The effect of social environment on estrogen excretion,scent marking,and sociosexual behavior in tamarins (Saguinus oedipus)

The influence of various social environments on estrogen excretion, scent marking, and the expression of sociosexual behavior was examined in cotton-top tamarins (Sanguinus o. oedipus). Behavioral observations and urine collections were conducted on five females while first housed in their natal family group or in the presence of another cycling adult female and then while housed with an unrelated adult male in a separate cage. Behavioral observations only were conducted on males in natal family groups and while housed with an unrelated adult female. Levels of urinary estrone and estradiol for females were measured by specific radioimmunoassays. Females housed in family groups or in the presence of an adult cycling female showed low and noncyclic patterns of estrogen excretion. Removal from these environments resulted in a rapid increase in urinary estrone and estradiol and three of five females demonstrated cyclic patterns of estrone excretion. Rates of anogenital marking in females were elevated after the social change, and sexual interactions, virtually absent in the original environments, were observed in all five females. In males, similar manipulations of the social environment affected the expression of sexual behavior, but not scent marking. The social environment, therefore has a profound impact on fertility and sociosexual behavior in cotton-top tamarin groups, with implications for callitrichid social structure and behavior.     

Fertility status,dominance, and scent marking behavior of family-housed female cotton-top tamarins (Saguinus oedipus) in absence of their mothers

The effect of the mother's absence on the fertility status and expression of scent marking behavior was examined in 12 sexually mature female cotton-top tamarins (Saguinus oedipus) living in four motherless families. Behavioral data and urine samples were collected on an average of five times per week and levels of estrone-glucuronide (E1G) were quantified directly by radioimmunoassay to establish whether the females showed ovarian cyclicity. Of the 12 females investigated only the dominant female in each motherless group exhibited regular E1G cycles. By contrast, low and acyclic hormonal profiles were found for subordinate sisters. In addition to differences in the patterns and levels of E1G, scent gland morphology and rates of scent marking differed between females: dominant, cycling females had elaborate glands and significantly higher rates of scent marking than subordinates. These results indicate that the presence of the mother (breeding female) is one important factor regulating ovarian function in cotton-top tamarin daughters. The findings also show that dominance status is a vital determinant of each female's subsequent physiological reproductive competence, with only the dominant female obtaining complete fertility and probably inhibiting ovulatory activity in her subordinate sisters. Scent marking behavior seems to be involved in the regulation of this phenomenon of intrasexual reproductive competition.     

Scent-marking in the tamarin, Saguinus oedipus: Sex differences and ontogeny

Many mammalian species which exhibit scent-marking behaviour show a pronounced sexual dimorphism in marking behaviour and scent gland morphology. However, several species of marmosets and tamarins do not show dimorphism in these traits. We examined sex differences in scent-marking structures and behaviour in cotton-top tamarins (Saguinus o. oedipus; Primates: Callitrichidae). While body size and weight were virtually identical in adult males and females, there were pronounced sex differences in scent gland size and in rates of marking behaviour. Females possessed larger anogenital and suprapubic glands and showed 10-fold higher rates of anogenital marking and slightly higher rates of suprapubic marking than males. Observations on the development of anogenital marking revealed a lack of dimorphism during the first 2 years. Adult rates of anogenital marking in females were only observed in females housed separately from their natal family group. The onset of adult levels of marking behaviour corresponds with the adoption of the role of a breeding adult female, suggesting that anogenital marking plays a role in sexual communication.     

Breeding of the cotton-top tamarin Saguinus oedipus oedipus: A comparison with the common marmoset

A colony experienced in the successful breeding of thecommon marmoset acquired 15 cotton-top tamarins for breeding purposes over a period of 2 yrs. Data are presented on the breeding of the cotton-top and compared with the breeding of the common marmoset. The tamarins did not breed as successfully as the common marmosets. There were several reasons for this: Cotton-tops took longer to produce young on initial pairing, had a longer birth interval, and showed a high incidence of suspected infanticide and parental neglect. These factors are thought to be largely responsible for the relatively low reproductive potential of the cotton-top in captivity.     

The endocrinology of puberty and reproductive functioning in female cotton-top tamarins (Saguinus oedipus) under varying social conditions

Sexual maturation and fertility were assessed in fourteen cotton-top tamarin (Saguinus oedipus) females under various social conditions. Six tamarin females (20-28 mo of age) showed a suppression of fertility while living with their families. Hormonal profiles demonstrated low, acyclic levels of urinary luteinizing hormone (LH) and estrone-conjugates (E1C). A rapid onset of ovarian and pituitary cyclicity occurred when four of the six females were removed from their families and paired with an unrelated male. In one female, an ovulatory LH peak occurred as early as eight days after pairing and resulted in conception and full-term pregnancy. Two of the six females were housed in total isolation for 30 days following their removal from the family and prior to pairing. Gradual increases in hormone concentrations occurred during isolation; however, there was no ovarian cyclicity until each female was paired with an unrelated male. In all six females, conception occurred before or as a result of the third ovulatory cycle. Partial isolation of a 36-mo-old female resulted in elevated LH and E1C levels, but cyclicity was not observed until the female was paired with an unrelated male. These findings indicate that removal of a female from the family alone does not initiate ovarian cycling. Sexual maturation, or puberty, occurs in female tamarins living with their families between 15 and 17 mo of age when mean LH and E1C levels began to increase. However, when a female is removed and paired at 9 mo of age with an unrelated male, elevated levels of LH and E1C may be seen by 10 and 11 mo of age. Our findings indicate that a suppression of fertility occurs in cotton-top tamarins living with their families, but that reproductive suppression does not affect the process of sexual maturation. Both removal from the family environment and stimulation by an unrelated male tamarin were necessary to induce normal reproductive activity. An acceleration of puberty occurred when a female tamarin was removed from her family early in development and paired with a male.     

The effects of social status on food-associated calling behaviour in captive cotton-top tamarins

We examined the effects of social environment on food-asociated calling of cotton-top tamarins, Saguinus oedipus, in two experiments. In experiment 1, we compared the food-associated calling behaviour of six juvenile tamarins living in their natal groups with their calling behaviour 9 months after being removed from family groups and paired. In experiment 2, we studied food-associated calling behaviour of nine cotton-top tamarins immediately before and after removal from their natal groups and pairing. The tamarins underwent three separate developmental processes in their calling behaviour. Animals removed from their natal groups showed an immediate reduction in vocalizations other than food-associated calls (C and D chirps). The development of precise adult forms of C and D chirps was more gradual and was a function of time since removal from their natal group rather than time since pairing. Finally, the postremoval tamarins persisted in applying C chirps to nonfood objects and showed no correlation between C-chirp rate and food preference, which is typical of immature tamarins. We conclude that social status plays an important role in the development of adult forms and usage of food-associated calls. Copyright 1999 The Association for the Study of Animal Behaviour.     

Neonatal and pubertal development in males of a cooperatively breeding primate, the cotton-top tamarin (Saguinus oedipus oedipus).

In cooperatively breeding groups of mammals, reproduction is usually restricted to a small number of individuals within the social group. Sexual development of mammals can be affected by social environment, but we know little regarding effects of the cooperative-breeding system on males. Cotton-top tamarin (Saguinus oedipus oedipus) offspring typically do not reproduce in their natal group, even though they may be physically mature. We examined neonatal and pubertal development in captive male cotton-top tamarins as an example of reproductive development within a cooperative-breeding system and to compare cotton-top tamarins with the general primate model. Puberty was characterized using both hormonal and physical measures. Data were collected on urinary levels of LH, testosterone (T), dihydrotestosterone (DHT), cortisol, and the ratio of DHT to T; testicular development; body weight; and breeding age. We determined that 1) pubertal LH secretion began at Week 37, 2) a surge of T secretion followed at Weeks 41-44, and 3) an increase in the metabolism of T to DHT may have occurred at an average age of 48.6 wk. Most of the rapid weight gain was completed by Week 24, before hormonal increases and rapid scrotal growth. We concluded that rapid pubertal testicular growth in captive cotton-top males was completed by an average 76 wk, but that completion of the individual pubertal spurt can occur between 56 and 122 wk. In a cooperative-breeding system, the opportunity for successful reproduction is dictated by the social environment, but we found no evidence that male offspring were developmentally suppressed in their natal social groups. Our findings suggest that puberty in male New World callitrichid primates occurs more quickly than puberty in Old World primates, even though both have similar patterns of development.     

Relationship between social interactions and sexual maturation in female Saguinus oedipus oedipus

4 female Saguinus oedipus oedipus were paired with strange, unrelated males while 5 remained in their natal family groups. A comparison of the frequency of selected social interactions involving these females when sexually immature versus mature was made. The frequency of sexual and affiliative interactions in male-female pairs was basically unchanged by the female's maturation. Mother-daughter interactions were also not changed in a consistent fashion by the daughters' maturation. Females with strange, unrelated males, either alone or as part of their natal group, displayed increases in marking behavior in association with sexual maturation.     

The stimulatory effect of males on the initiation but not the maintenance of ovarian cycling in cotton-top tamarins (Saguinus oedipus)

Prior studies have shown that female cotton-top tamarins usually do not ovulate while living with natal groups, and most females do not ovulate until they are paired with an unfamiliar adult male. To examine the role of unfamiliar adult males on stimulating ovarian function, four cotton-top females were studied during three conditions: females living with their natal group for six weeks, living alone but exposed to a single unfamiliar adult male located 15 cm away from the female's cage for four weeks, and living with an unfamiliar adult male for six weeks. Behavior and urinary hormonal concentrations were measured during the three conditions. Exposure to the male consisted of visual, auditory, and airborne olfactory contact. First ovulation occurred during exposure to the unfamiliar male in three of the four females indicating that direct physical or sexual contact with the male is not required for onset of ovarian cycling. The fourth female did not ovulate even during six weeks of direct contact with the unfamiliar adult male. In addition, four parous females in either family groups (3) or singly caged (1) were examined for ovarian function 4–6 months after the death or removal of their mates. All femals continued to cycle in the absence of the male indicating that the male was not needed to continue ovarian cycling. In fact, two of the females were pregnant at the time their males died and both delivered normal infants and resumed cycling. The results of this study indicate that an unfamiliar adult male may facilitate the onset of ovarian cycling without being in direct contact with the female and visual, auditory, or airborne olfactory cues may be involved. Once repeated ovarian cycling occurs the male is not required to maintain ovarian function.     

Do cavity‐nesting primates reduce scent marking before retirement to avoid attracting predators to sleeping sites?

The largest population of endangered golden lion tamarins (Leontopithecus rosalia, GLTs) decreased from approximately 330 to 220 individuals between 1995 and 2000 due to a dramatic increase in predation at sleeping sites. We used behavioral data from eight social groups in this population to test two hypotheses: First, if GLTs attempt to mitigate the risk of predation at sleeping sites, they should reduce their rates of scent marking just prior to retirement. Second, if the benefits of scent marking prior to entering the sleeping site merit an increase in the rate of marking, then tamarins should increase their rate of pre-retirement scent marking during the breeding season, when such behavior would have its greatest impact on reproductive fitness. We used a generalized linear model (GLM) repeated-measures analysis to compare rates of daytime scent marking with rates of marking just prior to retirement for males and females. In addition, we compared scent marking prior to retiring in the nonbreeding season to marking rates before retirement in the breeding season for males and both sexes considered concurrently. Contrary to our expectations, GLTs significantly increased their rates of scent marking during the 30 min prior to entering their sleeping site-an observation driven by an increase in male (but not female) rates of marking. Rates of marking before entering the sleeping site were greater in the nonbreeding season compared to the breeding season, when both sexes were considered concomitantly and when males were evaluated alone. We conclude that GLTs do not attempt to minimize predation risk by decreasing scent marking in the period before they enter their sleeping site, and that tamarins do not scent mark at this time of day in order to transmit information about reproductive status or to control reproduction of subordinates. We speculate that scent marking in the 30 min prior to entering sleeping sites may serve to reduce predation risk by enabling tamarin groups to return quickly to favored sleeping sites in the evening when crepuscular predators are active.     

Social influences on estrogen excretion and ovarian cyclicity in saddle back tamarins (Saguinus fuscicollis)

The effects of different social living conditions on estrogen excretion and on the ovarian cycle of saddle back tamarins were investigated. Urinary estrogens were monitored as indices of ovarian cyclicity in groups of adult females living under the following experimental conditions: (1) five parous females, each living with an adult castrated male (in one of the females plasma estradiol and progesterone were also measured); (2) five adult daughters living with their families. Each daughter was then removed from her family and paired with a vasectomized male. After pairing, scent marks collected from the family were introduced daily to one of the daughters and her mate. Scent exposure was then discontinued and hormone excretion measured for several weeks. The remaining four daughters were not exposed to family scent. The females living with castrated males showed urinary estrogen cycles of an average length of 17.5 ± 1.0 days. The plasma estrogen cycle was of the same length. The females studied under condition 2 showed low, noncycling estrogen levels while living in their families. They responded to pairing with an increase in the level of urinary estrogens, and four out of five showed regular estrogen cyclicity. The fifth female exposed to family scent marks after pairing also showed an increase in urinary estrogens. However, as long as scent transfer was maintained, no cycle was observed. Estrogen excretion increased again, and cyclicity commenced when scent transfer was discontinued. It is concluded that ovarian estrogen production is suppressed and cyclicity does not occur as long as daughters live in their families. Release from suppression and perhaps stimulation by the male cause a rapid increase in estrogen levels and the onset of cyclicity. Chemical stimuli produced by the family, perhaps particularly by the mother, may be involved in reproductive suppression.     

Cotton-top tamarins (Saguinus (o.) oedipus) in a semi-naturalistic captive colony

To test the prediction that the breeding success of captive cotton-top tamarins (Saguinus (o.) oedipus) could be improved by maintaining them in groups whose size and age-sex composition resembled those of wild groups, data were collated from 6.5 years of records from a breeding colony that otherwise had housing and husbandry procedures similar to those of other successful colonies. Group size and composition in the colony closely resembled those of wild groups, and infant survival was the highest yet reported for the species, with 69% of the 124 infants born reared by their parents to adulthood, and a mean surviving litter size of 1.5 infants. Abortion, stillbirth, and parental neglect of infants were rare. Parity had several effects on reproduction: mean litter size decreased, but percentage infant survival increased; interbirth intervals decreased in length; and seasonality in reproduction was more pronounced for the first four litters born to breeding females than for their subsequent litters, with a birth peak in the spring. Although a spacious and complex physical environment, retention of offspring in their natal families until experience of several sets of infant siblings had been obtained, and non-invasive husbandry and research techniques may all have contributed to the colony's success, it seems possible that the improvement over other colonies is due to the resemblance of group composition to those of wild tamarins.     

Effects of age, sex, and reproductive status on scent marking frequencies in the golden lion tamarin, Leontopithecus rosalia

This study reports on the longitudinal changes in scent marking frequencies of male and female lion tamarins in relation to age, reproductive status, and group composition. Juvenile males and females in family groups and subordinate males in trios (2 males, 1 female) scent marked infrequently. Juvenile females scent marked less than juvenile males and began scent marking later. Adult pair-bonded males and females scent marked with similar frequencies. Females showed scent marking increases during mid-pregnancy, but their scent marking decreased both before and again after parturition. Both males and females exhibited decreases in scent marking while transporting dependent infants.     

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 daughter's 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.     

The role of scent marking in the social communication of wild golden lion tamarins, Leontopithecus rosalia

The role of scent marking in the social communication of mammals is widely variable. One reason for this variation is that the function of scent marking may vary with different ecological and social conditions. The purpose of this study was to test four nonexclusive hypotheses explaining the role of scent-marking frequency in different ecological and social contexts for wild golden lion tamarins. Relative to ecological contexts, we compared scent-marking frequency during seasons of abundant and scarce food resources. Relative to social contexts, we compared scent-marking frequency when groups were isolated and when groups were in the presence of neighbouring groups. We found that the tamarins used scent marking to mark the location of food resources. Additionally, males used scent marking to communicate intrasexual dominance within their groups, while females did not. Our results also indicate that alpha females increased their scent-marking frequency to communicate to members of other groups, while the presence of members of other groups did not elicit a similar response by alpha males. We did not find evidence for a territorial function of scent marking in golden lion tamarins. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour      

Sexual communication between breeding male and female cotton-top tamarins (Saguinus oedipus), and its relationship to infant care

Male cotton-top tamarins have been shown to be responsive to female scent cues of ovulation, and are known to actively participate in infant care during the time when their mates are fertile. We measured urinary androgen levels and glucocorticoids in seven father tamarins for the first month following the birth of infants to determine 1) whether male tamarins showed an androgen response to their mate's postpartum ovulation, 2) when androgens rise relative to ovulation, 3) whether there is a glucocorticoid response, and 4) whether males alter their parenting behavior during their mate's receptive period. All of the males showed a significant increase in urinary androgens prior to the female's postpartum LH peak, which indicated ovulation. The hormonal increase, which included estradiol, occurred 3-7 days prior to the female's LH peak at a time that coincided with the female's follicular period. Corticosterone levels also peaked during that time, but did not correlate with androgen changes. Fathers did not alter their daily infant-carrying patterns relative to the androgen increase or at the time of the mate's LH peak. We conclude that male cotton-top tamarins experience an increase in androgens that coincides with their mate's postpartum ovulation, which ensures optimal fertility. However, this sexual communication does not alter father-infant interactions, which already occur at a high rate in this species.     

Changes in the activity of captive cotton-top tamarins (Saguinus oedipus) over the breeding cycle

The energetic costs of reproduction are likely to be particularly high in the Callitrichidae (marmosets and tamarins), which characteristically produce twin litters. The activity of five captive breeding pairs of cotton-top tamarins (Saguinus oedipus) was investigated for a 6-month period covering the second half of pregnancy and lactation. Breeding males showed few major changes in activity over this period, but breeding females reduced their levels of locomotion during late pregnancy, and during lactation they spent up to twice as much time feeding and foraging as they did during pregnancy. These results support the hypothesis that the costs that callitrichid females incur when reproducing are likely to have been an important factor in the evolution of these species' communal rearing systems.     

Rearing a second generation of cotton-top tamarins (Saguinus oedipus oedipus) in captivity

The average age at first parturition in captive-born female cotton-top tamarins was 31 months. Only 18% of full-term young born were successfully reared by primiparous females, but success increased with parity and 71% of babies born at 4th and 5th pregnancies were raised. 15% of litters were single births, 61% were twins and 24% were triplets. There was a seasonal distribution of births, with a clear peak in the spring months. The average interbirth interval was 294 days.     

Responsiveness of expectant male cotton-top tamarins, Saguinus oedipus, to mate's pregnancy

In the cotton-top tamarin, a primate where paternal care is critical to the survival of the offspring, we found that expectant fathers experienced multiple hormonal changes during their mate's pregnancy. Fathers that had experienced several previous births showed significant changes in urinary estrogens, androgens, prolactin and cortisol in the last 2 months before birth, whereas less-experienced fathers (LEF) did not. The female's midpregnancy rise in glucocorticoids was followed within 1-2 weeks by a peak of cortisol and corticosterone in her paired male in 70% of all males and 100% of all experienced males. Examination of behavioral interactions between the pairs did not reveal changes in rates of interactions between the experienced pairs over pregnancy. However, the less-experienced pairs had significantly higher levels of affiliative and sexual interactions. Therefore, behavioral communication between the pair did not appear to account for the hormonal changes occurring within the experienced fathers (EF). The midpregnancy rise of glucocorticoids in females may stimulate a glucocorticoid response in male tamarins and thereby activate other hormonal changes in males to prepare them for their parenting role.     

Food-sharing in cotton-top tamarins (Saguinus oedipus)

Food-sharing behaviour was observed in 9 captive families of cotton-top tamarins (range 4-14 individuals per group), during meals of fresh fruit. Food was transferred to infants by their parents and older sibs in response to begging, and was also offered to them without prior solicitation. Older, mature, reproductively suppressed individuals shared more than young immature monkeys. Infants in larger families received more food than those in smaller ones, though individuals in smaller families shared more. Transfer to infants increased to a maximum at 12 weeks of age and then declined gradually. At one year of age they no longer received food from others. Food sharing by older siblings is a form of helping behaviour which may increase their inclusive fitness, and benefit parents, both directly, by reducing the costs they incur in rearing young, and indirectly, by increasing the amount of food available to infants.