Endocrine Monitoring of Wild Dominant and Subordinate Female Leontopithecus rosalia

In captive callitrichid primates, female reproductive function tends to vary with social status. However, little is known about the interplay between these factors in wild groups. We report observations on normative ovarian function in dominant and subordinate female golden lion tamarins (Leontopithecus rosalia) living in wild groups. We monitored ovarian status by measuring, via enzyme immunoassay, concentrations of excreted pregnanediol glucuronide (PdG) and estrone conjugates (E₁C) in fecal samples collected noninvasively from individuals in social groups in the Poço das Antas Biological Reserve, Rio de Janeiro State, Brazil. Dominant breeding females demonstrated steroid levels similar to those previously reported for wild cotton-top tamarin females, with statistically significant rises during pregnancy. The duration of elevation of fecal steroids in breeding females was ca. 4 mo, which corresponds with estimates of gestation from captive studies. Low steroid concentrations from December to June suggest a seasonally-related period of infertility in female golden lion tamarins. Dominant and subordinate females demonstrated several differences in endocrine function. In general, younger females living in intact natal family groups showed no evidence of ovarian cyclicity. We noted endocrine profiles consistent with ovulation and subsequent pregnancy for behaviorally subordinate females living in groups with unrelated males or in which a reversal in female dominance status occurred. Results suggest that in addition to changes in female reproductive endocrinology associated with puberty, the regulation of reproduction in females in wild callitrichid groups can be sensitive to status and relatedness to breeding males.     

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.     

Effects of social status, age, and season on androgen and cortisol levels in wild male golden lion tamarins (Leontopithecus rosalia)

This study examines factors affecting androgen and cortisol levels in wild, male golden lion tamarins (Leontopithecus rosalia). Golden lion tamarins are a cooperatively breeding species in which groups often contain two potentially breeding males. Brothers frequently emigrate together and develop a clear dominance hierarchy, but interactions between them are primarily affiliative. Duos in which the males are not related are less stable. In addition, reproductive skew theory predicts that dominant males will be less likely to share reproduction with related subordinates. As such, we predicted that both androgens and cortisol would be higher in subordinate males unrelated to the dominant male. We also predicted that androgens in breeding males would be higher during the mating season than the birth/infant care season, as per Wingfield's "challenge hypothesis" (1990). Fecal samples were collected from 24 males in 14 social groups and assayed by enzyme immunoassay. Androgen levels were higher in breeding males during the mating season, thus supporting the challenge hypothesis. However, while subordinate males unrelated to the dominant male had significantly lower androgens than any other group, cortisol levels were not correspondingly higher. These results suggest that unrelated subordinate males show measurable reproductive suppression and may use strategies such as infantilization to avert aggression from dominant males.     

Patterns of urinary oestrogen excretion in female golden lion tamarins (Leontopithecus rosalia)

Daily urine samples were collected from 5 female golden lion tamarins (Leontopithecus rosalia) over a period of 3 or more months, and urinary oestrogen concentrations were determined by radioimmunoassay. Four females exhibited regular patterns of oestrogen excretion, with a peak-to-peak periodicity of 19.6 +/- 1.4 days. Levels of oestrogen excretion tended to vary between, but not within, individual females. Post-partum oestrogen patterns included periods of clear oestrogen cyclicity before conception, with dramatic elevations in oestrogen excretion following conception. Oestrone was the predominant urinary oestrogen excreted by female lion tamarins. Enzyme hydrolysis with Helix pomatia beta-glucuronidase/sulphatase was an efficient method of liberating conjugated oestrogens in tamarin urine. Urinary oestrogen determinations can provide useful information about reproductive status in female lion tamarins.     

Reproductive skew in female common marmosets: what can proximate mechanisms tell us about ultimate causes?

Common marmosets are cooperatively breeding monkeys that exhibit high reproductive skew: most subordinate females fail to reproduce, while others attempt to breed but produce very few surviving infants. An extensive dataset on the mechanisms limiting reproduction in laboratory-housed and free living subordinate females provides unique insights into the causes of reproductive skew. Non-breeding adult females undergo suppression of ovulation and inhibition of sexual behaviour; however, they receive little or no aggression or mating interference by dominants and do not exhibit behavioural or physiological signs of stress. Breeding subordinate females receive comparable amounts of aggression to non-breeding females but are able to conceive, gestate and lactate normally. In groups containing two breeding females,however, both dominant and subordinate breeders kill one another's infants. These findings suggest that preconception reproductive suppression is not imposed on subordinate females by dominants, at a proximate level, but is instead self-imposed by most subordinates, consistent with restraint models of reproductive skew. In contrast to restraint models, however, this self-suppression probably evolved not in response to the threat of eviction by dominant females but in response to the threat of infanticide. Thus,reproductive skew in this species appears to be generated predominantly by subordinate self-restraint, in a proximate sense, but ultimately by dominant control over subordinates' reproductive attempts.     

Correlates of molt in golden lion tamarins (Leontopithecus rosalia)

In this paper we describe the timing and correlates of molt for a native population of golden lion tamarins (Leontopithecus rosalia). We conducted 820 examinations of 267 adult tamarins over a 7.75 year period to determine the annual molting cycle in this population. Dorsal molt was an annual event for most individuals in the study population; however, 10% of sampled individuals apparently molted twice in a 12 month period. Duration of molt was estimated at 5–6 weeks. The proportion of samples in which tamarins were in molt was significantly greater during the wet season than the dry season and positively correlated with mean monthly precipitation and minimum temperature but not tamarin births, suggesting an environmental component to timing of molt. We found no sex differences in the occurrence of molt during wet or dry seasons. However, the relative frequency of samples in molt was significantly less for gravid females than for nongravid females. In four polygynous groups, socially dominant females gave birth before subordinate females, and younger reproductive females completed molt before older reproductive females. © 1995 Wiley-Liss, Inc.     

Reproduction of the emperor tamarin (Saguinus imperator) in captivity,with comparisons to cotton-top and golden lion tamarins

Little information has been published on the reproductive biology and behavior of the emperor tamarin (Saguinus imperator). We analyzed twelve years of data on emperor tamarins at the Los Angeles Zoo and made comparisons with data on cotton-top tamarins (Saguinus o. oedipus) and golden lion tamarins (Leontopithecus rosalia) from the same collection. Secondary sex ratios did not differ significantly from 50:50. Births were not strictly seasonal for any species. The number of infants reared had a significant effect on interbirth interval for all species, with shorter intervals when only one or no infants were reared, but females did sometimes conceive early in lactation. In emperor tamarin families, all fathers and most older siblings carried new infants, usually beginning within a few days after a birth. Previous exposure to younger siblings did not appear to be critical to the development of competent parental behavior by zooborn emperor tamarin females.     

Food Sharing in Lion Tamarins (<Emphasis Type="Italic">Leontopithecus chrysomelas</Emphasis>): Does Foraging Difficulty Affect Investment in Young by Breeders and Helpers?

Food sharing with immatures is an important and relatively well studied aspect of infant care in many cooperative species. A key point that has not yet been fully addressed, however, is how increasing the difficulty of obtaining food influences the willingness of breeders and helpers to provision immature offspring. We used captive golden headed lion tamarins (Leontopithecus chrysomelas) to examine how breeders and helpers differ in provisioning juvenile individuals according to the level of difficulty of obtaining food. The level of difficulty in obtaining food was varied by placing the food inside tubes that allowed access only by adults. When food acquisition became more difficult, food sharing with juveniles and breeding females increased significantly. Begging calls by breeding females and juveniles increased during the experimental condition, which probably led to increases in food sharing. Breeders and helpers did not differ in their contribution to provisioning when food was easily available, nor did they differ in their contribution when food was difficult to obtain. Breeding males in callitrichids have a prominent role in transferring food to offspring, but contrary to our expectations, they did not increase food transfer in the experimental condition. An unexpected result was the increased investment of the breeding female into her current offspring when the level of difficulty of obtaining food was higher. We suggest that breeding lion tamarin females are not as constrained by reproductive costs as breeding females of other callitrichids. Degree of reproductive skew is hypothesized as a factor affecting the contribution of breeders and helpers to offspring care in cooperative breeding mammals, though we suggest that more studies are needed to validate such a generalization.     

Social and reproductive factors affecting cortisol levels in wild female golden lion tamarins (Leontopithecus rosalia)

The steroid hormone cortisol has been associated with different levels of "stress" as well as different reproductive conditions in many primates. In callitrichids, cortisol has more often been reflective of female reproductive status than of chronic stress. In this study, we addressed the hypothesis that wild golden lion tamarin (Leontopithecus rosalia) females, whose social structure is characterized by low aggression and high social support, would not show rank ("stress")-related differences in glucocorticoids but would show reproductive changes. We collected 710 fecal samples from 22 adult females in Po?o das Antas Reserve, Brazil, and nearby reintroduction areas, and assayed them for cortisol. Differences in cortisol levels were found between different reproductive conditions. Females in the first trimester of pregnancy had lower cortisol levels than nonpregnant females, although we did not differentiate between basal and ovulating levels in nonpregnant females. Cortisol rose in the third trimester of pregnancy. Primiparous females had a higher rise in the third trimester than multiparous females. No differences in cortisol levels were found among dominant females, ovulatory subordinate females, or anovulatory subordinate females. These results are similar to those obtained in other studies of callitrichid females. The lack of differences in cortisol excretion between dominants and subordinates is likely due to the low levels of overt aggression and the high level of social support available to subordinate females.     

Costly reproductive competition between females in a monogamous cooperatively breeding bird

In many cooperatively breeding societies, only a few socially dominant individuals in a group breed, reproductive skew is high, and reproductive conflict is common. Surprisingly, the effects of this conflict on dominant reproductive success in vertebrate societies have rarely been investigated, especially in high-skew societies. We examine how subordinate female competition for breeding opportunities affects the reproductive success of dominant females in a monogamous cooperatively breeding bird, the Southern pied babbler (Turdoides bicolor). In this species, successful subordinate reproduction is very rare, despite the fact that groups commonly contain sexually mature female subordinates that could mate with unrelated group males. However, we show that subordinate females compete with dominant females to breed, and do so far more often than expected, based on the infrequency of their success. Attempts by subordinates to obtain a share of breeding impose significant costs on dominant females: chicks fledge from fewer nests, more nests are abandoned before incubation begins, and more eggs are lost. Dominant females appear to attempt to reduce these costs by aggressively suppressing potentially competitive subordinate females. This empirical evidence provides rare insight into the nature of the conflicts between females and the resultant costs to reproductive success in cooperatively breeding societies.     

Higher reproductive skew among birds than mammals in cooperatively breeding species

While competition for limited breeding positions is a common feature of group life, species vary widely in the extent to which reproduction is shared among females (‘reproductive skew’). In recent years, there has been considerable debate over the mechanisms that generate variation in reproductive skew, with most evidence suggesting that subordinates breed when dominants are unable to prevent them from doing so. Here, we suggest that viviparity reduces the ability of dominant females to control subordinate reproduction and that, as a result, dominant female birds are more able than their mammal counterparts to prevent subordinates from breeding. Empirical data support this assertion. This perspective may increase our understanding of how cooperative groups form and are stabilized in nature.     

Sex differences in the drivers of reproductive skew in a cooperative breeder

Many cooperatively breeding societies are characterized by high reproductive skew, such that some socially dominant individuals breed, while socially subordinate individuals provide help. Inbreeding avoidance serves as a source of reproductive skew in many high‐skew societies, but few empirical studies have examined sources of skew operating alongside inbreeding avoidance or compared individual attempts to reproduce (reproductive competition) with individual reproductive success. Here, we use long‐term genetic and observational data to examine factors affecting reproductive skew in the high‐skew cooperatively breeding southern pied babbler (Turdoides bicolor). When subordinates can breed, skew remains high, suggesting factors additional to inbreeding avoidance drive skew. Subordinate females are more likely to compete to breed when older or when ecological constraints on dispersal are high, but heavy subordinate females are more likely to successfully breed. Subordinate males are more likely to compete when they are older, during high ecological constraints, or when they are related to the dominant male, but only the presence of within‐group unrelated subordinate females predicts subordinate male breeding success. Reproductive skew is not driven by reproductive effort, but by forces such as intrinsic physical limitations and intrasexual conflict (for females) or female mate choice, male mate‐guarding and potentially reproductive restraint (for males). Ecological conditions or “outside options” affect the occurrence of reproductive conflict, supporting predictions of recent synthetic skew models. Inbreeding avoidance together with competition for access to reproduction may generate high skew in animal societies, and disparate processes may be operating to maintain male vs. female reproductive skew in the same species.     

Post-conception reproductive competition in cooperatively breeding common marmosets

Common marmosets are cooperatively breeding monkeys that exhibit high female reproductive skew. Subordinate females usually fail to breed as a consequence of ovulation suppression and inhibition of sexual behavior, and, even when they do breed, typically rear fewer infants than dominants. We evaluated possible mechanisms of post-conception reproductive competition by comparing hormonal profiles across pregnancy, pregnancy outcomes, infant survivorship, and behavior in laboratory-housed families containing one (N=9) or two (N=7) breeding females. Breeding females in plurally breeding groups did not exhibit well-defined dominance relationships and rarely engaged in escalated aggression with one another. No significant differences were found among singly breeding mothers, plurally breeding mothers, and plurally breeding daughters in urinary chorionic gonadotropin or estradiol sulfate concentrations during pregnancy, fetal biparietal diameter, frequency of spontaneous abortion, frequency of stillbirths, number of live-born infants per litter, or infant mortality rates. When females gave birth while another female in the family was pregnant, however, their infants were highly likely to be killed. The perpetrator was definitively identified in only one family, in which a pregnant female killed her daughter's infant. These results are consistent with observations of free-living common marmosets and suggest that breeding females do not regularly influence one another's pregnancy outcomes, but that they may commonly kill each other's infants, especially during their own pregnancy. Our findings further suggest that infanticide by breeding females may have selected for the evolution of reproductive restraint in subordinate female marmosets.     

Genetic variation within and among lion tamarins

The golden lion tamarin Leontopithecus rosalia rosalia, one of the rarest and most endangered of New World primates, has been the focus of an intensive research and conservation effort for two decades. During that period, managed breeding from 44 founders has brought the captive population to over 400 individuals, a number that equals or exceeds the estimated number of free-ranging golden lion tamarins. The extent of genetic variation among golden lion tamarins was estimated with an electrophoretic survey of 47 allozyme loci from 67 captive and 73 free-ranging individuals. The amount of variation was low, compared to 15 other primate species, with 4% of the loci being polymorphic (P), and with an average heterozygosity H estimate of 0.01 in these callitrichids. Electrophoretic analyses of captive and free-ranging animals (N = 31) of two allopatric morphotypes, Leontopithecus rosalia chrysopygus and L. r. chrysomelas, were similar to the L. r. rosalia findings insofar as they also revealed limited genetic polymorphism. Computation of the Nei-genetic distance measurements showed that the three morphotypes were genetically very similar, although discernible differentiation had occurred at two loci. These data are consistent with the occurrence of recent reproductive isolations of these subspecies.     

Phylogeny of lion tamarins (Leontopithecus spp) based on interphotoreceptor retinol binding protein intron sequences

The evolutionary relationships of the lion tamarins (Leontopithecus) were investigated using nuclear interphotoreceptor retinol binding protein (IRBP) intron sequences. Phylogenetic reconstructions strongly support the monophyly of the genus, and a sister relationship between the golden lion tamarin, Leontopithecus rosalia, and the black lion tamarin, L. chrysopygus, to the exclusion of the golden-headed lion tamarin, L. chrysomelas. The most parsimonious evolutionary reconstruction suggests that the ancestral lion tamarin and the common ancestor of L. rosalia and L. chrysopygus had predominantly black coats. This reconstruction is not consistent with a theory of orthogenetic evolution of coat color that was based on coat color evolution in marmosets and tamarins. An alternative reconstruction that is consistent with metachromism requires that ancestral lion tamarins had agouti hairs.     

Influence of the mother's reproductive state on the hormonal status of daughters in marmosets (Callithrix kuhlii)

Behavioral and endocrine suppression of reproduction in subordinate females produces the high reproductive skew that characterizes callitrichid primate mating systems. Snowdon et al. [American Journal of Primatology 31:11-21, 1993] reported that the eldest daughters in tamarin families exhibit further endocrinological suppression immediately following the birth of siblings, and suggested that dominant females exert greater control over subordinate endocrinology during this energetically challenging phase of reproduction. We monitored the endocrine status of five Wied's black tufted-ear marmoset daughters before and after their mother delivered infants by measuring concentrations of urinary estradiol (E(2)), pregnanediol glucuronide (PdG), testosterone (T), and cortisol (CORT). Samples were collected from marmoset daughters 4 weeks prior to and 9 weeks following three consecutive sibling-litter births when the daughters were prepubertal (M=6.1 months of age), peripubertal (M=11.9 months), and postpubertal (M=17.6 months). The birth of infants was associated with reduced ovarian steroid excretion only in the prepubertal daughters. In contrast, ovarian steroid levels tended to increase in the postpubertal daughters. Urinary E(2) and T levels in the postpubertal daughters were 73.8% and 37.6% higher, respectively, in the 3 weeks following the birth of infants, relative to prepartum levels. In addition, peak urinary PdG concentrations in peri- and postpubertal daughters were equivalent to luteal phase concentrations in nonpregnant, breeding adult females, and all of the peri- and postpubertal daughters showed clear ovulatory cycles. Cortisol excretion did not change in response to the reproductive status of the mother, nor did the concentrations change across age. Our data suggest that marmoset daughters of potential breeding age are not hormonally suppressed during the mother's peripartum period or her return to fertility. These findings provide an additional example of species diversity in the social regulation of reproduction in callitrichid primates.     

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.     

Urinary and plasma gonadotropin concentrations in golden lion tamarins (Leontopithecus r. rosalia)

This paper describes the development and validation of a plasma and urinary gonadotropin immunoassay for golden lion tamarins (Leontopithecus rosalia), an endangered New World callitrichid primate. The assay is derived from a macaque chorionic gonadotropin assay and was validated for both plasma and urine samples in L. rosalia. Levels of immunoreactive LH/CG in lion tamarin urine were highly correlated (r = + 0.98) with gonadotropin bioactivity. Immunoreactive LH/CG levels were examined in two contexts: in the urine of adult females and in the plasma of adult males after administration of estrogen. Peaks of gonadotropin excretion were detected in samples collected from nonpregnant adult females. The peaks occurred immediately prior to cyclic elevations in urinary estrogen excretion. Plasma LH/CG concentration in males measured 24 and 48 hours after a single 50 μg injection of estradiol benzoate were significantly lower than levels at these time points measured after control treatment. Together, the results of this study point to the utility of the gonadotropin assay for monitoring reproductive function in both female and male lion tamarins.     

Cross-generic Food Sharing in Tamarins

Adult-infant food-sharing behavior is a major component of the infant care strategies of callitrichids (marmosets and tamarins). It is particularly well-developed in cotton-top tamarins (Saguinus Oedipus) and lion tamarins (Leontopithecus spp), which show frequent adult-initiated food offering, as well as sharing of food in response to begging by infants. This report documents a case of cross-generic food sharing, in which a male golden-headed lion tamarin (Leontopithecus chrysomelas) shared food with an infant cotton-top tamarin. The lion tamarin provided more food to the infant than its mother did. This emphasizes the importance of this behavior in the reproductive strategies of the communally-rearing Callitrichidae and raises questions about mechanisms that underly it.