from wild adult Aotus azarai females in the Gran Chaco forests of Argentina during 3 years. Fecal estrone-1-glucuronide (E(1)C) and pregnenadiol-3-glucuronide (PdG) tended to rise in parallel during the luteal phase. The average cycle length was 22 ± 3 days (n = 5 females, 10 cycles). We identified 2 conceptive cycles and characterized the E(1)C and PdG profiles of 2 pregnancies. This report is the first of its kind on wild female owl monkeys. Despite the difficulties in sample collection and processing in the field and providing a species-specific validation in the laboratory, we show that fecal samples from A. azarai can be used for monitoring female reproductive status and function.

Mated pairs of owl monkeys (Aotus nancymaae) exhibit sex differences in response to unfamiliar male and female conspecifics.

In socially monogamous species, mate-guarding could be a reproductive strategy that benefits both males and females, especially when males contribute to parental care. By actively guarding mates, males may reduce their chances of being cuckolded, whereas females that mate-guard may reduce the likelihood that their mates will desert them or acquire additional mates, and hence limit or reduce paternal care of offspring. Owl monkeys (Aotus spp.) are socially monogamous with biparental care of young and, hence, potential beneficiaries of mate-guarding. We presented mated pairs of captive owl monkeys (A. nancymaae) with unfamiliar male and female conspecifics, to determine if either member of the pair exhibits intraspecific aggression toward an intruder or stays close to its mate, behaviors indicative of mate-guarding. Male mates were more responsible for the maintenance of close proximity between mates than females. Male mates also exhibited elevated levels of behavior that signify arousal when presented with a male conspecific. These responses by mated male owl monkeys are consistent with patterns that may help prevent cuckoldry.

Insect-foraging in captive owl monkeys (Aotus nancymaae).

Whereas the diets of diurnal primate species vary greatly, almost all nocturnal primate species consume insects. Insect-foraging has been described in nocturnal prosimians but has not been investigated in owl monkeys (Aotus spp.). We studied 35 captive owl monkeys (Aotus nancymaae) in order to describe their foraging behavior and to determine if there were any age or sex differences in their ability to capture insect prey. Because owl monkeys cooperate in parental care and in food-sharing, we expected social interactions involving insect prey. We found that owl monkeys most often snatched flying insects from the air and immobilized crawling insects against a substrate using their hands. Immatures and adult female owl monkeys attempted to capture prey significantly more often than did adult males; however, there was no difference in the proportion of attempts that resulted in capture. Social interactions involving prey appeared similar to those with provisioned food, but possessors of prey resisted begging attempts more so than did possessors of other food. Owl monkeys attempted to capture prey often (mean = 9.5 +/- 5.8 attempts/h), and we speculate that the protein and lipid content of captured prey is important for meeting the metabolic demands for growth and reproduction.