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Open Access Publications from the University of California

Scholarly Works (15 results)

  • Article
  • Peer Reviewed
UC Davis Previously Published Works (2023)
Some paired primates use complex, coordinated vocal signals to communicate within and between family groups. The information encoded within those signals is not well understood, nor is the intricacy of individuals behavioral and physiological responses to these signals. Considering the conspicuous nature of these vocal signals, it is a priority to better understand paired primates responses to conspecific calls. Pair-bonded titi monkeys (Plecturocebus cupreus) sing duets comprised of the male and females long call. Here, we use a playback study to assess female titi monkeys responses to different vocal stimuli based on the subjects pairing status. Six adult female titi monkeys participated in the study at two timepoints--pre-pairing and post-pairing. At each timepoint, subjects underwent three distinct playbacks--control recording, male solo vocalization, and pair duet. Behaviors such as locomotion and vocalizations were scored during and after the playback, and cortisol and androgen values were assessed via a plasma blood sample. Female titi monkeys attended more to social signals compared to the control, regardless of pairing status. However, in the time immediately following any playback type, female titi monkeys trilled more and spent a greater proportion of time locomoting during pre-pairing timepoints (compared to post-pairing). Female titi monkeys behavioral responses to social audio stimuli, combined with subjects increases in cortisol and androgens as paired individuals, imply female titi monkeys attend and respond to social signals territorially.
    Cover page: Pairing status and stimulus type predict responses to audio playbacks in female titi monkeys.
    • Thesis
    • Peer Reviewed
    UC Davis Electronic Theses and Dissertations (2023)

    Communication reinforces vital social bonds across the animal kingdom. Some of the most rare and specialized social systems require similarly specialized communication. One of the rarest social organizations in the animal kingdom, especially amongst mammals, is monogamy. Monogamous mates rely on a variety of communication modalities to find and initiate a bond, maintain their bond, coordinate daily activity, raise offspring, avoid predation, and defend shared resources, among other behaviors . Understanding these communication signals, both their structure and function, is of utmost importance in order to fully understand closely bonded social species. Coppery titi monkeys (Plecturocebus cupreus) are monogamous, South American monkeys who form selective, enduring psychosocial emotion attachments, referred to as pair bonds. Titi monkeys must form and maintain long term relationships, coordinate biparental care, and maintain control over a shared territory. These pair-bonded monkeys provide the perfect model system in which to investigate a variety of communication modalities in relationship to the unique pair bond. At the California National Primate Research Center, I investigated three aspects of titi monkey communication. First, I assessed patterns of individual identity in the morning adult duet contributions and infant trill vocalizations of this species. Strong patterns of individuality exist in adult duets, such that individuals are identifiable based on vocalizations alone. Second, I assessed female titi monkey responses to a variety of vocal stimuli in a playback experiment. Female titi monkey responses depended more on their own pairing status and reproductive status than the content of the social vocalization, suggesting titi monkeys respond generally to any unfamiliar acoustic signal. Finally, I presented titi monkeys with paired faces of their mate and a stranger in order to test for a partner preference in looking behavior. I found little evidence of visual partner preference based on two dimensional, static photos of titi monkey faces. However, age and pair-bond tenure predicted individuals’ looking behavior in the eye tracking paradigm. In total, this body of work deepens our understanding of two key communication modalities¬––vocal and visual-––in the uniquely pair-bonded titi monkey.

      • Article
      • Peer Reviewed
      UC Davis Previously Published Works (2020)
      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 ones 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 short-range 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.
        Cover page: Individuality in the vocalizations of infant and adult coppery titi monkeys (Plecturocebus cupreus).
        • Article
        • Peer Reviewed
        UC Davis Previously Published Works (2020)
        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 short-range 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.
          • Article
          • Peer Reviewed
          UC Davis Previously Published Works (2022)
          Acoustic signals are ubiquitous across mammalian taxa. They serve a myriad of functions related to the formation and maintenance of social bonds and can provide conspecifics information about caller condition, motivation and identity. Disentangling the relative importance of evolutionary mechanisms that shape vocal variation is difficult, and little is known about heritability of mammalian vocalizations. Duetting--coordinated vocalizations within male and female pairs--arose independently at least four times across the Primate Order. Primate duets contain individual- or pair-level signatures, but the mechanisms that shape this variation remain unclear. Here, we test for evidence of heritability in two call types (pulses and chirps) from the duets of captive coppery titi monkeys (Plecturocebus cupreus). We extracted four features--note rate, duration, minimum and maximum fundamental frequency--from spectrograms of pulses and chirps, and estimated heritability of the features. We also tested whether features varied with sex or body weight. We found evidence for moderate heritability in one of the features examined (chirp note rate), whereas inter-individual variance was the most important source of variance for the rest of the features. We did not find evidence for sex differences in any of the features, but we did find that body weight and fundamental frequency of chirp elements covaried. Kin recognition has been invoked as a possible explanation for heritability or kin signatures in mammalian vocalizations. Although the function of primate duets remains a topic of debate, the presence of moderate heritability in titi monkey chirp elements indicates duets may serve a kin recognition function.
            Cover page: Moderate evidence for heritability in the duet contributions of a South American primate
            • Article
            • Peer Reviewed
            UC Davis Previously Published Works (2021)
            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.
              Cover page: Parenting costs time: Changes in pair bond maintenance across pregnancy and infant rearing in a monogamous primate (Plecturocebus cupreus)
              • Article
              • Peer Reviewed
              UC Davis Previously Published Works (2023)
              Primates live in a variety of social groupings and vary in the expression of species-typical behaviors depending upon social conditions. Coppery titi monkeys (Plecturocebus cupreus) are pair-bonding, territorial primates often used to study neurobiology and social behavior in captivity at the California National Primate Research Center (CNPRC). At the center, titi monkeys are housed in cages of standardized size. However, the number of cages--and thus families--per room varies based upon the room size (small or large). Anecdotal evidence suggests titi monkeys behave differently in the two different room sizes. To empirically test this, we measured rates of pair-bonding related affiliation in 23 pairs of titi monkeys. We predicted that monkeys in small rooms would show higher rates of affiliation compared to large rooms. We used a between- and within- subjects design in which all subjects moved from either small to large or large to small rooms. Affiliative behavior was recorded via bihourly instantaneous scan samples. We found that titi monkey pairs affiliated significantly more in small rooms compared to large rooms (partial R2 = 0.1468, t(33) = -3.729, p-value < .0005). We also confirmed that the presence of offspring negatively impacts pair affiliation rates (partial R2 = 0.2240, t(33) = -0.181, p-value = 0.0011). The results of this study suggest that titi monkey pair behavior is influenced by room size, and thus the number of neighboring groups. Management decisions should consider the implications that housing may have on the results of social behavior research.
                Cover page: Room size and offspring presence impact pair-bonded primate affiliation
                • Article
                • Peer Reviewed
                UC Davis Previously Published Works (2020)
                The nonhuman primate provides a sophisticated animal model system both to explore neurobiological mechanisms underlying complex behaviors and to facilitate preclinical research for neurodevelopmental and neuropsychiatric disease. A better understanding of evolutionarily conserved behaviors and brain processes between humans and nonhuman primates will be needed to successfully apply recently released NIMH guidelines (NOT-MH-19-053) for conducting rigorous nonhuman primate neurobehavioral research. Here, we explore the relationship between two measures of social behavior that can be used in both humans and nonhuman primates-traditional observations of social interactions with conspecifics and eye gaze detection in response to social stimuli. Infant male rhesus macaques (Macaca mulatta) serving as controls (N = 14) for an ongoing study were observed in their social rearing groups and participated in a noninvasive, longitudinal eye-tracking study. We found significant positive relationships between time spent viewing eyes of faces in an eye tracker and number of initiations made for social interactions with peers that is consistent with similar observations in human populations. Although future studies are needed to determine if this relationship represents species-typical social developmental processes, these preliminary results provide a novel framework to explore the relationship between social interactions and social attention in nonhuman primate models for neurobehavioral development.
                  Cover page: New approaches to quantify social development in rhesus macaques (Macaca mulatta): Integrating eye tracking with traditional assessments of social behavior
                  • Article
                  • Peer Reviewed
                  UC Davis Previously Published Works (2021)
                  The Snake Detection Theory implicates constricting snakes in the origin of primates, and venomous snakes for differences between catarrhine and platyrrhine primate visual systems. Although many studies using different methods have found very rapid snake detection in catarrhines, including humans, to date no studies have examined how quickly platyrrhine primates can detect snakes. We therefore tested in captive coppery titi monkeys (Plecturocebus cupreus) the latency to detect a small portion of visible snake skin. Because titi monkeys are neophobic, we designed a crossover experiment to compare their latency to look and their duration of looking at a snake skin and synthetic feather of two lengths (2.5 cm and uncovered). To test our predictions that the latency to look would be shorter and the duration of looking would be longer for the snake skin, we used survival/event time models for latency to look and negative binomial mixed models for duration of looking. While titi monkeys looked more quickly and for longer at both the snake skin and feather compared to a control, they also looked more quickly and for longer at larger compared to smaller stimuli. This suggests titi monkeys' neophobia may augment their visual abilities to help them avoid dangerous stimuli.
                    • Article
                    • Peer Reviewed
                    UC Davis Previously Published Works (2022)
                    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.
                      Cover page: Effects of Chronic and Acute Intranasal Oxytocin Treatments on Temporary Social Separation in Adult Titi Monkeys (Plecturocebus cupreus)
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