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.     

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.     

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.     

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.     

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.     

Pterygodermatites nycticebi infections in golden lion tamarins (Leontopithecus rosalia rosalia) and aye‐ayes (Daubentonia madagascariensis) from a German zoo

In a golden lion tamarin (Leontopithecus rosalia rosalia) colony kept indoors in a German zoo, two animals presented a sudden onset of reduced general condition, lethargy, and diarrhea. At animal capture for clinical examination, adult nematode stages were observed after stress‐induced defecation. Despite treatment, two golden lion tamarins died in the following 2 days. At necropsy, spirurid stages were found in the lungs and intestine. Additionally, adult Pterygodermatites spp. were identified in histopathological samples of intestine and pancreas, confirming the previous diagnosis. Upon diagnosis, all animals were treated with ivermectin (0.2 mg/kg; SC). Thereafter, the general condition of the golden lion tamarins improved, whereby some of them excreted spirurid nematodes over 3 days. Four weeks after treatment, 20 fecal samples from the colony were examined and proved negative for parasitic stages. Given that common German cockroaches (Blattella germanica) are suitable intermediate hosts of Pterygodermatites nycticebi, 30 specimens were collected from seven different locations around the golden lion tamarins housing. Third‐stage larvae of Pterygodermatites spp. were recovered from those cockroaches. Regular anthelmintic treatments, coprological screenings, and controls for intermediate hosts were recommended. More than 2 years later, P. nycticebi infection was diagnosed again histopathologically in an aye‐aye (Daubentonia madagascariensis) which suddenly died. Coprological analysis confirmed the presence of spirurid eggs. Due to prosimian primates' cockroach‐eating habits and given that total cockroach eradication proved impossible, continuous cockroach control strategies and regular treatments of primates are currently performed to prevent further P. nycticebi infections.     

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.     

Optimal foraging theory predicts effects of environmental enrichment in a group of adult golden lion tamarins

The success of environmental enrichment programs in effecting specific changes in the behavior of captive animals has not always been uniform. Separate studies demonstrated both an increase in food competition and a decrease in food competition among captive group-living primates upon introduction of foraging devices. The objectives of this study were to measure the effects of variation in resource distribution and availability on food competition in a group of captive adult golden lion tamarins (Leontopithecus rosalia). The resource variables chosen were suggested from optimal foraging theory. The energy invested to obtain an item influenced food transfer and aggressive behaviors while food abundance did not. All individuals obtained an equivalent number of items over the course of the experiment from the foraging device, even though some tamarins obtained most of their food rewards directly from the device while others received their food rewards primarily through food transfer from other group members. Because the monkeys appeared highly motivated to obtain food from the test apparatus and did not habituate to it, the foraging device used in this experiment could be used as regular environmental enrichment for golden lion tamarins. One way to circumvent potentially unacceptable rates of aggression, with this or any feeding protocol that increases foraging task complexity and search time, may be to provide more than one foraging device per group. Zoo Biol 17:231–244, 1998. © 1998 Wiley-Liss, Inc.     

Acoustic structure of long calls in free-ranging groups of golden lion tarnarins,Leontopithecus rosalia

Like many other callitrichids, golden lion tamarins, Leontopithecus rosalia, emit Long Calls. Recordings of four free-ranging groups were made to explore different types of Long Calls. Three Long Call types were identified acoustically, and analyzed sonographically. The calls usually started with an Introductory Syllable (a chirp, a trill, or a whine) which was followed by either one, two, or three different phrases in a fixed sequential order. Each of the three phrases was unique and contained a typical number of syllables of characteristic shape, frequencies, and durations. Possible functions of these calls are discussed. © 1994 Wiley-Liss, Inc.     

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.     

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.     

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.     

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.     

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.     

Semen cryopreservation in golden‐headed lion tamarin,Leontopithecus chrysomelas

Wild animal genetic resource banking (GRB) represents a valuable tool in conservation breeding programs, particularly in cases involving endangered species such as the golden‐headed lion tamarin (Leontopithecus chrysomelas). Thus, we aimed to assess a sperm freezing protocol for golden‐headed lion tamarins using two different exenders: BotuBOV® (BB) and Test Yolk Buffer® (TYB). Ejaculates were collected by penile vibrostimulation from animals housed at São Paulo Zoological Park Foundation, São Paulo, Brazil, and after immediate analysis, two aliquots were diluted in BB and TYB. Postthawing samples were evaluated for total and progressive motility, plasma membrane and acrosome integrities, mitochondrial activity, susceptibility to oxidative stress, and sperm–egg‐binding. No differences between BB and TYB were found for most seminal parameters, except for acrosome integrity and susceptibility to oxidative stress (in both cases BB showed higher values). However, in spite of these differences and regardless of the extender used, postthaw sperm motility and viability with the described protocol were encouraging (on average >50% and >80%, respectively), indicating that sperm cryopreservation may be a short‐term measure for the conservation of golden‐headed lion tamarins.     

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.     

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.     

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.     

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.