Vocal buffering of the stress response: exposure to conspecific vocalizations moderates urinary cortisol excretion in isolated marmosets
Introduction
For members of a social species, one of the most profound moderators of function in the hypothalamic–pituitary–adrenal (HPA) axis during times of stress may be the presence of significant social partners (DeVries et al., 2003, Hennessy, 1997, Levine, 1993). This model of social support, sometimes known as buffering, postulates that during times of stress, the presence of significant social partners down-regulates activity in the HPA axis and hence serves to buffer the individual against the stressful stimulus (Cohen and Wills, 1985). Presumably, the beneficial effects associated with the physical presence of a significant social partner derive from the partner's ability to either modify the perceived intensity of the stressor, and/or to down-regulate the magnitude and duration of the HPA response during exposure to the stressful stimulus. This phenomenon has been well studied in the context of mother–offspring interactions. In some species, offspring that are exposed to stressful situations in the presence of the mother display significantly reduced behavioral and glucocorticoid responses to those stressors, relative to offspring exposed to the same stressors in the absence of the mother (see review in Hennessy, 1997). However, this effect of social support is not just limited to mother–infant dyads. Social buffering of behavioral and physiological responses to stress has also been reported in studies involving separation in adult nonhuman primates (e.g., heterosexual pairs: Mendoza and Mason, 1986, Smith et al., 1998; same-sex pairs: Gust et al., 1994).
The physical presence of a social partner is defined by an amalgamation of several distinct stimulus attributes (e.g., visual, olfactory, and auditory signals) as well as by the nature and pattern of social interactions. Presumably, the interactions of these signals function to provide a representation of one individual (the sender) and perhaps the relationship it represents to another individual (the receiver). In the absence of one or more of these signals, as often occurs in visually obscured environments, isolated individuals may attempt to maintain the positive effects of social support by using a single individually specific, or signature, signal rather than having to rely on a combination of several signals. Signature signals have been identified across a wide variety of birds and mammals (e.g., Charrier et al., 2003, Randall, 1989, Sayigh et al., 1998, Searby et al., 2004). Individually distinct communication signals are also prevalent among many nonhuman primates (e.g., Cleveland and Snowdon, 1982, Hammerschmidt and Todt, 1995, Jones et al., 1993, Jorgensen and French, 1998, Snowdon and Cleveland, 1980, Snowdon et al., 1983, Symmes et al., 1979). Therefore, if the physical presence of a social partner can moderate responses (i.e., reduce HPA axis activity) to stressful stimuli, it may be that, in addition to identity, these signature signals also communicate the beneficial effects of social support by communicating representations of individuals and the relationship they represent, in turn moderating the consequences of exposure to stressful events.
Marmosets, small tropical primates from the New World family Callitrichidae, are characterized by strong socioemotional attachments (“pair bonds”) between adult males and females, as well as cooperative infant care and prolonged residence of offspring in extended family groups (Rylands, 1993). Thus, social interactions are an important attribute of callitrichid life, and the resulting social relationships have profound impacts on marmoset physiology and behavior including reproduction (Ginther et al., 2001, Smith et al., 1997, Ziegler and Sousa, 2002), endocrine regulation (Shepherd and French, 1999, Smith and French, 1997, Smith et al., 1998), and communication (Elowson and Snowdon, 1994, Rukstalis et al., 2003, Snowdon and Elowson, 1999, Snowdon and Hodun, 1981, Vitale et al., 2003). In addition to these important social characteristics, marmosets also possess rich vocal repertoires that are used in a wide variety of contexts, including intragroup cohesion and maintenance of territories (Cleveland and Snowdon, 1982, Epple, 1968, Heymann, 1987, Hubrecht, 1985, Stevenson and Poole, 1976). These vocalizations are also known to have “signature” or individually distinct properties which can be used to distinguish individuals among group members (Jones et al., 1993, Jorgensen and French, 1998, Snowdon and Cleveland, 1980). In addition to strong attachments and signature vocalizations, marmosets have also been shown to experience social buffering of the stress response. Smith et al. (1998) demonstrated that marmosets removed from their home cage and exposed to a novel environment had significantly lower levels of urinary cortisol when their heterosexual pair mate was present versus when they were not. Therefore, the existence of complex social interactions, highly conserved, individually identifiable vocalizations, and evidence of social buffering make callitrichid primates ideally suited for examining the effects of individually specific signals on physiological responses to stressful events.
The purpose of the present study was to evaluate whether exposure to a single, individually specific, signal (i.e., phee call) could reduce the consequences of social separation and exposure to environmental novelty. Specifically, we predicted that exposure to the phee call of a significant social partner (i.e., pair mate) would reduce urinary cortisol excretion, a common indicator of psychosocial stress, in marmosets isolated and exposed to a novel environment. Additionally, it may be that exposure to vocalizations from individuals other than the focal animal's pair mate may also influence the physiological consequences of exposure to stressful events. However, given the individually specific nature of marmoset vocalizations and the long-term attachments formed between heterosexual pairs, we predicted that exposure to vocalizations from unfamiliar individuals would not reduce urinary cortisol production in socially isolated individuals exposed to novel environments. We also examined the effect of length of pairing and social proximity, if any, on urinary cortisol excretion upon exposure to a pair mate's vocalization.
Section snippets
Subjects and housing
Subjects for this study were 10 Wied's black tufted-ear marmosets (Callithrix kuhlii) housed in five preexisting, long-term heterosexual pairs at the University of Nebraska at Omaha's Callitrichid Research Center. Table 1 contains demographic information for all marmosets included in the study. The mean age and length of pairing prior to the beginning of the study were 6.8 and 4.4 years, respectively. Wire mesh enclosures for each pair measured approximately 1.2 × 0.9 × 2.4 m and were equipped
Results
Social isolation and exposure to environmental novelty induced a significant physiological stress response in marmosets. The results of our repeated-measures ANOVA revealed a significant interaction between time of sample collection and call condition on levels of urinary cortisol excretion [F(9) = 6.39, P < 0.0001]. After two h, marmosets separated from their pair mates had significantly higher levels of urinary cortisol when exposed to any of the three treatment conditions [unfamiliar calls: t
Discussion
Individual marmosets, isolated from their long-term pair mate and exposed to a novel environment, showed significant increases in the production of glucocorticoids across the 4-h trial period, while urinary cortisol in marmosets that remained in their undisturbed home cages was quite stable. Thus, social isolation and exposure to a novel environment appear to have constituted a significant source of stress. However, the amount of urinary cortisol measured in each condition depended on the
Acknowledgments
We wish to thank Heather Jensen and the volunteers and staff of the Callitrichid Research Center at UNOmaha for their excellent care of the marmoset colony. We would also like to thank Jeff Fite for comments on this manuscript. The work was supported, in part, by funds from the National Science Foundation (IBN 00-91030) and the National Institutes of Health (HD- HD 42882).
References (47)
- et al.
Vocal signature recognition of mothers by fur seal pups
Anim. Behav.
(2003) - et al.
Social modulation of stress responses
Physiol. Behav.
(2003) - et al.
Reproductive biology of captive male cotton-top tamarin monkeys as a function of social environment
Anim. Behav.
(2001) - et al.
Effect of a preferred companion in modulating stress in adult female rhesus monkeys
Physiol. Behav.
(1994) Hypothalamic–pituitary–adrenal responses to brief social separation
Neurosci. Biobehav. Rev.
(1997)- et al.
Social influences on cortisol and behavioral responses of preweaning, periadolescent, and adult guinea pigs
Physiol. Behav.
(2002) - et al.
Assessing the roles of social partners in maintaining mutual proximity, as exemplified by mother–infant relations in rhesus monkeys
Anim. Behav.
(1970) - et al.
Individual recognition by use of odours in golden hamsters: the nature of individual representations
Anim. Behav.
(2001) - et al.
Golden hamsters recognize individuals, not just individual scents
Anim. Behav.
(1994) - et al.
Temporal and social factors influencing behavioral and hormonal responses to separation in mother and infant squirrel monkeys
Psychoneuroendocrinology
(1993)
Parental division of labour and differentiation of attachments in a monogamous primate (Callicebus moloch)
Anim. Behav.
Individual foot drumming signatures in banner-tailed kangaroo rats Dipodomys spectabilis
Anim. Behav.
Acoustic recognition in macaroni penguins: an original signature system
Anim. Behav.
Psychosocial stress and urinary cortisol excretion in marmoset monkeys (Callithrix kuhlii)
Physiol. Behav.
Social and developmental influences on reproductive function in female Wied's black tufted-ear marmosets (Callithrix kuhlii)
Horm. Behav.
Close proximity of the heterosexual partner reduces the physiological and behavioral consequences of novel-cage housing in black tufted-ear marmosets (Callithrix kuhlii)
Horm. Behav.
Individual recognition of contact calls by pygmy marmosets
Anim. Behav.
Responses to context- and individual-specific cues in cotton-top tamarin long calls
Anim. Behav.
An ethogram of the common marmoset (Callithrix jacchus): general behavioral repertoire
Anim. Behav.
Individuality and stability of isolation peeps in squirrel monkeys
Anim. Behav.
Parent–daugther relationships and social controls on fertility in female common marmosets, Callithrix jacchus
Horm. Behav.
The complex vocal repertoire of the adult cotton-top tamarin (Saguinus oedipus oedipus)
Z. Tierpsychol.
Mother–infant attachment in the squirrel monkey: adrenal responses to separation
Behav. Biol.
Cited by (87)
An inconsistent social buffering effect from a static visual substitute in horses (Equus caballus): A pilot study
2023, Journal of Veterinary BehaviorSelection levels on vocal individuality: strategic use or byproduct
2022, Current Opinion in Behavioral SciencesBehavioral, neurochemical, and neuroimmune changes associated with social buffering and stress contagion
2022, Neurobiology of StressSocial buffering of stress – Physiological and ethological perspectives
2021, Applied Animal Behaviour Science