For many species, the presence of a significant social partner can lessen the behavioral and physiological responses to stressful stimuli. This study examined whether a single, individually specific, signature vocalization (phee call) could attenuate the physiological stress response that is induced in marmosets by housing them in short-term social isolation. Utilizing a repeated-measures design, adult marmosets (n=10) were temporarily isolated from their long-term pair mate and exposed to three conditions: signature vocalizations from the pair mate, phee calls from an unfamiliar opposite sex individual, or no auditory stimuli. Levels of urinary cortisol were monitored as a physiological indicator of the stress response. Urinary cortisol levels were also monitored, while subjects remained undisturbed in their home cages to provide baseline levels. Temporarily isolated marmosets showed significantly higher levels of urinary cortisol than undisturbed marmosets. However, the nature of the acoustic stimulus experienced during isolation led to differences in the excretion of urinary cortisol. Isolated marmosets exposed to a familiar pair mate's vocalization showed significantly lower levels of urinary cortisol than when exposed to unfamiliar marmoset vocalizations (P <0.04) or to no auditory stimuli (P <0.03). Neither the duration of pairing nor the quality of relationship in the pair (indexed by spatial proximity scores) predicted the magnitude of reduction in cortisol in the familiar vocalization condition. The results presented here provide the first evidence that a single, individually specific communication signal can decrease the magnitude of a physiological stress response in a manner analogous to the physical presence of a social partner, a process we term "vocal buffering."

Vocal plasticity in the face of changing social context is well‐documented in passerine birds, but the degree to which changes in social environment affect the vocal structure of non‐human primates is a topic which has remained largely unexplored. We assessed whether modification of social environments, in this case the presence of marmosets in neighboring cages, influenced the vocal morphology of phee calls, which possess ‘signature’‐like features, in Wied's black tufted‐ear marmosets (Callithrix kuhlii). Individual phee calls were obtained over a period of 8 wk from 11 animals maintained in rooms with stable social environments. After this baseline phase, seven marmosets were housed for an additional 8 wk in rooms that contained cages with unfamiliar marmosets, while four marmosets maintained the same neighbors as the first phase. Calls were digitized and both frequency and temporal parameters were measured. Multivariate discriminant function analyses (DFA) generated from vocalizations collected in the first phase produced functions that accurately classified calls to the correct individual, showing that calls had significant individual distinctiveness. DFAs generated from vocalizations in the first phase of the study continued to show high classification accuracy for marmosets in a stable social environment, but DFAs from the first phase were significantly less likely to correctly classify vocalizations in marmosets that were housed next to novel conspecifics. These data show that phee calls, which have signature‐like properties in marmosets, can be modified by changes in social context. The results suggest a degree of plasticity in vocal signals that is rare among non‐human primates.

All female primates incur energetic costs associated with producing and caring for offspring, but females belonging to the New World primate family Callitrichidae, the marmosets and tamarins, appear to face even further demands. In fact, the energetic demands of rearing callitrichid infants are thought to have led to the evolution of cooperative infant care in these species. If this explanation is true, then one might expect that natural selection should also have shaped patterns of maternal behavior to be sensitive to the costs of reproduction and equipped females to reduce their investment in offspring under certain conditions. Therefore, we examined the maternal effort and postpartum endocrine profiles of individual female marmosets (Callithrix kuhlii) across conditions that represented two hallmarks of callitrichid reproduction-conception during the early postpartum period and alloparental assistance. When females conceived during the early postpartum period and faced the upcoming demands of caring for their newly conceived litters (Study 1), they significantly reduced their caregiving effort and had significantly higher postpartum levels of estradiol relative to breeding attempts in which conception occurred later in the postpartum period. Postpartum estradiol was negatively correlated with maternal carrying effort. When experienced alloparents were present (Study 2), females again reduced their caregiving effort relative to breeding attempts in which experienced alloparents were not present. Postpartum cortisol, however, did not vary as a function of experienced alloparental assistance. The results of these studies suggest that female marmosets have been subjected to similar selection pressures as females of other primate taxa-to maximize their reproductive success by reducing their investment in offspring under the worst and best of conditions-and suggest that hormones may mediate within-female variation in maternal care. These studies also provide support for the notion that mothers are "flexible opportunists" when it comes to providing care to their young.

The proximate mechanisms that regulate transitions in mammalian female reproductive effort have not been widely studied. However, variation in circulating levels of the androgenic steroid hormone testosterone (T) appears to mediate a trade-off between investment in current and future offspring in males. The purpose of this study was to investigate the possibility that T is also associated with transitions in the reproductive effort of females, by examining the relationship between urinary T excretion, maternal caregiving behavior, and the timing of the postpartum conception in female Wied's black tufted-ear marmosets (Callithrix kuhlii). We examined the maternal carrying effort and peripartum T profiles of six females across two conditions: (1) when they conceived during the period of infant dependence (DPID), such that gestation was coupled with lactation; and (2) when the same females conceived after the period of infant dependence (APID). We also assessed the relationship between postpartum T levels and caregiving effort. When female marmosets conceived DPID, they dramatically reduced their caregiving effort, and had higher levels of urinary T, relative to when they conceived APID. Further, the litter-to-litter changes in maternal caregiving effort that we observed were related to variation in urinary T excretion; as weekly levels of urinary T excretion increased, concurrent caregiving effort declined. Our results suggest that variation in T secretion may regulate transitions in female reproductive behavior, and that the regulation of male and female parental behavior may be mediated by homologous neuroendocrine mechanisms.

Corticotropin-releasing hormone (CRH) has multiple roles in coordinating the behavioral and endocrine responses to a host of environmental challenges, including social stressors. In the present study we evaluated the role of CRH in mediating responses to a moderate social stressor in Wied's black tufted-eared marmosets (Callithrix kuhlii). Male and female marmosets (n=14) were administered antalarmin (a selective CRH-1 receptor antagonist; 50 microg/kg, p.o.) or vehicle in a blind, counterbalanced, crossover design. One hr after treatment, marmosets were separated from long-term pairmates and then housed alone in a novel enclosure for 7 hr. Behavior was recorded during separation and upon reunion with the partner, and urine samples for cortisol assay collected before, during, and after the intervention. Separation from partners elevated urinary cortisol concentrations over baseline for both conditions, but antalarmin treatment reduced the magnitude of the elevation. Antalarmin also lowered rates of behavioral patterns associated with arousal (alarm and "e-e" vocalizations, object manipulate/chew), but had no effect on contact calls, locomotory activity or alertness. Although most patterns of social behavior upon reunion with the partner were not affected by antalarmin, antalarmin-treated marmosets displayed more sexual behavior (mounts and copulations) upon reunion. These data indicate that antagonism of the CRH-1 receptor acts to reduce the magnitude of both endocrine and behavioral responses to a moderate social stressor without causing any overall reduction in alertness or general activity. This supports the hypothesis that CRH, acting through its type 1 receptor, is involved in coordinating the responses to anxiety-producing events. These results further suggest that the marmoset is a useful model for exploration of the role of CRH in mediating the behavioral and neuroendocrine responses to psychosocial stressors, particularly in the context of heterosexual social relationships.