The forests of Argentina’s Formosa province are home to Azara’s owl monkey (Aotus azarae), a pair-living and sexually monogamous primate. Weighing about three pounds and measuring roughly a foot long, these primates boast huge, red eyes nearly half the size of their faces and tails as long as their bodies. Unlike most primates that live in larger social groups, these monkeys live in small family units, with both sexes sharing the responsibilities of territory defense.
A recent study—the most extensive investigation of owl monkey scent-based behaviors in the wild to date—has shed light on their use of scents and smell to communicate with each other. The team, led by Eduardo Fernandez-Duque, a professor of anthropology at Yale University, discovered that olfaction—the detection of chemical odorants in the air—is crucial for coordinating their reproduction and serves as a defense strategy to protect the core area of A. azarae’s home ranges.
Twenty-Eight Years of Data
The study was conducted through the Owl Monkey Project, a program established by Fernandez-Duque in 1996. For twenty-eight years, Fernandez-Duque and his team have been gathering data on owl monkeys, incorporating methods from population biology, behavioral science, genetics, endocrinology, ecology, and demography. Fernandez-Duque emphasized that one of the main benefits of conducting a project with such a long time frame has been the opportunity to study multiple generations of monkeys, given the species’ average lifespan of twenty years. “For understanding evolution, how things are inherited and change over time, the number of generations is a much more informative metric,” Fernandez-Duque said. “I think this is what makes our project very, very robust.”
Through their project, the researchers investigated how owl monkeys use scent signals to coordinate reproduction and assert territorial boundaries. By documenting the frequency, patterns, and locations of scent-marking by owl monkeys, they sought to determine whether these behaviors correlate with reproductive activity or territorial defense, offering insights into how scent shapes their social structures.
Data for this study was gathered from fourteen groups of owl monkeys between 2004 and 2017 using a detailed behavioral ethogram. An ethogram is a comprehensive catalog of specific behaviors that researchers use to systematically record and classify animal actions. This ethogram, developed by Fernandez-Duque and Tony Di Fiore, a professor of anthropology at UT Austin, outlined specific owl monkey behaviors to be recorded and standardized observations of individual monkeys across different time periods. To apply this ethogram, the researchers collected focal samples, which involved observing an individual animal for twenty minutes at a time and recording its behavior in two-minute intervals. Using this behavioral data, they hoped to determine when and why owl monkeys engage in certain olfactory behaviors, possibly linking them to reproductive activity or territorial defense.
“We formed our predictions from observations in the field, as there are a lot of different behavioral, social, and physiological differences between owl monkeys and other species,” said Margaret Corley, an associate research scientist in Yale’s Department of Ecology and Evolutionary Biology and the second author of the study. “There is biparental care, for example, where males are the primary carriers and caregivers for infants, which is very unusual for primates.” Given these unique traits, the researchers recognized that the role of olfactory signals in owl monkeys might be uniquely shaped by their unusual social structure. While many primates use scent for communication, they hypothesized that owl monkeys have highly developed scent-marking behaviors that serve both territorial and mating functions. This hypothesis was informed by years of field observations, including the work of Andrea Spence-Aizenberg, a co-author of the study whose doctoral dissertation focused on the chemical content of the monkeys’ olfactory signals, and how these cues influence mate selection.
Olfaction’s Role in Reproduction
One of the first challenges the researchers faced in the field was distinguishing male and female owl monkeys, which have nearly identical sizes, facial features, and genitalia. To make the monkeys’ sex more quickly identifiable, the team captured the animals and fitted them with bead collars. While we humans need these visual markers, all monkeys need is their sense of smell.
“When we were in the forest once, we saw a monkey walk through a branch, lower their rump, and rub his genitals against a female,” Fernandez-Duque said. “This matched what had been described for owl monkeys in captive settings: they are scent-marking. What we didn’t know is, what are owl monkeys picking up from these chemical signatures?”
As the team narrowed down the kind of information contained in scent markings and examined the role of olfaction in the lab, they discovered sexual dimorphism in the scent markings: males and females were producing different signals. Lab analysis showed age-based variations in chemical signals as well. The collar system allowed the researchers to easily follow the monkeys from behind, causing less disturbance than when observing them from the front. Based on their observations, the team reached a robust conclusion: scent-marking and other olfactory behaviors play an important role in communication between owl monkey pair mates, especially for reproductive coordination.
Adults performed most of the olfactory behaviors observed, and males performed most of the genital inspections, likely to gather information about the females’ reproductive status. However, there were minimal sex differences when it came to other behaviors, like scent-marking, urine washing, and partner-marking behaviors. “To me, that emphasizes the other things we know about owl monkeys: that they live in pairs, and males and females experience relatively equal levels of mating competition,” Corley said. The reduced sexual dimorphism found among owl monkeys reflects their unique monogamous and pair-living social system. In contrast, males of other primate species that live in larger groups face greater competition for mates, which leads to pronounced physical and behavioral differences between sexes as the males develop traits to help them compete.
Scent-Marking as Territorial Defense
The lack of sex differences in scent-marking behaviors indicates that both males and females contribute to the defense of their home ranges and territories. While previous studies found little evidence supporting the idea that scent-marking serves a territorial function, this study suggests scent-marking may be used to defend valuable core areas and resources rather than an entire home range. Around twenty years ago, Fernandez-Duque began noticing fights between solitary monkeys and those belonging to different groups. Over the next few years, his team realized their population was not solely made up of social groups consisting of a mated pair and their offspring: about twenty to twenty-five percent of the monkeys were actually solitary young adults floating around the homes of their peers, trying to find a group to join. They called these solitary individuals “floaters.”
“The discovery of floaters completely changed the way in which we look at mating systems and the social systems of these primates,” Fernandez-Duque said. “Not only do owl monkeys interact with neighbors, [but] they also interact with male and female individuals roaming free in their neighborhood trying to move into their households.”
The discovery of these floaters provided new insight into the potential role of olfaction: Fernandez-Duque and his team realized that many of the fights they had observed between owl monkeys were likely not between neighbors, but between floaters and established families. This conclusion aligned with their data: most scent-marking behaviors occurred in core areas of their ranges. Urine washing and scent-marking were especially common in areas of high overlap between groups, pointing to their usage as forms of territorial signaling. Therefore, scent-marking may serve as a deterrent to other groups and solitary floaters, keeping them from intruding on these core areas, potentially as a strategy for mate defense. Male monkeys, in particular, may use olfactory cues to deter potential rivals.
Conclusions
The team has relied on identifying consistent patterns across monkey groups and seasons as key indicators of more meaningful biological trends. Corley noted that in observational research, correlations can be drawn, but causation cannot.
“An important point in our research group has been to emphasize when interpreting our results that statistical significance doesn’t mean biological significance,” Corley said. “It is necessary to understand the biological relevance of the results we find, regardless of what a single mathematical index may provide.”
While there is value in natural observational research, Fernandez-Duque stressed that lab work is critical to understanding the nutrition, physiology, and paternity of each species. Blood and tissue samples can be extracted to analyze the hormonal values of different animals. From this information, the genetic monogamy of owl monkeys—whether each monkey reproduces exclusively with a single partner—can be determined.
Going forward, the Owl Monkey Project aims to further examine the genetics, endocrinology, energetics, physiology, behavior, and population demography of the owl monkeys in the Formosa Province. Alba Garcia de la Chica, the first author of the study and current co-director of the Owl Monkey Project, is developing projects to study the animals in a different landscape within the region and increase the team’s capacity to obtain genetic samples. “We try to keep a consistent field presence to monitor group changes,” Corley said. “We have to take into account that there may be missing months and some seasons may be better represented than others, but the methods we have in place help establish consistency.”
These ongoing efforts have allowed Fernandez-Duque’s team to continuously contribute to anthropological literature. Their research, spanning topics from intrasexual competition in monogamous primates and floaters to the chemical composition of glandular secretions, helps scientists better understand the evolutionary mechanisms and motivations shaping different reproductive and social behaviors in primates.