Development of a partner preference test that differentiates between established pair bonds and other relationships in socially monogamous titi monkeys (Callicebus cupreus)

Abstract

Partner preference, or the selective social preference for a pair mate, is a key behavioral indicator of social monogamy. Standardized partner preference testing has been used extensively in rodents but a single test has not been standardized for primates. The goal of this study was to develop a partner preference test with socially monogamous titi monkeys (Callicebus cupreus) adapted from the widely used rodent test. In Experiment 1, we evaluated the test with pairs of titi monkeys (N=12) in a three-chambered apparatus for three hours. The subject was placed in the middle chamber, with grated windows separating it from its partner on one side and an opposite sex stranger on the other side. Subjects spent a greater proportion of time in proximity to their partners’ windows than the strangers’, indicating a consistent preference for the partner over the stranger. Touching either window did not differ between partners and strangers, suggesting it is not a reliable measure of preference. Subjects chose their partner more than the stranger during catch and release sessions at the end of the test. In Experiment 2, we compared responses of females with current partners (N=12) in the preference test with other relationship types representing former attachment bonds (N=13) and no attachment bond (N=8). Only females from established pair bonds spent significantly more time near their partner’s window compared to the stranger indicating that this measure of preference is unique to current partners. Other measures of preference did not differentiate behavior toward a current partner and other relationship types. This test reproduces behavioral patterns found in previous studies in titi monkeys highlighting the accuracy of this new partner preference test. This test can be used as a standardized measure of partner preference in titi monkeys to quantitatively study pair bonding and evaluate factors influencing partner preference.

Challenges to the Pair Bond: Neural and Hormonal Effects of Separation and Reunion in a Monogamous Primate

“…They show a behavioral preference for their partner over a stranger (Carp et al, 2016); their partner can buffer their stress response to novelty (Hennessy et al, 1995; Mendoza et al, 2000); and they display distress upon separation from their partner, which is not reduced by the presence of another animal (Mendoza and Mason, 1986a,b; Mendoza, 1991; Laugero et al, 2011; Ragen et al, 2012). Distress is displayed both physiologically by increased cortisol concentrations and behaviorally by contact calls for the mate and increased locomotion (Mendoza et al, 2000; Ragen et al, 2012).…”

Serotonin 1A agonism decreases affiliative behavior in pair-bonded titi monkeys

“…Much of our understanding of pair-bonding in primates comes from the study of the socially monogamous titi monkey ( Callicebus cupreus ), which forms selective and enduring pair-bonds between a single adult male and female (Mason, 1966). This relationship, and attachment relationships more broadly, involve specific preference for and proximity maintenance to the attachment figure (Carp et al, 2015), physiological and affective response to involuntary separation from the attachment figure (Hennessy, 1997), and social buffering of stress responses in the presence of the attachment figure that does not occur in the presence of another individual (Mason and Mendoza, 1998). …”

Pair bond formation leads to a sustained increase in global cerebral glucose metabolism in monogamous male titi monkeys (Callicebus cupreus)

“…Animals were fed twice daily (0830 and 1330 h) a diet consisting of New World monkey chow, rice cereal, banana, apples, raisins, and baby carrots and water was available ad libitum . Further details of husbandry and training are available elsewhere (Tardif et al, 2006), with caging identical to that described in (Carp et al, 2016). …”

“…They duet, maintain small territories which they defend against intrusion, and the male is the main carrier of the infants (Mason, 1966, 1968, Mendoza and Mason, 1986b). Adult pairs display many characteristics of a pair bond, including preference for their partner (Carp et al, 2016), distress upon separation (Mendoza and Mason, 1986a), and the ability of the partner to buffer stress (Mendoza et al, 2000). In a previous study, we showed that males that had been in long-term pairs, vs. males that were not paired, showed many differences in regional cerebral glucose metabolism (rCGM) using positron emission tomography (PET) with [ 18 F]-fluorodeoxyglucose (FDG)(Bales et al, 2007).…”