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.     

Microsatellite variation within and among recently fragmented populations of the golden lion tamarin (Leontopithecus rosalia)

Four variable microsatellite loci were used toexamine the genetic diversity and differentiation of golden lion tamarins (Leontopithecus rosalia) in four populations recently isolated by habitat fragmentation. Using Rst estimates of genetic differentiation, a considerable genetic divergence was detected among these populations, with an averagedifferentiation of 31%. Significant differences in allele number among these populations were found. However, the heterozygosity among these populations was not statistically different. These results suggestthat loss in allele diversity was faster than loss in heterozygosity. Conservation implications, particularly for golden lion tamarins, are then discussed. Loss of allelic diversity might be as serious a concern to endangered species as heterozygosity or inbreeding.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

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.     

Hepatocellular carcinoma in two captive golden‐headed lion tamarins (Leontopithecus chrysomelas)

Two cases of hepatocellular carcinoma (HCC) in 2 female captive golden‐headed lion tamarins (Leontopithecus chrysomelas) are described. HCC was diagnosed in both, with pulmonary metastasis in one of them. Neoplastic cells were positive for hepatocyte‐specific antigen (HSA) by immunohistochemistry, confirming the diagnosis.     

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.     

Mating patterns in the golden lion tamarin (Leontopithecus rosalia): continuous receptivity and concealed estrus

Sociosexual behavior was monitored on a daily basis for 3 months in 5 pairs of golden lion tamarins (Leontopithecus rosalia). Urine samples were collected daily from each female and urinary estrogen cycles were determined by radioimmunoassay. Mounts and copulations were observed during all phases of the estrogen cycle. Peaks or regular cycles in sexual behavior were not documented. There were no significant changes in affiliative behavior by females or males that were associated with changes in urinary estrogen values. A negative relationship between pair bond duration and frequency of sexual interactions was observed: newly established pairs exhibited 2-6 times more frequent sexual behavior than a long-established pair. The lack of a conspicuous sexual signal in female golden lion tamarins may be related to a pattern of continuous sexual receptivity. Both reproductive patterns, concealed estrus and continuous receptivity, are explicable in relation to either monogamous or polyandrous mating systems.     

Dinucleotide microsatellite primers designed for a critically endangered primate,the black lion tamarin (Leontopithecus chrysopygus)

Black lion tamarin (BLT) monkeys (Leontopithecus chrysopygus) have suffered a severe reduction in their natural range and are consequently critically endangered. Because allozyme data showed very low levels of variation, it was not clear if these monkeys had much genetic diversity. We designed microsatellite primers for BLTs, and from them we identified nine polymorphic loci, seven of which were tested on golden lion tamarins (GLTs) (Leontopithecus rosalia). All of the seven polymorphic loci and two other monomorphic BLT loci were polymorphic in GLTs. The microsatellite markers identified here are directly applicable to ongoing lion tamarin population and conservation genetics studies.     

Infection with Trypanosoma cruzi TcII and TcI in free-ranging population of lion tamarins (Leontopithecus spp): an 11-year follow-up

Here, we present a review of the dataset resulting from the 11-years follow-up of Trypanosoma cruzi infection in free-ranging populations of Leontopithecus rosalia (golden lion tamarin) and Leontopithecus chrysomelas (golden-headed lion tamarin) from distinct forest fragments in Atlantic Coastal Rainforest. Additionally, we present new data regarding T. cruzi infection of small mammals (rodents and marsupials) that live in the same areas as golden lion tamarins and characterisation at discrete typing unit (DTU) level of 77 of these isolates. DTU TcII was found to exclusively infect primates, while TcI infected Didelphis aurita and lion tamarins. The majority of T. cruzi isolates derived from L. rosalia were shown to be TcII (33 out 42) Nine T. cruzi isolates displayed a TcI profile. Golden-headed lion tamarins demonstrated to be excellent reservoirs of TcII, as 24 of 26 T. cruzi isolates exhibited the TcII profile. We concluded the following: (i) the transmission cycle of T. cruzi in a same host species and forest fragment is modified over time, (ii) the infectivity competence of the golden lion tamarin population fluctuates in waves that peak every other year and (iii) both golden and golden-headed lion tamarins are able to maintain long-lasting infections by TcII and TcI.     

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.     

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.