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.     

Immigration in wild groups of golden lion tamarins (Leontopithecus rosalia)

Seventeen territorial groups of wild golden lion tamarins were monitored for periods of 10–76 months. Immigration into established groups was rare (0.48 immigrating individuals per group per year) and occurred mostly in the context of replacement of breeding individuals. Nonreplacement immigration events usually occurred in conjunction with some other change in group composition (e.g., an emigration or another immigration). Aggression by resident tamarins toward potential immigrants appeared to be the proximate factor limiting movement into groups. Most such aggression was intrasexual, but potential female immigrants were sometimes chased by male as well as female residents. Immigration was highly male biased (85% of individuals). Factors possibly contributing to this bias were inheritance of breeding positions by adult daughters (reducing female and increasing male immigration opportunities), ability of males but not females to join groups already containing a same-sex breeding individual, and the fact that potential female immigrants appeared to face some intersexual as well as intrasexual aggression. Male and female roles in the maintenance of a monogynous mating system are considered in light of these results. Contrasts with data from intruder studies on captive golden lion tamarins [French & Inglett, Animal Behaviour 37:487–497, 1989] are discussed. © 1996 Wiley-Liss, Inc.     

Food transfers in wild and reintroduced golden lion tamarins,Leontopithecus rosalia

We collected data from wild and reintroduced golden lion tamarins (Leontopithecus rosalia) to describe the behavior of donor and recipient during food transfers, evaluate the effect of supplemental feeding on food transfer behavior, and examine various hypotheses concerning the function of food transfers in primates. Behavioral observations were conducted on 12 groups of tamarins with young (N = 30) between the ages of 1 week and 1 year old. Results show that food transfers involve various behaviors, from steals by recipients to offers by donors; transfers mostly derive from adults and are directed at immature weaned young (between 3 and 9 months old); and that most items transferred were prey or fruits that require skill to process. Eleven percent of food transfers were preceded by an adult vocalization specific to that context, whereas 86% were preceded by conspicuous infant vocalizations and begging behavior. The most common vocalizations were loud and atonal (rasps) and broad banded frequency modulated (trills). Infants born to reintroduced parents vocalized less, whereas reintroduced adults vocalized more before transferring food than their wild counterparts. Reintroduced adults and young received more food transfers (4.4 per hr) than did wild‐born adults and young (2.2 per hr). Our findings suggest that food transfer in golden lion tamarins is best understood as provisioning of young that have not fully developed foraging skills to ensure they get the necessary resources for growth and survival. Am. J. Primatol. 48:305–320, 1999. © 1999 Wiley‐Liss, Inc.     

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.     

Foraging ecology and use of space in wild golden lion tamarins (Leontopithecus rosalia)

In this paper we describe the use of space and feeding ecology of seven groups of golden lion tamarins observed for a total of 2,164 hr in Poço das Antas Reserve, Rio de Janeiro, Brazil. Relative to habitat availability in the home ranges of these groups, lion tamarins spent more time than expected in relatively undisturbed swamp forests and less time than expected in more degraded hillside and pasture habitats. Home range area was correlated with group biomass but not group size. Golden lion tamarins fed primarily on fruits and small animal prey, but relied heavily on floral nectar during seasonal periods of relatively low fruit availability. Compared to other New World monkeys, lion tamarins used larger home range areas and exhibited longer daily path lengths than would be predicted by group biomass alone. We suggest that this pattern of foraging and use of space may be explained by the relatively greater availability of cryptic prey and their microhabitats in forests that are flooded and/or have closed canopies than in forests that are in earlier stages of succession where prey may be more susceptible to desiccation during the dry season. Am. J. Primatol. 41:289–305, 1997. © 1997 Wiley-Liss, Inc.     

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.     

Provisioning in wild golden lion tamarins (Leontopithecus rosalia): benefits to omnivorous young

Provisioning may act to cushion weaned young from dietary insufficiencyand errors during the period in which they are mastering complexforaging techniques or learning to identify appropriate dietaryitems. That is, young mammals who receive food from others maygain nutritional and/or informational benefits. I conducteda longitudinal study of 13 wild golden lion tamarins 11–56weeks of age in six groups to evaluate hypotheses regardingthe functions of provisioning. All members belonging to thisprimate taxonomic family (the Callitrichidae) are cooperativebreeders and are known to provision their young more frequentlythan do other primate species, except humans. My results, togetherwith experimental findings, suggest that juveniles receive bothnutritional and informational benefits from being provisioned.My juvenile study subjects received animal prey (invertebratesand small vertebrates) from others more frequently than plantresources (fruits and hardened exudates). Apparently difficult-to-handlefruits were more likely to be transferred than readily processedfruits. These results support the nutritional benefits hypothesisbecause the young received items, particularly lipid- and protein-richprey, that they might not otherwise have acquired. That juvenilesfed independently on, and were provisioned with, the same fruitson the same day is counterevidence to the nutritional benefitshypothesis, however. The informational benefits hypothesis wassupported because juveniles received a large variety of foods(including more than 20% of fruit species eaten) and receiveduncommon fruits that were easily acquired. Adults emitted food-offeringcalls to encourage the transfer of prey to juveniles, particularlywhen the prey was whole and alive.     

Spontaneous tool use in captive, free-ranging golden lion tamarins (Leontopithecus rosalia rosalia)

Two types of tool use were observed in eight captive, free-ranging golden lion tamarins (Leontopithecus rosalia rosalia). All eight individuals used twigs and/or radio collar antennae to pry bark from trees and probe crevices, presumably for invertebrates. Three individuals used tools for grooming. In two animals, antennae were used as grooming tools while the third individual used a stick while grooming. The complexity of the free-ranging environment may have played a role in the expression of tool use behavior in these animals, as tool use has never been observed in captive tamarins living in traditional enclosures or wild tamarins. Social transmission may be one of the mechanisms responsible for the acquisition of tool use — six of the eight tool users resided in two social groups, and the only two individuals that used antennae as grooming tools were a bonded pair. These are the first published observations of tool use by golden lion tamarins or any callitrichid in a non-experimental setting and provide further data supporting the theory of a link between extractive foraging and tool use.     

Ectoparasitic acari found on golden lion tamarins (Leontopithecus rosalia rosalia) from Brazil

Anesthetized golden lion tamarins (Leontopithecus rosalia rosalia), a highly endangered species, were examined for ectoparasites by brushing the fur and swabbing the ears. Ectoparasites recovered from the fur included four species of immature ticks (Amblyomma spp.), three species of chiggers (Euschoengastia sp., Microtrombicula brennani and Speleocola tamarina), and one species of follicular mite (Rhyncoptes anastosi). Ectoparasites do not seem to be of particular significance to the health of the golden lion tamarin; this may in part result from grooming.     

Sources of variability in numbers of live births in wild golden lion tamarins (Leontopithecus rosalia)

We examined the effects of several variables on the number of live births in multiparous females in a wild population of golden lion tamarins (Leontopithecus rosalia). Independent variables included the number of infants born to a female the previous breeding season, the number of infants weaned the previous breeding season, the female's age and body mass, the number of adult males and helpers in the group, and the inbreeding coefficient of the offspring. We also tested the hypothesis that trapping and chemical immobilization during pregnancy affected the number of live births. Female body mass was the only statistically significant predictor of the number of live-born infants in the current season when both first and second peaks were included. Characteristics that predicted higher numbers of infants in the first peak of a season were the number of infants born the previous season and the body mass of the female. The greater the number of infants born the previous season, the greater the number of infants born in the first peak of the current season. Factors positively correlated with the number of live births in the second peak within a season included the number of infants born the previous season, as well as the number of available helpers. Due to sample size constraints, the analysis of litters in the second peak did not include body mass of the female as a variable. Inbreeding and handling did not affect the number of live births. We found no evidence that current reproduction negatively impacts future reproduction in this species. We also found no evidence for an age-related reduction in fertility.     

Changes in locomotor and foraging skills in captive-born, reintroduced golden lion tamarins (Leontopithecus rosalia rosalia)

The behavior of reintroduced, captive-born animals is understudied, limiting the scientific understanding and utility of reintroduction as a conservation tool. This work describes changes in locomotor and foraging behaviors in captive-born golden lion tamarins over the first 18 months after their release into the wild. The subjects included 73 individuals living in and around the Poco das Antas Biological Reserve in Brazil between 1984 and 1996. The differences between animals that survived 6 months after release and those that did not indicate that initial deficiencies in locomotor and foraging abilities are related to survival. Behavioral changes in both juvenile and adult individuals during the first 6 and 18 months after release appear to be primarily related to locomotor abilities; however, the effect of provisioning on foraging abilities is unknown. Juvenile animals showed a larger number of changes relative to adults during the first 6 and 18 months, suggesting that placing tamarins into complex environments early in development may promote the expression of natural behaviors and increase survival opportunities after their release. However, when this is not possible, the best mechanism for reintroducing adult members of this species involves intensive post-release support rather than pre-release training, which confers few behavioral advantages. Recommendations for future reintroductions with this and other species include introducing animals to complex environments early in development, and collecting data systematically.     

High rates of pregnancy loss by subordinates leads to high reproductive skew in wild golden lion tamarins (Leontopithecus rosalia)

Across taxa, cooperative breeding has been associated with high reproductive skew. Cooperatively breeding golden lion tamarins (Leontopithecus rosalia) were long thought to have a monogynous mating system in which reproduction was limited to a single dominant female. Subordinates with few reproductive opportunities delayed dispersal and remained in the natal group to provide alloparental care to siblings, thus allowing dominant reproductive females to meet the energetic needs associated with high rates of reproduction and successful infant rearing. The goal of this study was to re-assess monogyny in wild golden lion tamarin groups based upon pregnancy diagnoses that used non-invasive enzyme immunoassay for progesterone and cortisol, combined with weekly data on individual weight gain, bi-annual physical examinations noting pregnancy and lactation status and daily behavioral observations. We established quantitative and qualitative criteria to detect and determine the timing of pregnancies that did not result in the birth of infants. Pregnancy polygyny occurred in 83% of golden lion tamarin groups studied. The loss of 64% of subordinate pregnancies compared to only 15% by dominant females limited reproductive success mainly to dominant females, thus maintaining high reproductive skew in female golden lion tamarins. Pregnancy loss by subordinate adults did not appear to result from dominant interference in subordinate hormonal mechanisms, but more likely resulted from subordinate abandonment of newborn infants to mitigate dominant aggression.     

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.     

Locomotion of free-ranging golden lion tamarins (Leontopithecus rosalia) at the National Zoological Park

Locomotor behavior and substrate use of cage-reared golden lion tamarins (Leontopithecus rosalia), newly released and free-ranging on the grounds of the National Zoological Park, were studied to determine if locomotion changed following exposure to naturalistic conditions. The animals employed a predominantly quadrupedal locomotor profile, incorporating leaping and vertical climbing to a lesser degree. There was no clear evidence of a change in locomotion due to the high degree of variability in these behaviors. The locomotor repertoire of the free-ranging group differed from that of groups occupying unenriched but relatively large conventional enclosures, indicating that whereas locomotion is plastic with respect to environment, substrate characteristics influence locomotor behavior and may promote stereotypical behavior. However, due to anatomical constraints, the locomotor repertoire tended to be less variable than substrate use. Similar behaviors were used in moving through a variety of habitat features in spite of strong associations between specific locomotor styles and substrate classes. © 1994 Wiley-Liss, Inc.     

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.     

Acoustic differences between spontaneous and induced long calls of golden lion tamarins,Leontopithecus rosalia

Long calls are emitted by several primate taxa and appear to have multiple functions related to spacing mechanisms and reproduction. Yet, in some species the spontaneous rate of emission of these calls is low, and playbacks are used to elicit long calls to augment the sample size of studies. The objective of this study was to compare the acoustic structure of spontaneously emitted and experimentally induced long calls of golden lion tamarins. Results from 6 adult tamarins show that spontaneously emitted long calls differ acoustically from experimentally induced long calls in several frequency measures. Several explanations for these differences are discussed. We conclude that regardless of the underlying mechanisms, playbacks elicit responses that may be different from naturally occurring calls.     

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.     

Social contributions to the foraging behavior of young wild golden lion tamarins (Leontopithecus rosalia): Age-related changes and partner preferences

In cooperatively breeding species, group members other than the parents contribute to the care of the young. The costs and benefits to caregiving may vary with the type of care provided and with caregiver characteristics such as age, sex, reproductive status, and foraging ability. Here I examine the relative contributions of parents, helpers and same-aged twins to the foraging and feeding activities of the young in a longitudinal study of wild golden lion tamarins, specifically with regard to direct food transfer, tolerance for coforaging or cofeeding by immatures and signaling young as to the location of profitable prey-foraging sites. I found that the type of food-related assistance varied as a function of the age of the immature and among group members. Rates of food transfer steadily declined as immatures aged, while coforaging rates peaked when juveniles were in the middle age group. Mothers and fathers were the most generous in terms of providing food to begging young. Mothers most often directed juveniles to productive foraging sites, and female helpers never did. Older siblings did not vary caregiving effort according to sex or age. Adult and subadult foraging ability was not a strong predictor of the rates at which prey was given to the young or the rates at which caregivers tolerated coforaging by immatures on plant and prey resources. Thus, foraging ability did not appreciably influence generosity to or tolerance of the young.     

Clinical, biochemical, and electrocardiographic aspects of Trypanosoma cruzi infection in free-ranging golden lion tamarins (Leontopithecus rosalia)

Background Wild golden lion tamarins from the Biological Reserve of Poço das Antas, Rio de Janeiro, Brazil, have high prevalence of Trypanosoma cruzi infection leading us to clinically assess the disease in this endangered species. Methods 34 tamarins were sampled for the presence of T. cruzi infection (through serology) and clinical evaluation (electrocardiography, blood counts and biochemical analysis). Results 32% of the sampled tamarins were T. cruzi positive, 45% of these displayed cardiac abnormalities. Main cardiac abnormality in infected tamarins was T wave low voltage; R wave low voltage and V3S wave high voltage were also found. The tamarins displaying T wave low voltage had high proportion of seric cardiac creatine kinase. Seric mean total protein was significantly higher in infected tamarins. Conclusions Sampled tamarins displayed typical signs of T. cruzi infection, similar to experimentally infected primates and human natural infection. Potential risk of T. cruzi infection to this endangered species is discussed.     

Census and distribution of the golden lion tamarin (Leontopithecus rosalia)

During 1990–1992, a survey of the golden lion tamarin, Leontopithecus rosalia, was carried out throughout its known distribution area. Forest remnants were identified by visual interpretation of Landsat‐TM satellite images. Localities occupied by L. rosalia were first identified by interviews with local people. All forests more than 20 ha in size, and for which two or more interviews suggested the presence of the species, were surveyed using “play‐back” recordings of lion tamarin long calls. The total wild population of L. rosalia, including that of the Poço das Antas Biological Reserve, was estimated to be 562 individuals in 109 groups. The lion tamarins were generally found in four major areas of forest (six or more groups per forest, not including Poço das Antas), with a further 12 groups isolated in small forest patches. Currently the species' distribution is restricted to just four municipalities in the state of Rio de Janeiro: Silva Jardim, Cabo Frio, Saquarema, and Araruama. Although they are typically confined to lowland forest of <300 m altitude, L. rosalia was recorded at an altitude of 550 m in one locality. Average group size varied from 3.6 to 5.7 individuals, and densities from 0.39 groups/km² to 2.35 groups/km² (2.17 individuals/ km² to 8.53 individuals/km²). Six of the isolated groups found during the survey were successfully translocated to a forest of 2,400 ha. There is now also a significant population of reintroduced lion tamarins. Overall, however, the possibilities for further expansion of the wild population are severely limited. Am. J. Primatol. 59:29–44, 2003. © 2003 Wiley‐Liss, Inc.