Charles T. Snowdon

Are subordinates always stressed? a comparative analysis of rank differences in cortisol levels among primates

Among primate species there is pronounced variation in the relationship between social status and measures of stress physiology. An informal meta-analysis was designed to investigate the basis of this diversity across different primate societies. Species were included only if a substantial amount of published information was available regarding both social behavior and rank-related differences in stress physiology. Four Old World and three New World species met these criteria, including societies varying from small-group, singular cooperative breeders (common marmoset and cotton top tamarin) to large-troop, multi-male, multi-female polygynous mating systems (rhesus, cynomolgus, talapoin, squirrel monkeys, and olive baboon). A questionnaire was formulated to obtain information necessary to characterize the stress milieu for individuals in particular primate societies. We standardized cortisol values within each species by calculating the ratio of basal cortisol concentrations of subordinates to those of dominants in stable dominance hierarchies and expressing the ratio as a percentage (relative cortisol levels). The meta-analysis identified two variables that significantly predicted relative cortisol levels: subordinates exhibited higher relative cortisol levels when they (1). were subjected to higher rates of stressors, and (2). experienced decreased opportunities for social (including close kin) support. These findings have important implications for understanding the different physiological consequences of dominant and subordinate social status across primate societies and how social rank may differ in its behavioral and physiological manifestations among primate societies.

The Relationship of Cortisol Levels to Social Environment and Reproductive Functioning in Female Cotton-Top Tamarins, Saguinus oedipus

Cortisol levels were examined in 17 cotton-top tamarin monkeys (Saguinus oedipus) to determine: (1) if first-morning void urine sampling could be used as a noninvasive method for monitoring cortisol excretion, (2) if capture and bleeding were associated with changes in urinary cortisol levels, (3) the relative cortisol levels in reproductively active and reproductively suppressed females, and (4) the relationship between cortisol levels and changes in social condition in cotton-top tamarins. Mean urinary cortisol levels during ovarian cycling did not differ between captured and bled females and undisturbed females. Mean cortisol levels were significantly lower in females who were housed in their natal groups and reproductively suppressed than in the same females when they were removed and placed adjacent to a novel male and ovarian cycling began. For all females, mean cortisol levels were higher during the periovulatory period than during the nonperiovulatory period of the ovulatory cycle, with mean cortisol levels higher in newly cycling females than in long-term cycling females. No differences were found in mean cortisol levels between long-term cycling females and prepubertal females and postpubertal natal females. Cortisol levels from long-term cycling females were much lower than during the first two to three ovarian cycles occurring in newly cycling female tamarins, during the last part of pregnancy, and during the first 6 weeks postpartum. These data provide evidence that (1) suppression of ovarian cycling in postpubertal females remaining in their natal family is not associated with stress-induced changes in cortisol levels, (2) cortisol levels are not strictly tied to reproductive condition, and (3) social change may be reflected in cortisol elevation.

Detection of the chemical signals of ovulation in the cotton-top tamarin, Saguinus oedipus

Abstract Abstract. Behavioural, visual or chemical signalling of the ovulatory period occurs in most mammalian species. In primates, the type of signalling has been linked to mating strategies. It has been suggested that monogamous and polyandrous primates conceal evidence of the periovulatory period. Cotton-top tamarins, Saguinus oedipus , do not display visual or consistent changes in sexual behavioural cues indicating the periovulatory period, although conceptions occur on 84% of all post-partum ovulations in captivity. To examine the possibility that olfactory cues of ovulation are used to signal other tamarins of the females reproductive status, daily scent marks were collected from a donor female during the ovulatory cycle and transferred to the home cage of eight male-female pairs for testing. Recipient females contacted the platform containing the scent mark significantly more often during the periovulatory period (3 days around the urinary luteinizing hormone peak of the donor female) than the non-periovulatory period (the rest of the cycle: follicular and luteal). Recipient males increased the frequency of mounts of the cagemate female and penile erection rates were significantly higher during the donor females periovulatory period. These results provide evidence that there is a direct olfactory cue of ovulation in female tamarins and that this cue affects the males sexual behaviour. This evidence does not support the theory of concealed ovulation since the monogamous cotton-top tamarin appears to signal the timing of ovulation.

The effects of control over high intensity noise on plasma cortisol levels in rhesus monkeys

The effects of control over exposure to high intensity noise on plasma cortisol levels and social behaviors were examined in rhesus monkeys. There were four conditions: control over noise, loss of control over noise, no control over noise, and no noise. Plasma cortisol data indicated that animals with control over high intensity noise stimulation did not differ from animals exposed to no noise at all. Plasma cortisol levels were significantly elevated in animals with no control over high intensity noise and in animals experiencing a loss of control over noise. Animals which experienced loss of control over noise showed increased aggressive behavior while animals with no control over noise showed significantly less social contact than other animals.

Hormonal Responses to Parental and Nonparental Conditions in Male Cotton-Top Tamarins,Saguinus oedipus,a New World Primate

The socially monogamous cotton-top tamarin (Saguinus oedipus) monkey is a cooperative breeder with the breeding male providing extensive parental care shortly after birth. We examined the relationship of urinary prolactin and cortisol excretion both to male parental care and as a stress response in the cotton-top tamarin monkey. First-morning urine samples were collected to determine hormonal concentrations. Hormonal and behavioral data were collected on 8 male cotton-top tamarins during the 2 weeks before and the 2 weeks following birth of infants to their mate, 11 nonparental males with exposure to females, and three eldest sons from large family groups. Prolactin levels were significantly higher in experienced fathers during the postpartum period than in the other males, while cortisol levels were significantly lower in experienced fathers and eldest sons. Prolactin levels in experienced fathers were consistently elevated before birth, following birth, and after infants were weaned; prolactin levels during times of infant independence were still significantly higher than those in nonfather males. First-time fathers exhibited prolactin levels that were significantly higher after the births of infants than these same males did when they were paired with nonpregnant females. Elevated prolactin concentrations also occurred prior to the first birth, suggesting that males may be receiving cues from their pregnant females. The elevated prolactin levels in parental males may be associated with the experience of the fathers. Correlation between prolactin levels and number of successful births, number of previous births, and age were high. The care of newborn infants did not appear to be a stressful event since cortisol levels were not elevated postpartum. Both cortisol and prolactin were elevated following capture and injection of saline or a dopaminergic receptor antagonist, indicating that prolactin does respond to acute stress. Cortisol levels did not coincide with prolactin levels except under acute stress conditions, suggesting that different neural pathways are probably involved in prolactin release during parental care versus acute stress. These studies provide evidence that male urinary prolactin levels may be elevated due to cues from pregnant females and the constant exposure of males to the family environment.

Social development during the first twenty weeks in the cotton-top tamarin (Saguinus o. oedipus)

Abstract Fourteen infant cotton-top tamarins from five captive family groups were studied during the first 20 weeks of life. We examined the roles of parents and of siblings of different ages as caregivers and as social companions for the infants, as well as the effects of group composition and group size on these roles. Parents and adult siblings played similar active roles in infant caregiving during the first few weeks after birth, with males showing a greater involvement than females. In groups without other offspring the two parents showed equal infant caregiving behaviour, whreas fathers carried more than mothers did in groups with offspring present. Although infants received more caregiving from males, they showed a preference for contact and proximity with their mothers. No sex differences were found in infant behaviour or in the direction of behaviour by caregivers toward infants. Twins showed greater amounts of both social and solitary play in weeks 15–20 than did singletons, and there was no effect of the number of older siblings on the amount of play shown by an infant.

Pygmy marmosets, Cebuella pygmaea, modify vocal structure in response to changed social environment

Abstract Abstract. Pygmy marmosets displayed plasticity in vocal structure over a 5-month study of nine individuals. Changes in acoustical structure of a contact call, the trill, were investigated when two unfamiliar, captive populations of monkeys were placed together in a common acoustical environment. Monkeys representing four age categories (infant, juvenile, subadult and adult) were studied in three time blocks: 9 weeks of no acoustical interaction, the first 4 weeks after contact and 6-10 weeks after contact. Analyses of variance showed that the monkeys made coextensive shifts in two frequency measures (bandwidth and peak frequency) making parallel vocal changes rather than converging on or diverging from one anothers call form. Call duration initially showed distinct population differences that disappeared after acoustic contact between the populations. Comparable analyses of trills given by pygmy marmosets that did not experience novel social companions did not show significant changes. These results suggest greater vocal plasticity across age ranges than has been hitherto described for a non-human primate and suggest the importance of social factors in vocal architecture.

Individual recognition of contact calls by pygmy marmosets

Individual recognition by voice has been frequently assumed to be an important phenomenon in the social species. The present study on pygmy marmosets (Cebuella pygmaea) demonstrated that there are distinctive acoustic features in each of two contact calls by which individuals could be distinguished from each other. Individual pygmy marmosets responded differently depending on which type of contact call was given and on the identity of the vocalizing animal. Playbacks of individual calls through hidden speakers produced some evidence for differential individual responses, but only when they originated from familiar locations. These results indicate that pygmy marmosets recognize each other on the basis of their contact calls.

Acoustic adaptation in pygmy marmoset contact calls: Locational cues vary with distances between conspecifics

Summary1.The pygmy marmoset, Cebuella pygmaea, has four trill variants in its vocal repertoire. One of these trills has a different behavioral message from the other three. However, the remaining trills, which were physically different from each other, did not seem to differ in their behavioral messages.2.The three trills can be ordered according to their acoustic cues for sound localization. This suggested that the most localizable trill is used when caller and recipient are far apart, while the least localizable trill is used only when animals are close together.3.A field study in the Peruvian Amozon showed that this was correct. Thus, pygmy marmosets seem to use selectively the variations in trill structure to minimize locatability when other cues are available for determining location and to maximize locatability when other means of determining location are absent.4.Pygmy marmoset trills contain mostly high frequency components which decay rapidly over short distances in humid, forested environments. However, these high frequencies are shown to be above the major frequencies of ambient noise in the environment, thus giving the pygmy marmoset a frequency window for communication. Furthermore, the frequencies of the marmoset trills are above the maximum auditory sensitivity of their major predators.

An investigation of categorical speech discrimination by rhesus monkeys

The categorical discrimination of synthetic human speech sounds by rhesus macaques was examined using the cardiac component of the orienting response. A within-category change which consisted of stimuli differing acoustically in the onset of F2 and F3 transitions, but which are identified by humans as belonging to thesame phonetic category, were responded to differently from a no-change control condition. Stimuli which differed by the same amount in the onset of F2 and F3 transitions, but which human observers identify as belonging toseparate phonetic categories, were differentiated to an even greater degree than the within-category stimuli. The results provide ambiguous data for an articulatory model of human speech perception and are interpreted instead in terms of a feature-detector model of auditory perception.