Toni E. Ziegler

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.

Social vocalizations can release oxytocin in humans.

Vocalizations are important components of social behaviour in many vertebrate species, including our own. Less well-understood are the hormonal mechanisms involved in response to vocal cues, and how these systems may influence the course of behavioural evolution. The neurohormone oxytocin (OT) partly governs a number of biological and social processes critical to fitness, such as attachment between mothers and their young, and suppression of the stress response after contact with trusted conspecfics. Rodent studies suggest that OTs release is contingent upon direct tactile contact with such individuals, but we hypothesized that vocalizations might be capable of producing the same effect. To test our hypothesis, we chose human mother–daughter dyads and applied a social stressor to the children, following which we randomly assigned participants into complete contact, speech-only or no-contact conditions. Children receiving a full complement of comfort including physical, vocal and non-verbal contact showed the highest levels of OT and the swiftest return to baseline of a biological marker of stress (salivary cortisol), but a strikingly similar hormonal profile emerged in children comforted solely by their mothers voice. Our results suggest that vocalizations may be as important as touch to the neuroendocrine regulation of social bonding in our species.

Seasonal and Social Correlates of Fecal Testosterone and Cortisol Levels in Wild Male Muriquis (Brachyteles arachnoides)

Fecal testosterone and cortisol levels were analyzed from six wild male muriquis (Brachyteles arachnoides) over a 19-month period at the Estação Biológica de Caratinga in Minas Gerais, Brazil, to investigate the hormonal correlates of seasonal sexual behavior and environmental conditions. Group mean testosterone levels based on weekly samples from the six males did not differ between copulatory and noncopulatory periods or between rainy and dry seasons. Cortisol levels did change with copulatory periods, and were significantly higher during the second dry season, when mating continued following an exceptionally heavy rainy season, than during the first dry season, when mating ceased. Males exhibited individual variation in the timing of their hormone shifts relative to their sexual activity, but neither hormone levels nor sexual activity were related to male age. Despite individual differences in the timing of testosterone fluctuations around the onset and offset of the copulatory season, all males exhibited elevated cortisol concentrations following a slight increase in testosterone at the beginning of the copulatory season. Both the lack of significant changes in testosterone levels with the onset of the rainy and copulatory season and the lack of prebreeding increases in cortisol may be related to the low levels of overt aggression displayed by male muriquis over access to mates.

Urinary oxytocin and social bonding in related and unrelated wild chimpanzees

Animals that maintain cooperative relationships show gains in longevity and offspring survival. However, little is known about the cognitive or hormonal mechanisms involved in cooperation. Indeed, there is little support for a main hypothesis that non-human animals have the cognitive capacities required for bookkeeping of cooperative exchanges. We tested an alternative hypothesis that cooperative relationships are facilitated by an endocrinological mechanism involving oxytocin, a hormone required for bonding in parental and sexual relationships across mammals. We measured urinary oxytocin after single bouts of grooming in wild chimpanzees. Oxytocin levels were higher after grooming with bond partners compared with non-bond partners or after no grooming, regardless of genetic relatedness or sexual interest. We ruled out other possible confounds, such as grooming duration, grooming direction or sampling regime issues, indicating that changes in oxytocin levels were mediated by social bond strength. Oxytocin, which is thought to act directly on neural reward and social memory systems, is likely to play a key role in keeping track of social interactions with multiple individuals over time. The evolutionary linkage of an ancestral hormonal system with complex social cognition may be the primary mechanism through which long-term cooperative relationships develop between both kin and non-kin in mammals.

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.

Hormones associated with non-maternal infant care: a review of mammalian and avian studies.

Hormonal changes during non-maternal infant care have been demonstrated in many cooperatively breeding bird species, some monogamous rodents and two species of New World primates. Coevolution of hormones and social traits may have provided for the different breeding systems that occur today. Several hormones have been shown to covary with the breeding systems of vertebrates. Elevated levels of the hormone prolactin with male parenting behaviours are common to many birds, rodents and the callitrichid monkeys Callithrix jacchus and Saguinus oedipus. In birds, prolactin may be elevated in both male and female breeders during various stages of nest building, egg laying, incubating and feeding of young. Testosterone levels appear to have an inverse relationship to prolactin levels during infant care in birds and rodents, but this relationship has not been examined for primates. In cooperatively breeding birds, helpers who remain at the nest also have elevated levels of prolactin when displaying parental care behaviours. Prolactin levels are elevated in helper callitrichid monkeys during the postpartum period. Monogamous male rodents demonstrate elevated prolactin levels with parental care behaviour but, in contrast to the birds, the mechanisms mediating prolactin increase appear to differ for male and female rodents. Two factors may influence male parental behaviours and hormonal changes: stimuli from the pregnant female and stimuli from the newborn pups; whereas maternal behaviours are influenced by the maternal hormones of the female and the pup stimuli. An experiential factor may also influence male parental behaviours. Neuropeptides such as oxytocin and vasopressin appear to be involved in male rodent parental care and there may be an interaction between a series of hormones and neurosecretions and stimuli from mates and pups. Studies of Saguinus oedipus, the cotton-top tamarin, suggest that prolactin levels are responsive to stimuli from contact with infants and the level of infant care experience influences the levels of prolactin with male infant care. Father tamarins also have elevated levels of prolactin before the birth of infants suggesting that cues from the pregnant female are important. Prolactin’s role in parental care may have evolved from prolactin’s role in other reproductive functions. Hormonal regulation of non-maternal care may occur due to a complex interaction of many hormones and neurotransmitters. Studies described here should provide the impetus for further work on parental care hormones in a wide variety of primates.

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.

The PPAR-γ agonist pioglitazone modulates inflammation and induces neuroprotection in parkinsonian monkeys

BackgroundActivation of the peroxisome proliferator-activated receptor gamma (PPAR-γ) has been proposed as a possible neuroprotective strategy to slow down the progression of early Parkinsons disease (PD). Here we report preclinical data on the use of the PPAR-γ agonist pioglitazone (Actos®; Takeda Pharmaceuticals Ltd.) in a paradigm resembling early PD in nonhuman primates.MethodsRhesus monkeys that were trained to perform a battery of behavioral tests received a single intracarotid arterial injection of 20 ml of saline containing 3 mg of the dopaminergic neurotoxin 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Twenty-four hours later the monkeys were assessed using a clinical rating scale, matched accordingly to disability, randomly assigned to one of three groups [placebo (n = 5), 2.5 (n = 6) or 5 (n = 5) mg/kg of pioglitazone] and their treatments started. Three months after daily oral dosing, the animals were necropsied.ResultsWe observed significant improvements in clinical rating score (P = 0.02) in the animals treated with 5 mg/kg compared to placebo. Behavioral recovery was associated with preservation of nigrostriatal dopaminergic markers, observed as higher tyrosine hydroxylase (TH) putaminal optical density (P = 0.011), higher stereological cell counts of TH-ir (P = 0.02) and vesicular monoamine transporter-2 (VMAT-2)-ir nigral neurons (P = 0.006). Stereological cell counts of Nissl stained nigral neurons confirmed neuroprotection (P = 0.017). Pioglitazone-treated monkeys also showed a dose-dependent modulation of CD68-ir inflammatory cells, that was significantly decreased for 5 mg/kg treated animals compared to placebo (P = 0.018). A separate experiment to assess CSF penetration of pioglitazone revealed that 5 mg/kg p.o. induced consistently higher levels than 2.5 mg/kg and 7.5 mg/kg. p.o.ConclusionsOur results indicate that oral administration of pioglitazone is neuroprotective when administered early after inducing a parkinsonian syndrome in rhesus monkeys and supports the concept that PPAR-γ is a viable target against neurodegeneration.

Activation of Neural Pathways Associated with Sexual Arousal in Non-Human Primates

To evaluate brain activity associated with sexual arousal, fully conscious male marmoset monkeys were imaged during presentation of odors that naturally elicit high levels of sexual activity and sexual motivation.