No abstract

Eye-tracking methods measure what humans and other animals visually attend to in the environment. In nonhuman primates, eye tracking can be used to test hypotheses about how primates process social information. This information can further our understanding of primate behavior as well as offer unique translational potential to explore causes of or treatments for altered social processing as seen in people with neurodevelopmental disorders such as autism spectrum disorder and schizophrenia. However, previous methods for collecting eye-tracking data in nonhuman primates required some form of head restraint, which limits the opportunities for research with respect to the number of or kinds of primates that can undergo an eye-tracking study. We developed a novel, noninvasive method for collecting eye tracking data that can be used both in animals that are difficult to restrain without sedation as well as animals that are of different ages and sizes as the box size can be adjusted. Using a transport box modified with a viewing window, we collected eye-tracking data in both New (Callicebus cupreus) and Old World monkeys (Macaca mulatta) across multiple developmental time points. These monkeys had the option to move around the box and avert their eyes from the screen, yet, they demonstrated a natural interest in viewing species-specific imagery with no previous habituation to the eye-tracking paradigm. Provided with opportunistic data from voluntary viewing of stimuli, we found that juveniles viewed stimuli more than other age groups, videos were viewed more than static photo imagery, and that monkeys increased their viewing time when presented with multiple eye tracking sessions. This noninvasive approach opens new opportunities to integrate eye-tracking studies into nonhuman primate research.

Duets in pair-bonding primates serve as a primary mode of communication between pairs, and duets may provide cues to conspecifics regarding the calling individual or pair. Here, we test the hypothesis that pulse elements in coppery titi monkey duets vary with condition and identity of the caller. We predicted that pulse elements would vary with age, sex, or pair-bond length. We estimated pulse rate and duration for 378 pulse elements from the duets of 74 captive titi monkeys (Plecturocebus cupreus). We found inter-individual variation in both features, and evidence for vocal convergence among pair mates in pulse rate. Age was the best predictor of pulse rate, and pulse rate decreased with age. Age and pair-bond length reliably predicted pulse duration. Our results suggest that variation in titi monkey duets reflects differences in caller condition and pair identity, and contribute to growing evidence for vocal plasticity in nonhuman primates.

As social animals, many primates use acoustic communication to maintain relationships. Vocal individuality has been documented in a diverse range of primate species and call types, many of which have presumably different functions. Auditory recognition of one's neighbors may confer a selective advantage if identifying conspecifics decreases the need to participate in costly territorial behaviors. Alternatively, vocal individuality may be nonadaptive and the result of a unique combination of genetics and environment. Pair-bonded primates, in particular, often participate in coordinated vocal duets that can be heard over long distances by neighboring conspecifics. In contrast to adult calls, infant vocalizations are shortrange and used for intragroup communication. Here, we provide two separate but complementary analyses of vocal individuality in distinct call types of coppery titi monkeys (Plecturocebus cupreus) to test whether individuality occurs in call types from animals of different age classes with presumably different functions. We analyzed 600 trill vocalizations from 30 infants and 169 pulse-chirp duet vocalizations from 30 adult titi monkeys. We predicted that duet contributions would exhibit a higher degree of individuality than infant trills, given their assumed function for long-distance, intergroup communication. We estimated 7 features from infant trills and 16 features from spectrograms of adult pulse-chirps, then used discriminant function analysis with leave-one-out cross-validation to classify individuals. We correctly classified infants with 48% accuracy and adults with 83% accuracy. To further investigate variance in call features, we used a multivariate variance components model to estimate variance partitioning in features across two levels:within-and between-individuals. Between-individual variance was the most important source of variance for all features in adults, and three of four features in infants. We show that pulse-chirps of adult titi monkey duets are individually distinct, and infant trills are less individually distinct, which may be due to the different functions of the vocalizations. K E Y W O R D S discriminant function analysis, pair bonding, vocal duetting, vocalization individuality

In socially monogamous titi monkeys, involuntary separation from a pair mate can produce behavioral distress and increased cortisol production. The neuropeptide oxytocin (OXT) is thought to play an important role in the separation response of pair-bonded species. Previous studies from our lab have shown that chronic intranasal oxytocin (IN OXT) during development can have long-term effects on adult social behavior. In the current study, we examined the chronic and acute effects of IN OXT or Saline (SAL) on the subjects’ response to a brief separation from their pair mates. Subjects with a history of chronic IN OXT or SAL treatment during development received a single dose of OXT or SAL as adults 30 min before being separated from their pair mate. Chronic treatment consisted of a daily dose of IN OXT (0.8 IU/kg) or SAL (control) from 12 to 18 months of age. Subjects (N = 29) were introduced to a pair mate at 30 months of age. After the pairs had cohabitated for 5 months, pairs underwent two “Brief Separation” (OXT and SAL) and two “Non-Separation” (OXT and SAL) test sessions. Vocalizations and locomotion were measured as behavioral indices of agitation or distress during the Brief Separation and Non-Separation periods (30 min each). We collected blood samples after the Brief Separation and Non-Separation periods to measure cortisol levels. Our results showed subjects treated with chronic OXT had a reduction in long call and peep vocalizations compared to subjects treated with chronic SAL. Subjects treated with chronic SAL and acute OXT produced more peeps and long calls compared to animals treated with acute SAL; however, patterns in this response depended on sex. Cortisol and locomotion were significantly higher during the Brief Separation period compared to the Non-Separation period; however, we did not find any treatment or sex effects. We conclude that chronic IN OXT given during development blunts the separation response, while acute OXT in chronic SAL subjects had sexually dimorphic effects, which could reflect increased partner seeking behaviors in males and increased anxiety in females.

Most pair-living primate species engage in duets, wherein males and females produce coordinated vocalizations. Previous analyses of male gibbon contributions to the duet have shown that calls are individually distinct. Here we investigate variation in the temporal and spectral parameters in the male contribution to the duet, also known as the coda, of wild, nonhabituated male Müller's Bornean gibbons (Hylobates muelleri), recorded both opportunistically and as a response to playbacks at the Stability of Altered Forest Ecosystems site in Sabah, Malaysia. We used linear discriminant function analysis to estimate the intra-and interindividual variation in 13 spectral and temporal parameters of the vocalizations (N = 337) of 31 male gibbons. To further understand how call features vary within and between individuals we used a multivariate, variance components model to investigate how variance in features was partitioned at these two levels. We could identify males with a 66% accuracy using leave-one-out cross-validation, a relatively low score compared to female Müller's Bornean gibbons and males of other species. We found that for some features (such as maximum frequency of the notes) most of the variance occurred between males, but for others (specifically total duration of the call and duration of rest in between notes) most of the variance occurred within a single male. Overall, male Müller's Bornean gibbon coda vocalizations showed greater variability relative to their female counterparts, raising questions about potential differences in the function of the male and female contributions to the duet in Müller's Bornean gibbons and the gibbon taxon as a whole.

Across diverse systems including language, music and genomes, there is a tendency for longer sequences to contain shorter constituents; this phenomenon is known as Menzerath's Law. Whether Menzerath's Law is a universal in biological systems, is the result of compression (wherein shortest possible strings represent the maximum amount of information) or emerges from an inevitable relationship between sequence and constituent length remains a topic of debate. In non-human primates, the vocalizations of geladas, male gibbons and chimpanzees exhibit patterns consistent with Menzerath's Law. Here, we use existing datasets of three duetting primate species (tarsiers, titi monkeys and gibbons) to examine the wide-scale applicability of Menzerath's Law. Primate duets provide a useful comparative model to test for the broad-scale applicability of Menzerath's Law, as they evolved independently under presumably similar selection pressures and are emitted under the same context(s) across taxa. Only four out of the eight call types we examined were consistent with Menzerath's Law. Two of these call types exhibited a negative relationship between the position of the note in the call and note duration, indicating that adherence to Menzerath's Law in these call types may be related to breathing constraints. Exceptions to Menzerath's Law occur when notes are relatively homogeneous, or when species-specific call structure leads to a deterministic decrease in note duration. We show that adherence to Menzerath's Law is the exception rather than the rule in duetting primates. It is possible that selection pressures for long-range signals that can travel effectively over large distances was stronger than that of compression in primate duets. Future studies investigating adherence to Menzerath's Law across the vocal repertoires of these species will help us better elucidate the pressures that shape both short- and long-distance acoustic signals.

Relationships support social animals’ health, but maintaining relationships is challenging. When transitioning to parenthood, new parents balance pair‐bond maintenance with infant care. We studied pair‐bond maintenance via affiliation in 22 adult titi monkey pairs (Plecturocebus cupreus) for 16 months centered around their first offspring's birth. Pair affiliation peaked during pregnancy, decreased across the postpartum period, and rose after reaching minimum affiliation 32.6 weeks postpartum. Pairs in which fathers carry infants more than average had lower affiliation at the infant's birth and return to an increase in affiliation sooner. Parents of infants who were slow to independence had higher rates of affiliation. Titi monkey infants actively prefer their fathers; mothers may avoid their infant‐carrying mate, suggesting infants play an active role in parental affiliative decline. Our data supports previous findings that affiliation between partners declines following an infant's birth, but demonstrates new knowledge about the extent and duration of affiliative decline.