Sociosexual development,pair bond formation,and mechanisms of fertility suppression in female cotton-top tamarins (Saguinus oedipus oedipus)

The effect of various social environments on sociosexual behavior was examined in six young female cotton-top tamarins (Saguinus oedipus oedipus) and in three established breeding females. Behavioral observations and hormonal samples were collected on young females while they were living with their families, when they were isolated from conspecifics, and after they were paired with an unrelated male. While living with the family, all females showed a suppression of fertility and low frequencies of sociosexual behavior. Following removal from the family, isolated females displayed an increase in rate of scent marking and an increase in hormonal levels. When young females were paired with males, they were exposed to scent secretions from their natal families, from an unfamilar family, and from a control for a total of 24 weeks. After pairing, hormonal levels increased dramatically, and ovarian cyclicity began. An increase in sociosexual behavior and elevated levels of scent marking accompanied this physiological change. Newly paired females had higher rates of affiliative behavior and scent marking than did established breeding females. However, both newly paired and established breeding males were more likely to initiate contact, grooming bouts, and social sniffing than were females. Time to first ovulation was later in females who were exposed to scent secretions from their natal families than it was in those females given a control for the first 8 weeks following pairing. No female conceived during exposure to scent secretions. However, once normal ovarian cycling had begun or a pregnancy was established, exposure to scent secretions had no effect. Thus, the social environment influences the fertility, sociosexual behavior, and pair bond formation of cotton-top tamarins. In addition, chemical stimuli found in the scent secretions produced by the natal family are most likely involved in reproductive suppression.     

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.     

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.     

The Role of Gonadal Steroid Receptor Activation in the Restoration of Sociosexual Behavior in Adult Male Rats

This work tested the hypothesis that gonadal steroid receptor activation was necessary for the restoration of several sociosexual behaviors (such as copulatory behavior, partner preference, 50-kHz vocalizations, and scent marking) in testosterone-treated gonadectomized male rats. Gonadal steroid receptors were blocked by systemic administration of the antiandrogen hydroxyflutamide, the antiestrogen RU 58668, or both antagonists simultaneously in a restoration paradigm. Inhibiting androgen receptors with hydroxyflutamide blocked the restoration of male copulatory behavior, partner preference (time spent with a sexually receptive female over a nonreceptive female), 50-kHz ultrasonic vocalizations, and scent marking. On the other hand, we did not find that blocking estrogen receptors with RU 58668 inhibited the restoration of copulatory behavior or partner preference in testosterone-treated gonadectomized male rats, even though the level of brain nuclear estrogen receptor occupation was significantly reduced to the level found in gonadectomized males. However, the restoration of scent marking and 50-kHz vocalizations were impaired by RU 58668. Blocking both nuclear androgen and estrogen receptors with the two antagonists simultaneously did not have a greater inhibitory effect than treatment with each antagonist alone. Therefore, the activation of nuclear estrogen receptors is necessary for the restoration of some, but not all, sociosexual behaviors, which are also androgen receptor-dependent. Besides nuclear estrogen receptors, there are additional, but unknown, targets of estradiol that play a role in mediating copulatory behavior in adult male rats. Moreover, the signals from multiple gonadal steroid signaling pathways converge in the regulation of some sociosexual behaviors in adult male rats.     

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.     

Behavioral and social correlates of escape from suppression of ovulation in female common marmosets housed with the natal family

Although female common marmosets typically do not breed while housed with their natal families, up to half ovulate at least once while housed with the intact natal family, and a similar proportion conceive if an unrelated adult male is present in the group. In this study, we investigated the behavioral and social correlates of escape from suppression of ovulation by daughters housed in intact natal families or in families in which the father had been replaced by an unrelated adult male. Focal-animal behavioral data were collected from daughters that were (N = 7) or were not (N = 10) undergoing ovulatory cycles while housed with the natal family and from daughters that were (N = 5) or were not (N = 3) cycling or pregnant in families containing an unrelated male. Additionally, four cyclic and six acyclic females housed in intact natal families underwent simulated “prospecting” tests. Cyclic and acyclic daughters in intact natal families did not engage in sexual interactions with the father and showed few differences from one another in their interactions with the parents. Moreover, cyclic and acyclic daughters did not differ in their willingness to leave the family for short periods or to investigate an unfamiliar family in “prospecting” tests. However, daughters that underwent ovarian cycles in the presence of an unrelated male showed numerous behavioral differences from those in intact natal families, including frequent courtship and sexual behaviors with the male, reduced affiliative interactions with the mother, and elevated frequencies of aggressive display behavior. Moreover, these females were less likely to behave submissively towards the mother or the adult male. These findings suggest that both suppression of ovulation and inhibition of sexual behavior normally contribute to reproductive failure in female marmosets living with their natal families, and that the two components of suppression may become dissociated under specific social conditions. Am J Primatol 41:1–21, 1997. © 1997 Wiley-Liss, Inc.     

Chemical communication of reproductive status in female cotton-top tamarins (Saguinus oedipusoedipus)

Among Callitrichids, scent secretions have been identified as carrying information regarding species, subspecies, gender, social status, individuality, hormonal status, and timing of ovulation. We propose that information regarding familiarity and reproductive status is also communicated. Seven male–female pairs of cotton-top tamarins (Saguinus oedipus oedipus) were presented with several drops of distilled water, a scent secretion from the female of that pair, scent secretions from unfamiliar, reproductively mature but noncycling females, and scent secretions from unfamiliar, reproductively cycling females. Behavioral responses from both males and females were recorded over a 10 min period. Differences in behavioral response for both males and females were significant across all four conditions. This indicates that cotton-top tamarins are capable of discriminating a familiar scent from an unfamiliar scent as well as the reproductive status of an unfamiliar female. The communication of this information may play an important role in regulating mate selection, reducing reproductive competition, and stabilizing transfers in and out of groups in the wild. Am. J. Primatol. 45:337–349, 1998. © 1998 Wiley-Liss, Inc.     

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.     

Sex differences in scent marking in Propithecus edwardsi of Ranomafana National Park, Madagascar

In this study we compared the scent-marking rates of females with those of males. Specifically, we examined the ability of season, dominance status, and natal status to explain the frequency of scent marking in female sifakas living wild in Ranomafana National Park, Madagascar, and compared the results with those published for males [Pochron et al., American Journal of Primatology, in press]. We also sought to determine whether vulnerability to infanticide affects marking frequency in adults of either sex, and whether female reproductive status affects female marking behavior. We found that males marked at twice the rate of females, and like males, females in single-female groups marked at the highest rates. Dominant females and non-natal females marked at higher rates than did subordinate females and natal females, a pattern also seen in males. This suggests that scent marks may convey important information about status. Neither females nor males varied their marking frequency with the presence of vulnerable infants. Females did not alter marking frequency with reproductive state, and like males, they marked at higher rates in the period prior to the mating season than they did in the mating season itself. This implies that females may use scent marks more for intrasexual aggression or territoriality than for mate attraction.     

Synchronization of ovarian cycles within and between social groups in golden lion tamarins (Leontopithecus rosalia)

Synchronization of ovarian events has been reported in a number of primate species, with the temporal resolution of synchrony ranging from the occurrence of seasonal breeding within the annual cycle to a close matching of ovarian events within a single ovarian cycle. However, ovarian synchrony has not been reported in a New World primate. The temporal association of ovarian events was examined in female golden lion tamarins (Leontopithecus rosalia) living in the same or different social groups. Ovarian cyclicity was monitored by measuring the excretion of urinary estrogen metabolites. There was a high degree of synchronization in the occurrence of urinary estrogen peaks for females in different social groups (mean peak discrepancy = 2.1 days) and in females housed in the same social group (mean peak discrepancy = 1.3 days). Contrary to previous reports on callitrichid primates, daughters housed in their natal family group exhibited cyclic patterns of urinary estrogen excretion. These findings represent the first explicit demonstration of ovarian synchrony in a New World primate, and the tight coupling of ovarian cycles in female tamarins resembles the nature of menstrual synchrony in human females.     

The reproductive status of nonbreeding group members in captive golden lion tamarin social groups

Reproductive activity is limited to only one female in many species of callitrichid primates (marmosets and tamarins): daughters and subordinate females do not produce offspring. A suppression of ovulatory cyclicity is responsible for the lack of reproductive activity in three species of callitrichids studied to date. This study evaluated the endocrine status of golden lion tamarins (Leontopithecus rosalia) housed as daughters or sons in family groups and of individuals housed in isosexual peer groups. Daughters 17 months of age and older and a subordinate female had high levels of estrogen excretion. Mean levels of estrogen excretion in these females were similar to those of nonpregnant, breeding adult females (17.14 ± 6.82 versus 11.93 ± 6.33 μg/mg creatinine, respectively). Estrogen profiles were similar to those of breeding adult females, with sinusoidal cycles in estrogen excretion. Younger daughters in family groups (10 and 12 months old) showed markedly lower levels of estrogen excretion (0.84 ± 0.58 μg/mg creatinine). Estrogen profiles lacked the sinusoidal nature of cycles in older daughters and breeding females, and elevations in estrogen excretion occurred frequently and remained elevated for 1 or 2 days. Plasma testosterone levels in males varied widely, but mean concentrations did not differ among males housed in different social conditions. These results suggest that older daughters and subordinate females may be capable of expressing normal ovarian function in the presence of a breeding adult female. This finding may account for two unusual observations in the lion tamarin: the high level of female-female aggression and the presence of groups in the wild with more than one actively breeding female.     

Scent marking in two western Amazonian populations of woolly monkeys (Lagothrix lagotricha)

We describe patterns of scent marking observed in two wild populations of lowland woolly monkeys that were the subjects of long-term studies in the westernmost portion of the Amazon basin. The woolly monkeys engaged primarily in two types of scent marking: chest rubbing and anogenital rubbing. In both study populations, males and females performed both types of scent marking, but males chest-rubbed more commonly than females, while females engaged in more anogenital rubbing. We evaluated two nonexclusive hypotheses for the function of scent marking by woolly monkeys: 1) that scent marking is used in sociosexual contexts, and 2) that scent marking is used to convey information about occupancy of or willingness to defend an area from conspecifics in other social groups. We found no association between the occurrence of scent-marking behavior and location within the home range, but did find that scent marking occurred more commonly than expected on days when copulations, mating solicitations, and intergroup encounters were observed. Additionally, mating activity and chest rubbing were highly correlated across the yearly cycle, even when the potentially confounding variable of ripe fruit availability was controlled for. In woolly monkeys, overt male-male competition is rare and female choice is an important part of the mating system. Our results are most consistent with the idea that scent marking plays a role in advertising male quality or competitive ability, and perhaps in coordinating mating activity.     

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.     

Scent-marking behaviour of the honey badger, Mellivora capensis (Mustelidae), in the southern Kalahari

We investigated sexual and seasonal patterns in scent-marking behaviour of the honey badger, by direct observations of habituated individuals (five females, four adult males, two young males). Four categories of scent-marking behaviour were identified: (1) scent marking at latrines; (2) token urination in holes along the foraging path; (3) squat marking at single-use sites; and (4) functional excretion. Females and young males used all four types of scent marking, but adult males were not observed to use token urination. A strategy of hinterland scent marking was used, as was predicted from the large home ranges of both male and female honey badgers. There were significant sexual differences in marking rate: adult males primarily used latrines and adult females favoured token urination. Latrine scent marking in adult male honey badgers provides support for the ‘scent-matching’ hypothesis. Females visited latrines when they were in oestrus. However, the low level of marking activity during a visit and the intensive smelling suggested a scent-matching function rather than reproductive advertisement. Token urination appeared to be related to the maintenance of spatiotemporal separation in females, although we also observed token urination in young males. While the placement of urine in foraging holes and its relation with successful digging attempts offer some support for the foraging efficiency hypothesis, we consider this unlikely, because we did not observe it in adult males and there was no seasonal pattern. Squat marking occurred under a wide range of conditions in both males and females and may be related to marking valuable resources. It is likely that scent marking in honey badgers has many functions.     

The effects of gonadal hormones on scent marking and related behavior and morphology in female gray short-tailed opossums (Monodelphis domestica)

The hormonal control of scent marking and related behavior and morphology was examined in female gray short-tailed opossums. Females rarely scent marked when intact or following ovariectomy. Testosterone (T) but not estradiol (E) treatment stimulated chest marking while either hormone stimulated head marking in ovariectomized females tested alone. When the same females were tested with males, T-treated females showed little scent marking of any type; E-treated females showed hip marking in significantly more tests than females in the other treatment groups. Suprasternal scent glands (absent in intact females) and phalluses of females that received T were significantly larger than those of animals that received E or control animals. These findings are discussed with respect to similarities and differences between marsupial and eutherian females and between male and female gray opossums in the hormonal control of sexually dimorphic behavior and morphology.     

Effects of prepubertal ovariectomy on the development of scent glands, scent marking, and aggressive behaviors of female tamarin monkeys (Saguinus fuscicollis)

The effects of prepubertal ovariectomy on scent gland development, scent marking behavior, and on social interactions with strange adult conspecifics were studied in adult females cohabiting with intact males. Eight females were ovariectomized and eight underwent control surgery at 6 months of age. All were returned to their families after surgery and allowed to reach sexual maturity. At 18 months of age, each female was permanently paired with an adult, intact male. When the subjects were 21 months old, the social interactions of all pairs with strange adults were tested in a situation analogous to a territorial encounter. The scent marking activities of the subjects and their mates were studied during “territorial encounters,” in trial-free control situations, and in the presence of novel objects. Ovariectomy prior to puberty retarded the development of the scent gland but did not inhibit it completely. Social interactions with strange conspecifics were also affected. Ovariectomized females showed fewer threat displays than did control females, but there was no significant difference in the amount of injurious aggression both female groups directed at the strangers. Under all testing conditions, ovariectomized females tended to scent mark less frequently with the circumgenital-suprapubic gland than did controls. This difference was statistically significant only under some of the testing conditions. Intact females scent marked more frequently than their males but ovariectomized females did so only under trial-free testing conditions. The sternal scent gland was used very infrequently by all subjects and there was no difference in marking activity between males and females or between ovariectomized and control females.     

Age-related changes on marking, marking-like behavior and the scent gland in adult Mongolian gerbils (Meriones unguiculatus).

Marking behavior, marking-like behavior [3], and changes of the scent glands were observed in aged Mongolian gerbils. In Experiment 1, changes in the marking and marking-like behavior with aging were evaluated in adult male and female Mongolian gerbils of an inbred strain aged 6 to 36 months. The frequency of marking behavior in males was significantly higher than females throughout the observation period except at 36 months of age. On the other hand, frequency of marking-like behavior in males, but not in females decreased with aging, significantly. In Experiment 2, changes of the scent gland in adult males and females aged 6 to 36 months were morphologically evaluated. Macroscopic examination revealed an increase in the size length and width of the glands of males aged 12 months and females aged 6 months. Histologically the glands of all the males and females aged 6 months developed moderately or well. Some of the 12-month-old males and females showed acinar atrophy of the glands, and all the females aged 18 months or more had highly atrophied scent glands. From these results, we concluded that there is no relationship between the changes of marking behavior and those of the scent glands in aged male Mongolian gerbils, and assume that marking behavior in aged animals does not have an important meaning as marking. In Experiment 3, marking and marking-like behavior in castrated adult Mongolian gerbils aged 16 weeks were observed. The result showed that marking behavior, not marking-like behavior was inhibited after castration. From these findings, we consider that generally marking behavior in Mongolian gerbils consists of androgen-dependent marking behavior and androgen-independent marking behavior (marking-like behavior).     

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.     

Social and reproductive conditions modulate urinary cortisol excretion in black tufted-ear marmosets (Callithrix kuhli)

The links between psychosocial stress, social status, reproductive function, and urinary cortisol were assessed in social groups of black tufted-ear marmosets (Callithrix kuhli). Urinary cortisol excretion was monitored in cases of intrafamily conflict (“sibling fights”) and in daughters in four distinct social contexts: in the family group, while housed singly or in same-sex pairs, and while paired with a male pairmate. Cortisol excretion was elevated in participants in intra-family conflict on the day of and the day following the conflict, relative to concentrations a week prior to or following the conflict. Daughters in natal family groups had concentrations of cortisol that did not differ from reproductively active adult females. This finding held for daughters who were either anovulatory or undergoing ovulatory cycles while in the natal family group. Natal family members and male pairmates exerted buffering effects on levels of activity in the hypothalamic pituitary adrenal axis (HPA) in female C. kuhli. Placing females in solitary housing led to significantly increased cortisol excretion. In the 2 months subsequent to pairing with a male partner, excreted cortisol concentrations in females declined significantly. Daughters removed from their natal family group and housed with a sister did not exhibit increased cortisol levels. These data reveal that activity in the (HPA) axis in marmosets is sensitive to psychosocial stressors, and that urinary cortisol can provide a useful quantitative measure of HPA reactivity. As in other callitrichids, delayed breeding in daughters and reproductive anomalies in C. kuhli appear to be mediated by mechanisms other than elevated HPA activity. Am. J. Primatol. 42:253–267, 1997. © 1997 Wiley-Liss, Inc.     

Lack of effects of castration on scent marking, displays, and aggression in a South American primate (Saguinus fuscicollis).

The social interactions of 12 adult, permanently cohabiting male-female pairs with strange conspecifics were studied before and after the male of each pair was either castrated or underwent control surgery. Prior to surgery, the pairs directed a relatively high amount of injurious aggression and displays toward the stranger. Aggression, display behavior, and scent marking tended to be more frequent in females. Moreover, female strangers received more aggression than male strangers, particularly by female subjects. Castration of the males did not result in a decrease in aggression, display behavior, and scent marking. On the contrary, the agression scores of all subjects tended to be higher after surgery, an increase which was probably caused by extraexperimental variables.