Maria Bernardete Cordeiro de Sousa

Novel aspects of glucocorticoid actions.

Normal hypothalamic‐pituitary‐adrenal (HPA) axis activity leading to the rhythmic and episodic release of adrenal glucocorticoids (GCs) is essential for body homeostasis and survival during stress. Acting through specific intracellular receptors in the brain and periphery, GCs regulate behaviour, as well as metabolic, cardiovascular, immune and neuroendocrine activities. By contrast to chronic elevated levels, circadian and acute stress‐induced increases in GCs are necessary for hippocampal neuronal survival and memory acquisition and consolidation, as a result of the inhibition of apoptosis, the facilitation of glutamatergic neurotransmission and the formation of excitatory synapses, and the induction of immediate early genes and dendritic spine formation. In addition to metabolic actions leading to increased energy availability, GCs have profound effects on feeding behaviour, mainly via the modulation of orexigenic and anorixegenic neuropeptides. Evidence is also emerging that, in addition to the recognised immune suppressive actions of GCs by counteracting adrenergic pro‐inflammatory actions, circadian elevations have priming effects in the immune system, potentiating acute defensive responses. In addition, negative‐feedback by GCs involves multiple mechanisms leading to limited HPA axis activation and prevention of the deleterious effects of excessive GC production. Adequate GC secretion to meet body demands is tightly regulated by a complex neural circuitry controlling hypothalamic corticotrophin‐releasing hormone (CRH) and vasopressin secretion, which are the main regulators of pituitary adrenocorticotrophic hormone (ACTH). Rapid feedback mechanisms, likely involving nongenomic actions of GCs, mediate the immediate inhibition of hypothalamic CRH and ACTH secretion, whereas intermediate and delayed mechanisms mediated by genomic actions involve the modulation of limbic circuitry and peripheral metabolic messengers. Consistent with their key adaptive roles, HPA axis components are evolutionarily conserved, being present in the earliest vertebrates. An understanding of these basic mechanisms may lead to novel approaches for the development of diagnostic and therapeutic tools for disorders related to stress and alterations of GC secretion.

Hormonal changes related to paternal and alloparental care in common marmosets (Callithrix jacchus)

The physiological mechanisms of parental and alloparental care in cooperatively breeding nonhuman primate species such as the common marmoset (Callithrix jacchus) are poorly known. In this study, we examined prolactin and cortisol plasma levels of fathers and older offspring of both sexes, with and without previous experience in infant carrying, around parturition and during infant carrying. Blood samples were collected from fathers and older offspring and prolactin and cortisol were measured by RIA and EIA, respectively. Prolactin levels of both caretakers were not influenced by infants birth, previous experience or proximity to parturition. However, prolactin levels increased in both caretakers while in physical contact with infants and also with the number of infants being carried in older offspring. These findings suggest that increased prolactin seems to be mainly due to physical effort rather than a physiological trigger of paternal and alloparental care in common marmosets. Cortisol levels were higher for experienced fathers shortly before parturition which could act to reinforce affiliative bonds between breeding males and females at this time or in the ability of males to detect the proximity of the parturition or both.

Parent-Daughter Relationships and Social Controls on Fertility in Female Common Marmosets, Callithrix jacchus

This study examined the reproductive status of mothers and daughters to determine if parent-eldest daughter interactions would influence the daughters fertility in the cooperatively breeding common marmoset, Callithrix jacchus. Twice weekly fecal samples were collected for hormonal analyses from seven daughters and their mothers and analyzed for cortisol, estradiol, and progesterone by EIA. Behavioral data were collected three times weekly while the daughters were under three conditions: natal family, after removing from the family and paring with a novel male, and after removing from the paired condition and placed back with the family (renatal). Under the natal condition, five of the seven daughters exhibited ovarian cycles while their mother was pregnant or displaying ovarian cycling. The five cycling daughters spent significantly more time initiating affilative behaviors with their mothers than with their fathers and showed significant changes in their behavior over the length of the ovarian cycle. However, aggression, submission, and sexual behaviors were very low for daughters in the natal phase. No differences between cortisol levels were found for a daughter and her mother. Cortisol levels showed a significant and sustained increase upon pairing within the first 20 days. All females but one cycled while paired. Six of the seven females were accepted back into the family after pairing and five of the seven females were ovulating. These results suggest that marmoset daughters are not necessarily reproductively suppressed while living with the family. Additionally, these data suggest that female marmosets that leave their family to explore mating opportunities with other groups may return to their family without reproductive or aggressive consequences.

Two Breeding Females within Free-Living Groups May Not Always Indicate Polygyny: Alternative Subordinate Female Strategies in Common Marmosets (Callithrix jacchus)

The mating system of callitrichids has been reported to be monogamous, polygynous and polyandrous. In Callithrix jacchus, groups with 2 breeding females and groups with 1 breeding female have been reported. Our purpose was to evaluate the occurrence of occasional reproduction by subordinate females in free-ranging C. jacchus groups characterized as monogamous. Four groups were monitored at a field site of IBAMA-Brazil for between 20 and 72 months. We recorded the birth of 7 sets of twins to subordinate females that had never reproduced before. Sexual activities were recorded opportunistically: dominant females copulated with only the resident male, while subordinates copulated with extra-group males. We suggest these were essentially monogamous groups that occasionally had 2 reproductive females. Between-group copulations seem to be an alternative strategy used by the subordinates. Despite the costs, there would probably be benefits as a result of scanning for vacancies for reproductive positionsin neighbouring groups and the establishment of ties with extra-group males that might become a reproductive partner in the future.

Morning and Afternoon Patterns of Fecal Cortisol Excretion among Reproductive and Non-Reproductive Male and Female Common Marmosets, Callithrix jacchus

Adult female common marmosets show diurnal variation in the pattern of fecal cortisol excretion, with low levels in the morning and higher levels in the afternoon. In this species females compete to reproduce, the subordinate ones have their fertility suppressed, and cortisol levels tend to be higher in reproductive (dominant) than in non-reproductive females. To determine if males show the same diurnal variation and the influence of reproductive condition on the pattern of fecal cortisol excretion, we collected fecal samples from 10 captive adult (5 male and 5 female) common marmosets (Callithrix jacchus) living in 3 family groups in outdoor cages in the Núcleo de Primatologia, Natal, RN, Brazil. All fecal samples were collected from 05:00 a.m. to 05:00 p.m. (a light phase of approximately 12 hours), twice a week for 4 consecutive weeks for each family. We standardized as morning the period from 05:00 to 11:00 a.m. and as afternoon 11:00 a.m. to 05:00 p.m. Fecal cortisol was measured in the samples after extraction procedures (hydrolysis and solvolysis) followed by enzyme-immunoassay. The MANOVA post hoc Tukey test showed that the diurnal excreted cortisol did not vary among males and was significantly lower than in females. When the reproductive condition of males and females was taken into account, statistical analysis showed that fecal cortisol did not differ within reproductive and non-reproductive males and females. Baseline values for cortisol in feces were higher in females than in males, even among those that were not reproducing. This probably reflects the fact that the relationship between females is more tense within the social group since they have to dispute and maintain their reproductive status. Besides reflecting different reproductive strategies for males and females of common marmosets, the low excretion of cortisol in males may be the consequence of low cortisol levels in blood or may be due to different mechanisms involved in its excretion in this gender.

Mating Systems and Female–Female Competition in the Common Marmoset, Callithrix jacchus

Mating systems in callitrichids are flexible, but usually only one female breeds. Reproductive skew models suggest that either dominant individuals can control the incidence of subordinate reproduction, and that when subordinates breed, it represents a concession from the dominant individual (Optimal Skew Model (OSM)), or alternatively, that subordinates breed because dominants are unable to control them (Incomplete Control Model (ICM)). We present data both from a captive study and a long term field study to test which model better explains mating systems and female-female competition in Callithrix jacchus. A 10-year study of a wild population allowed us to identify three possible mating systems occurring in groups: monogyny, monogyny with breeding attempts from subordinates (pseudo-polygyny), and polygyny. Comparison of interbirth intervals and time to produce a surviving offspring indicated that polygyny is costly to females, suggesting that females should benefit from monopolization of reproduction. Data from an experimental captive study indicated that dominant females are not always able to physiologically and/or behaviorally suppress subordinate females’ reproduction. The literature suggests that helpers are necessary to ensure the survival of dominant females’ offspring; however, our field data show that not all adults help equally. A few individuals, mostly adult males, participate significantly more in infant care than other helpers, suggesting that dominant females gain little by retaining subordinate females in their groups. These results indicate that dominant females are not able to control subordinates’ reproduction, suggesting that the flexibility of C. jacchus mating systems is better explained by ICM than by OSM.

Behavioral and Hormonal Analysis of Social Relationships Between Oldest Females in a Wild Monogamous Group of Common Marmosets (Callithrix jacchus)

Social organization in common marmosets (Callithrix jacchus) appears to be based on a hierarchy of dominance, in which dominant females limit the reproductive functioning of subordinates. Reduced fertility was documented for captive but not for wild females. We investigated social dynamics and hormonal profiles of females living in a wild group. We collected behavioral and hormonal data during 7 mo from the reproductive and two nonreproductive adult females (probably daughters), and their interactions with the reproductive male. The subjects lived in a monogamous group at Nísia Floresta field station in northeastern Brazil. We collected behavioral data as all day follows, once a week and fecal material twice a week. We analyzed fecal samples for cortisol and progesterone using enzyme immuno assay (EIA) techniques. During the first three months we monitored the reproductive female (GRE) and the oldest nonreproductive female, (GIO). After the disappearence of GIO, we monitored the next oldest subordinate adult female, (GRA). GRE had just given birth at the beginning of the study, and she gave birth 6 mo later. During the last 2 weeks of GREs gestation, GRA showed elevated progesterone levels, indicating ovarian cycling. Cortisol levels from GRE and GRA reached very high levels then. During GRAs cycling period, her interactions with the reproductive male (GT) were lower than when she was not cycling. We saw sexual interactions only between GT and GRE. The results provide evidence that ovarian function in mature subordinate females might be affected by the reproductive condition of the dominant female.

Reproduction and aging in marmosets and tamarins.

This chapter presents data on the relations between reproduction and aging in both captive and free-ranging marmosets and tamarins. The relationship is examined from two perspectives. First, the relation of age to physiological impairments in reproductive function is explored. Callitrichid females, in common with many other nonhuman primates, begin to display anovulation associated with follicular depletion at a point relatively close to the maximum life span. Unlike Old World primates, however, they continued to display significant steroidogenic activity in the ovary. There are age effects on some reproductive output variables, such as litter size and inter-birth interval, though the effects are often small. Like other mammals, male marmosets display a change in levels of androgens with age, although the magnitude of the decrease is not large and they actually mount an elevated response to GnRH challenge as they age. We also examined whether age affects either the establishment or maintenance of a breeding position, the factors most important in determining lifetime reproductive success. Infant mortality did increase with increasing parturitions, suggesting that there may have been aging or parturition effects on lactation. Generally, marmoset females were well past the age of sexual maturity at the beginning of the tenure and approaching 8-9 years at the end of it. Reproductive decline did not appear to be a gradual process, but a rather abrupt one, often causing the dismantling of the group. There are potentially interesting relations among maternal age, mass and declining reproductive performance, given the known importance of mass as a determinant of reproductive success in female callitrichids.

Social isolation disrupts hippocampal neurogenesis in young non-human primates

Social relationships are crucial for the development and maintenance of normal behavior in non-human primates. Animals that are raised in isolation develop abnormal patterns of behavior that persist even when they are later reunited with their parents. In rodents, social isolation is a stressful event and is associated with a decrease in hippocampal neurogenesis but considerably less is known about the effects of social isolation in non-human primates during the transition from adolescence to adulthood. To investigate how social isolation affects young marmosets, these were isolated from other members of the colony for 1 or 3 weeks and evaluated for alterations in their behavior and hippocampal cell proliferation. We found that anxiety-related behaviors like scent-marking and locomotor activity increased after social isolation when compared to baseline levels. In agreement, grooming—an indicative of attenuation of tension—was reduced among isolated marmosets. These results were consistent with increased cortisol levels after 1 and 3 weeks of isolation. After social isolation (1 or 3 weeks), reduced proliferation of neural cells in the subgranular zone of dentate granule cell layer was identified and a smaller proportion of BrdU-positive cells underwent neuronal fate (doublecortin labeling). Our data is consistent with the notion that social deprivation during the transition from adolescence to adulthood leads to stress and produces anxiety-like behaviors that in turn might affect neurogenesis and contribute to the deleterious consequences of prolonged stressful conditions.

Changes in peak expiratory flow and respiratory strength during the menstrual cycle

This study evaluated the spirometry and respiratory static pressures in 17 young women, twice a week for three successive ovulatory menstrual cycles to determine if such variables changed across the menstrual, follicular, periovulatory, early-to-mid luteal and late luteal phases. The factors phases of menstrual cycle and individual cycles had no significant effect on the spirometry variables except for peak expiratory flow (PEF) and respiratory static pressures. Significant weak positive correlations were found between the progesterone:estradiol ratio and PEF and between estrogen and tidal volume (r = 0.37), inspiratory time (r = 0.22), expiratory time (r = 0.19), maximal inspiratory pressure (r = 0.25) and maximal expiratory pressure (r = 0.20) and for progesterone and maximal inspiratory pressure (r = 0.32) during the early-to-mid luteal phase. Although most parameters of the spirometry results did not change during the menstrual cycle, the correlations observed between sexual hormones and respiratory control variables suggest a positive influence of sexual female hormones controlling the thoracic pump muscles in the luteal phase.