Female Common Marmosets Research Articles

Reproductive skew and the threat of eviction: a new perspective

Most recent models of the partitioning of reproduction attempt to explain patterns of skew on the assumption that dominant individuals have complete control over breeding opportunities within the group, but may nevertheless concede a share of direct reproduction to subordinates as an incentive to remain peacefully in the association. Although these models may be applicable to some animal societies, we argue that they fail to provide a comprehensive theory of skew. Instead, we suggest that subordinates may often be able to claim unsanctioned reproduction for themselves, but will be forced to exercise a degree of reproductive restraint lest they incite ejection by the dominant. Reproductive skew, in other words, may reflect the threat of ejection (inducing subordinate restraint) rather than the threat of subordinate departure (inducing reproductive concessions by dominants). We present a simple ESS model of reproductive skew under these circumstances, which demonstrates that a shift in emphasis from reproductive concessions by dominants to reproductive restraint on the part of subordinates, radically alters the predictions of skew models. High group productivity, high relatedness and (when group members are related) strong ecological constraints are all expected to lead to reduced skew (the opposite conclusions to those of previous, concession-based analyses). The reason is that these factors reduce the benefits (or increase the costs) of ejection to the dominant, who therefore does best to tolerate more subordinate reproduction.

Efficacy and effects of short- and medium-term contraception in the common marmoset (Callithrix jacchus) using melengestrol acetate implants.

This study examines the effect of melengestrol acetate (MGA) implants on reproductive function and various biochemical parameters, ovarian activity, and uterine morphology in ten female common marmosets implanted for either 6-8 or 19-21 months. Measures of body weight, concentrations of urinary glucose and blood liver enzymes were taken. Ovarian activity was assessed by analysis of urinary progestin levels and ultrasound examinations of the ovaries. Ultrasonography was also used to evaluate uterine morphology. MGA was highly effective in preventing pregnancies in the study animals. No changes in biochemical parameters were found; however, seven females developed a substantial weight gain during the study. Follicular development was not suppressed, as indicated by the presence of antral follicles, luteinized structures, and elevated urinary progestin levels. The uteri of the MGA-treated subjects were moderately enlarged with a thickened endometrium that showed a marked change in structural appearance indicative of hypertrophy and decidualization. After implant removal these changes quickly disappeared and all females ovulated within 3 weeks and conceived within 4 months post-treatment. MGA appears to be an acceptable contraceptive in the marmoset, although non-steroidal methods should be evaluated as possible potential alternatives.

Ingestion of calcium solutions by common marmosets (Callithrix jacchus).

Callithrix jacchus, the common marmoset, is a small New World primate that feeds on insects, fruit, and gum, and has a high reproductive rate for a primate. Insects are generally a poor source of dietary calcium, while gums may contain significant levels of calcium. Their high reproductive rate also suggests that reproductive female C. jacchus might be susceptible to calcium deficiency. Thus, we hypothesized that common marmosets might find solutions containing calcium to be palatable. We used choice experiments to examine this phenomenon in 14 male and 19 female common marmosets. Animals were presented with identical water bottles containing either deionized water or a calcium lactate solution (either 2% or 4% calcium lactate by weight) and intake was measured. Serum 25-OH-vitamin D was monitored in a subset of the animals in the experiment to examine the role of vitamin D in this behavior. Our results demonstrated that C. jacchus can distinguish between plain water and a calcium lactate solution, and that in general they prefer calcium solutions. Although animals with marginal vitamin D status did have strong preferences for calcium solutions, they did not ingest significantly more of the calcium solutions than animals that were vitamin D-replete. Nulliparous females and males did not differ in the amounts of calcium solutions ingested. Lactating females ingested the greatest volume of the calcium solutions.

Unusual case of metabolic bone disease in a common marmoset (Callithrix jacchus)

Metabolic bone disease was diagnosed in an 11-month-old female common marmoset (Callithrix jacchus). It was depressed, reluctant to move, and was cachectic and small for its age. Laboratory findings included...

Suppression of Cortisol Levels in Subordinate Female Marmosets: Reproductive and Social Contributions

Socially subordinate female common marmosets (Callithrix jacchus) have markedly lower plasma cortisol levels than dominant females. Subordinate females also undergo hypoestrogenemic anovulation, and estrogen can elevate glucocorticoid levels. Therefore, we previously hypothesized that this cortisol difference is mediated by rank-related differences in reproductive hormones, probably estradiol. To test this possibility, we characterized the effects of the ovarian cycle and ovariectomy on plasma cortisol concentrations. Beginning in the early follicular phase, basal blood samples were collected from seven cycling female marmosets daily for 16 days and at 2- to 3-day intervals for another 16 days. Samples were collected identically from seven anovulatory subordinate females and seven long-term ovariectomized females. Cortisol levels changed reliably across the ovarian cycle, with levels in the mid- to late follicular, peri-ovulatory, and early luteal phases higher than those in the remainder of the cycle. Cortisol levels of cycling females were significantly higher than those of subordinates at all parts of the cycle, but were significantly higher than those of ovariectomized females only during the midcycle elevation. Unexpectedly, subordinates had significantly lower cortisol levels than ovariectomized females, as well as higher estradiol and estrone levels and lower progesterone and luteinizing hormone (LH) levels. These results confirm that circulating cortisol concentrations are modulated by reproductive function in female marmosets but also indicate that low cortisol levels in subordinate females cannot be attributed simply to hypoestrogenemia. Instead, other factors, such as direct effects of social subordination or suppression of LH levels, contribute to suppression of cortisol in subordinates.

Diurnal variation on the excretion patterns of fecal steroids in common marmoset (Callithrix jacchus) females.

The use of fecal steroid analysis to assess gonadal and adrenal function in primates has rapidly increased in recent years due to the ability to collect feces from nonhuman primates living in wild conditions. These techniques offer an exciting new potential for enhancing our knowledge of the endocrine status of free-living animals. Prior to using these techniques under field conditions, it is important to determine the diurnal variation of fecal excreted steroids for assessing possible time limitations on fecal collections. The following study investigates the diurnal frequency of defecation and patterns of steroid levels excreted in feces from four female common marmosets, Callithrix jacchus, living in a family group. These females represented three reproductive conditions: early pregnancy, ovarian cycling, and noncycling (postpubertal). Cortisol, estradiol, and progesterone were extracted and analyzed by enzyme immunoassay. Diurnal variations in steroid levels were found by ANOVA for cortisol and progesterone but not for estradiol. Significantly higher levels of cortisol were found in the afternoon, while the reverse was found for progesterone. All females showed the same pattern of steroid level change, except for cortisol in the pregnant female. Since all females defecated within the first hour after they awoke in the morning, this time was determined to be the most effective time to collect feces. The consistency of our findings reinforces the usefulness of this approach for studying reproductive and adrenocortical function in marmosets and also indicates that fecal collection should be limited to either morning or afternoon collections.

Behavioral discrimination between circumgenital odor from peri-ovulatory dominant and anovulatory female common marmosets (Callithrix jacchus).

Social peer groups of callitrichid monkeys [marmosets and tamarins] exhibit intrasexual dominance hierarchies in captivity. This laboratory study employed two-choice behavioral discrimination bioassys to test the hypothesis that scent from female common marmosets contains chemical cues that permit discrimination between dominant females in the periovulatory versus luteal phase of the ovarian cycle and females holding dominant versus subordinate status. When scent from only dominant females was presented, marmosets directed significantly greater amounts of investigatory behavior toward peri-ovulatory scent versus scent collected during the luteal phase of the ovarian cycle. Animals of both sexes demonstrated significant discriminatory behavior between scent deposited by dominant versus subordinate females, but only when the dominant female was in the peri-ovulatory phase of the ovarian cycle. Test animals directed equal amounts of investigative behavior toward scent from luteal-phase dominant females and subordinate females. Female test subjects deposited significantly more scent marks over presented scents than did male subjects, particularly when the scent had been donated by a peri-ovulatory female. Chemical odors specific to the periovulatory and luteal phases of the ovarian cycle may play a role in mediating behavioral interactions among marmosets.

Diurnal variation on the excretion patterns of fecal steroids in common marmoset (Callithrix jacchus) females

The use of fecal steroid analysis to assess gonadal and adrenal function in primates has rapidly increased in recent years due to the ability to collect feces from nonhuman primates living in wild conditions. These techniques offer an exciting new potential for enhancing our knowledge of the endocrine status of free-living animals. Prior to using these techniques under field conditions, it is important to determine the diurnal variation of fecal excreted steroids for assessing possible time limitations on fecal collections. The following study investigates the diurnal frequency of defecation and patterns of steroid levels excreted in feces from four female common marmosets, Callithrix jacchus, living in a family group. These females represented three reproductive conditions: early pregnancy, ovarian cycling, and noncycling (postpubertal). Cortisol, estradiol, and progesterone were extracted and analyzed by enzyme immunoassay. Diurnal variations in steroid levels were found by ANOVA for cortisol and progesterone but not for estradiol. Significantly higher levels of cortisol were found in the afternoon, while the reverse was found for progesterone. All females showed the same pattern of steroid level change, except for cortisol in the pregnant female. Since all females defecated within the first hour after they awoke in the morning, this time was determined to be the most effective time to collect feces. The consistency of our findings reinforces the usefulness of this approach for studying reproductive and adrenocortical function in marmosets and also indicates that fecal collection should be limited to either morning or afternoon collections.

Diurnal variation on the excretion patterns of fecal steroids in common marmoset (Callithrix jacchus) females

The use of fecal steroid analysis to assess gonadal and adrenal function in primates has rapidly increased in recent years due to the ability to collect feces from nonhuman primates living in wild conditions. These techniques offer an exciting new potential for enhancing our knowledge of the endocrine status of free-living animals. Prior to using these techniques under field conditions, it is important to determine the diurnal variation of fecal excreted steroids for assessing possible time limitations on fecal collections. The following study investigates the diurnal frequency of defecation and patterns of steroid levels excreted in feces from four female common marmosets, Callithrix jacchus, living in a family group. These females represented three reproductive conditions: early pregnancy, ovarian cycling, and noncycling (postpubertal). Cortisol, estradiol, and progesterone were extracted and analyzed by enzyme immunoassay. Diurnal variations in steroid levels were found by ANOVA for cortisol and progesterone but not for estradiol. Significantly higher levels of cortisol were found in the afternoon, while the reverse was found for progesterone. All females showed the same pattern of steroid level change, except for cortisol in the pregnant female. Since all females defecated within the first hour after they awoke in the morning, this time was determined to be the most effective time to collect feces. The consistency of our findings reinforces the usefulness of this approach for studying reproductive and adrenocortical function in marmosets and also indicates that fecal collection should be limited to either morning or afternoon collections. Am. J. Primatol. 46:105–117, 1998. © 1998 Wiley-Liss, Inc.

Behavioral discrimination between circumgenital odor from peri‐ovulatory dominant and anovulatory female common marmosets (Callithrix jacchus)

Social peer groups of callitrichid monkeys [marmosets and tamarins] exhibit intrasexual dominance hierarchies in captivity. This laboratory study employed two-choice behavioral discrimination bioassys to test the hypothesis that scent from female common marmosets contains chemical cues that permit discrimination between dominant females in the peri-ovulatory versus luteal phase of the ovarian cycle and females holding dominant versus subordinate status. When scent from only dominant females was presented, marmosets directed significantly greater amounts of investigatory behavior toward peri-ovulatory scent versus scent collected during the luteal phase of the ovarian cycle. Animals of both sexes demonstrated significant discriminatory behavior between scent deposited by dominant versus subordinate females, but only when the dominant female was in the peri-ovulatory phase of the ovarian cycle. Test animals directed equal amounts of investigative behavior toward scent from luteal-phase dominant females and subordinate females. Female test subjects deposited significantly more scent marks over presented scents than did male subjects, particularly when the scent had been donated by a peri-ovulatory female. Chemical odors specific to the peri-ovulatory and luteal phases of the ovarian cycle may play a role in mediating behavioral interactions among marmosets. Am. J. Primatol. 46:265–284, 1998. © 1998 Wiley-Liss, Inc.

Vasopressin and oxytocin immunoreactive neurons and fibers in the forebrain of male and female common marmosets (Callithrix jacchus)

Vasopressin (AVP) and oxytocin (OT) immunoreactive (ir) neurons and fibers were examined in the forebrain of male and female common marmosets (Callithrix jacchus). As expected from previous studies of cell distribution in the rodent and primate brain, AVP-ir cells were most evident in the paraventricularis, supraopticus, and suprachiasmaticus of the hypothalamus. AVP-ir cells were also widely distributed in the lateral hypothalamus and the bed nucleus of the stria terminalis. A sexually dimorphic pattern of AVP-ir cells was found in the bed nucleus of the stria terminalis, in which males had more AVP-ir cells than females. OT-ir cells were found in the paraventricularis and supraopticus of the hypothalamus as well as in the bed nucleus of the stria terminalis and the medial amygdala. Male and female marmosets did not differ in the distribution of OT-ir cells. Fibers for both AVP and OT were evident outside of the hypothalamic-neurohypophyseal tract, but a plexus of AVP-ir fibers in the lateral septum or lateral habenular nucleus, as seen in the rat brain, could not be detected for either peptide.

Vasopressin and oxytocin immunoreactive neurons and fibers in the forebrain of male and female common marmosets (Callithrix jacchus)

Vasopressin and oxytocin immunoreactive neurons and fibers in the forebrain of male and female common marmosets (Callithrix jacchus)

The pair-bond formation and its role in the stimulation of reproductive function in female common marmosets (Callithrix jacchus)

The sociosexual relationship between male and female common marmosets (Callithrix jacchus) is characterized by pair-bond formation, which includes sexual and social interactions such as contact, huddling and allogrooming. The formation of heterosexual pairs in captivity sometimes is unsuccessful in terms of reproduction. We investigated the existence of a correlation between characteristics of sociosexual interaction of marmoset pairs and its role in stimulating reproductive function in females. We studied pair-bond formation during the first 10 weeks of pairing in eight unrelated heterosexual pairs of common marmosets (Callithrix jacchus) without prior sexual experience. In three of them, pregnancy occurred during the study period (group SR), and we compared the profile of their sociosexual interactions with that of the five other couples in which pregnancy was not registered (group NS) during that period. The results show differences between the two groups, related mainly to affiliative responses between male and female, with significantly higher levels of allogrooming and simultaneous piloerection in the SR group. Although we did not find significant differences in the frequency of mounting behavior between groups, their reproductive success was different, suggesting that some behavioral patterns related to cooperative interactions between the male and female could be expressing the pair-bond. These behaviors may be influencing the females' physiology and consequently successful reproduction in the species.

Escape from social suppression of sexual behavior and of ovulation in female common marmosets.

In cooperatively breeding species, socially subordinate animals typically curtail their reproductive efforts and help to rear the offspring of the dominant individuals. This reproductive inhibition can be mediated by social suppression of reproductive physiology andor sexual behavior and is thought to be triggered by behavioral or sensory cues from the dominant animals. Such social suppression of reproduction is exemplified by the common marmoset (Callithrix jacchus), a small, coooperatively breeding New World monkey that usually gives birth to dizygotic twins. Most social groups of this species contain only a single, dominant, breeding female; subordinate females usually fail to ovulate and do not engage in sexual beha~ior.'-~ However, reproductive suppression appears to be highly variable: subordinate females occasionally o v ~ l a t e , ~ . ~ and wild groups have been reported to contain two breeding females5 To clarify the proximate causes of variation in the occurrence of reproductive suppression, we characterized the ovulatory activity of female common marmosets housed in either intact natal families (n = 41) or families into which an unrelated adult male had been introduced (n = 13) following the death of the father when the daughters were 1011 months old (prepubertal) or following the experimental removal of the father when the daughters were 18-21 months old (postpubertal). Blood samples were collected twice weekly and assayed for plasma progesterone (P) by enzymeimmunoassay. Ovulation was considered to have occurred on the day preceding a sustained elevation of P above 10 nglml, and pregnancies were identified from P profiles and abdominal palpation and were confirmed by ~ltrasonography.~ To characterize the behavioral correlates of escape from reproductive suppression, we collected a total of 4 hours of focal-animal behavioral data from each of 17 daughters in intact natal families and 8 daughters in families containing an unrelated male.7 Ovarian activity ranged from anovulation to isolated ovulatory cycles to regular, repeated cycles. In intact natal families, 46.3% of daughters (19 of 41) ovulated at

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.

Familial influences on ovulatory function in common marmosets (Callithrix jacchus).

Previous studies have indicated that many, but not all, female common marmosets (Callithrix jacchus) housed with their natal families undergo social suppression of ovulation. In this study, we further characterized ovulatory activity in common marmoset daughters to determine the prevalence of social suppression of ovulation and to elucidate familial influences on daughters' ovarian activity. Blood samples were collected twice weekly from each of 46 daughters for 5-12 months, usually beginning when the daughters were 12 months of age. Plasma progesterone concentrations indicated that 46.3% of daughters in intact natal families ovulated at least once, with the age at first ovulation averaging 17.2 months; however, none of these daughters became pregnant. Daughters' ovulatory cycles showed several significant differences from those of older females housed with unrelated adults, including longer periods between successive luteal phases, shorter luteal phases, and lower peak and mean luteal-phase progesterone levels. Daughters were significantly more likely to ovulate in families in which the mother was experimentally prevented from sustaining pregnancies, and in families in which the father had been replaced by an unrelated adult male and when the daughter was approximately 10-11 months of age. Daughters in families containing an older sister never ovulated; in contrast, those with a female littermate were not less likely to ovulate than were other daughters, but had more sporadic ovarian cycles and significantly lower mean luteal-phase progesterone levels. These results confirm and extend previous findings that up to half of female common marmosets may ovulate while housed with the natal family but that virtually none sustain pregnancies, suggesting that suppression of ovulation is only one of several components of reproductive failure. Furthermore, these results demonstrate that daughters' likelihood of ovulating, as well as the endocrine profiles of their ovulatory cycles, can be modulated by numerous social influences within the family.

Behavioural and endocrine predictors of dominance and tolerance in female common marmosets, Callithrix jacchus

As a result of social subordination, female common marmosets undergo suppression of ovulation and inhibition of sexual behaviour. This study examined the possibility that subordination also results in decreased aggressiveness and increased submissiveness towards same-sex strangers. Thirty-two adult females were pre-assigned to eight mixed-sex social groups. The females' behavioural and adrenocortical responses to brief confrontations with each of three female strangers were assessed under two conditions: while subjects were pair-housed with a male and while they were living in established, mixed-sex groups. Only 22% of subjects threatened stimulus females in the heterosexual pairs condition, 47% submitted and 31% showed no agonism. These agonistic behaviour patterns reliably predicted whether a female would become dominant or subordinate in a mixed-sex group. When animals were housed in established social groups, both dominant and subordinate females either showed similar responses to stimulus animals as they did in the earlier condition or became somewhat less responsive. Plasma cortisol levels did not correlate with agonistic behaviour and were not elevated by stranger-encounter testing. Finally, in the first 10 days following group formation, subordinate females that had shown ovulatory cyclicity prior to group formation were significantly more likely to receive persistent aggression from their dominant female groupmate than subordinates that had been anovulatory. These results suggest that attainment of social status between female marmosets is closely related to pre-existing individual differences in agonistic behaviour, whereas tolerance between females depends upon ovarian function.

Specular microscopy of the corneal endothelial cells in common marmosets.

The corneal endothelia of 12 female common marmosets (age: 12-18 months) were examined with a contact-type specular microscope under general anesthesia. The specular microscopy showed uniform-sized, hexagonal endothelia arranged regularly on the innermost layer of the cornea. The endothelial plane was smooth; however, it occasionally had irregular undulation or parallel folds. The cell density (cells/mm2) in common marmosets was similar to that in cynomolgus monkeys.

Metabolism of reproductive steroids during the ovarian cycle in two species of callitrichids, Saguinus oedipus and Callithrix jacchus, and estimation of the ovulatory period from fecal steroids.

Gonadal steroids were measured in daily fecal samples providing comparative data on steroid metabolism in two genera of New World primates. Circulating bioactive LH and progesterone concentrations and fecal progesterone, pregnanediol, estradiol, and estrone concentrations were measured by collecting blood and daily fecal samples from four captive common marmoset females and four cotton-top tamarin females for 30 days. High recoveries (> 80%) of labeled steroids that were added directly to the feces before extraction were recovered from feces of both species. Because of the presence of complex steroid conjugates, only one fifth the amount of estradiol was measured without solvolysis as compared to the amount measured with solvolysis. In tamarins, steroids were metabolized rapidly, with all postovulatory increases occurring within two days after the circulating LH peak (an increase of 2 SD higher than mean follicular levels). In marmosets, steroid excretion was slower; increased steroid levels occurred 2-4 days after the LH peak except in the case of estrone, which did not consistently increase after the LH peak. Circulating estrone and estradiol both contributed to the high excretion of estradiol in the feces from both species. The timing in the delay in excretion of fecal steroids was used to accurately determine the ovulatory period to within a 2-day window. This degree of accuracy is possible when the duration of the delay to the LH peak is known for a given species. Additionally, steroid concentrations were highly correlated between frozen and lyophilized fecal samples (0.81 +/- 0.07 SEM), indicating that fluid removal from the feces did not effectively alter steroid profiles.

Group size, composition, and reproductive success in wild common marmosets (Callithrix jacchus).

Data from published sources about size and composition of wild common marmoset groups (Callithrix jacchus) were analyzed to see if the number of juveniles in a group is closely related to the number of other group members. Mean group size was 8.7 members including 4.4 adults (1.8 females, 2.5 males), 2.9 subadults, and 1.4 juveniles. The number of juveniles was significantly positively correlated to the number of adult males. Groups with one or two adult males had significantly fewer juveniles (mean: 1:1 juveniles) than groups containing more than two adult males (mean: 2.0 juveniles). Apart from a different number of subadults, results showed obvious similarities between common marmosets and tamarins of the genus Saguinus in size and composition of subgroups of adults as well as the key role of adult males in mediating the reproductive success of a breeding female. Common marmoset females seem to gain direct fitness benefits in increased reproductive success from the presence of a larger number of adult males. Whether or not other group members get fitness benefits depends on the reproductive strategy of adult males (monogamy vs. polyandry), their kinship, and on the genetic relationship of nonbreeders to the offspring of the breeding female. © 1995 Wiley-Liss, Inc.