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.     

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.     

Food sharing among captive Leontopithecus rosalia.

Captive L. rosalia were observed to exchange food routinely in family groups, a process varying from donation to theft. Donation involved the use of 'invitational' signals which operated most efficiently in parent-infant sharing and in donating live prey. Food moved, by sharing and theft, toward: (a) males prior to the female's first conception; (b) females during late pregnancy; (c) carriers of infants; (d) weanlings; (e) juveniles when infants died; (f) third animals in trios, regardless of their age and relatedness to the pair. Successful reproduction, a complex behavior involving all group members in cooperative infant care and provisioning, is probably enhanced by captive L. rosalia's food-sharing habits.     

Ontogenetic characteristics of the vomeronasal organ in Saguinus geoffroyi and Leontopithecus rosalia,with comparisons to other primates

It has been suggested that the variability of the primate vomeronasal organ (VNO) may be greater than previously thought, especially among New World monkeys. It is not clear to what extent VNO variation reflects ontogenetic, functional, or phylogenetic differences among primates. The present study investigated VNO anatomy in an ontogenetic series of two genera of callitrichid primates, in order to assess recent attempts to develop VNO character states and to examine the evidence for VNO functionality at different life stages. A sample of six Leontopithecus rosalia, one L. chrysomelas, and six Saguinus geoffroyi was serially sectioned and stained using various methods. Two adult Callithrix jacchus were also sectioned for comparative purposes. The VNO of each primate was examined by light microscopy along its entire rostrocaudal extent. VNOs of the tamarins were described to determine whether they fit into 1 of 3 character states recently attributed to various New World monkeys. At birth, the two species of tamarins differed in the nature of communication between the VNO and nasopalatine duct (NPD). Two of 3 neonatal S. geoffroyi exhibited a fused VNO duct in a more dorsal position (adjacent to the nasal cavity) compared to that of L. rosalia. The VNO duct communicated with the NPD and was patent in neonatal L. rosalia. Both species appeared to have an age-related increase in the amount of sensory epithelium in the VNO. Subadult L. rosalia had caudal regions of the VNO that were exceptionally well-developed, similar to those of strepsirhine primates. Compared to subadults, all adult callitrichids appeared to have more ventral communications of the VNO duct directly into the NPD. Adult S. geoffroyi and L. chrysomelas both had VNO sensory epithelium separated by multiple patches of nonsensory epithelium. This contrasted with the VNOs of C. jacchus, which had a nearly continuous distribution of receptors on all surfaces of the VNO. The findings indicate that tamarins have delayed maturation of the VNO epithelium, and that some species have little or no perinatal function. These results also suggest that ontogenetic changes in craniofacial form may alter the position of the VNO in tamarins. The present study supports the use of at least two character states to categorize the VNO of various callitrichids, but it is suggested that one of these, previously called "reduced sensory epithelium" should be instead termed "interrupted sensory epithelium." The distribution of VNO sensory epithelium does not appear to reflect phylogenetic influences; it is more likely a functional characteristic that varies throughout postnatal life. Therefore, this chemosensory system has a high degree of plasticity relating to age and function, which in some instances can confound the use of characteristics as phylogenetic traits. Further study is needed to quantify VNO receptors in various species to determine if functional differences exist and if some species have more precocious VNO function than others.     

Frugivory and seed dispersal of golden lion tamarin (Leontopithecus rosalia (Linnaeus, 1766)) in a forest fragment in the Atlantic Forest, Brazil

The influence of the golden lion tamarin (Leontopithecus rosalia) as a seed disperser was studied by monitoring two groups of tamarins from December 1998 to December 2000 (871.9 hours of observations) in a forest fragment in south-east Brazil. The tamarins consumed fruits of 57 species from at least 17 families. They ingested the seeds of 39 species, and 23 of these were put to germinate in the laboratory and/or in the field. L. rosalia is a legitimate seed disperser because the seeds of all species tested germinated after ingestion, albeit some in low percentages. These primates do not show a consistent effect in final seed germination, because they benefit some species while damaging others. Feces were examined for seeds that had been preyed upon or digested.     

Chromosomal evolution in the African Arvicanthine rats (Murinae, Rodentia): comparative cytogenetics of Lemniscomys (L. zebra, L. rosalia, L. striatus) and Arvicanthis dembeensis

Chromosomenevolution bei den afrikanischen arvicanthinen Ratten (Murinae, Rodentia): Vergleichende Cytogenetik von Lemniscomys (L. zebra, L. rosalia, L. striatus) und Arvicanthus dembeensis
Chromosomenbänderungsanalysen (G- und C- Bänderung) wurden an zwei Arten von Lemniscomys ( L. zebra, L. rosalia ) und einer dritten Art aus Benin ( L. striatus ) durchgeführt, um den Verlauf der Chromosomenevolution in dieser Gattung zu verfolgen. Ein Mustervergleich mit der G-Bänderung macht es möglich, die Umstrukturierung der Chromosomen der Karyotypen zu erkennen. Die beiden Arten aus Tansania ( L. rosalia 2n=54, FNa=62; und L. zebra 2n=54, FNa=58) sind durch zwei perizentrische Inversionen voneinander unterschieden. Ein Polymorphismus für das X-Chromosom findet sich in beiden Arten. L. rosalia zeigt außerdem zwei verschiedene Formen des Y-Chromosoms. Das Bänderungsmuster von L. striatus (2n=44, FNa=68) aus Benin läßt im Vergleich zu L. zebra fünf Robertsonsche Fusionen erkennen. Außerdem ist der Karyotyp von L. rosalia aus Tansania verschieden von dem der für Südafrika (2n=48, FNa=62) beschrieben wurde und sollte daher als eine eigene Art betrachtet werden. Eine vergleichende Bänderungsanalyse mit einer anderen arvicanthinen Art ( Arvicanthus dembeensis, 2n=62, FNa=62) zeigt zwischen den beiden Gattungen eine vollständige Homologie in den G-Banden und die Unterschiede beruhen ausschließlich auf Tandem-Fusionen, perizentrischen Inversionen und Robertsonschen Fusionen.     

Comparative chromosome analysis (R- and C-bands) of two South African murid species, Lemniscomys rosalia and Rhabdomys pumilio (Rodentia, murinae)

We carried out a comparative chromosome analysis (R- and C-bands) on two South African murid rodent species, Lemniscomys rosalia and Rhabdomys pumilio, whose banded karyotypes are reported here for the first time. The study revealed that, in spite of minor differences in diploid number and the number of autosomal arms (48 vs. 46 and 58 vs. 60, respectively), these species differ by at least 10 structural rearrangements, comprising seven Robertsonian translocations (two of which share monobrachial homology), two tandem translocations, and one pericentric inversion. Despite the high level of chromosomal differentiation observed, almost complete homologous banding patterns were detected between the two species. The present study therefore strengthens the hypothesis about the close phylogenetic affinities between L. rosalia and R. pumilio and their belonging to a set of genera referred to as "arvicanthine" rodents.     

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.     

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.     

Pattern of late DNA replication of the allocyclic X chromosome in Cebus apella and Leontopithecus rosalia chrysomelas fibroblasts

The pattern of late DNA replication in the allocyclic X chromosome has been studied in the primary fibroblasts of two neotropical primates (Cebus apella and Leontopithecus rosalia chrysomelas). A comparison with previous reports showed a pattern identical with that of (1) the allocyclic X chromosome of human fibroblasts, and (2) the allocyclic X chromosome of rhesus and Cebus lymphocytes. Our results show that at least in one species (C. apella), and probably in rhesus and Leontopithecus, there is no tissue-specific difference between the late DNA replication patterns of the allocyclic X chromosome as there is between human lymphocytes and fibroblasts.     

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.     

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.     

Energy intake, energy expenditure, and reproductive costs of female wild golden lion tamarins (Leontopithecus rosalia)

Callitrichid females are often described as energetically constrained. We examined the energy budgets of 10 female wild golden lion tamarins (GLTs, Leontopithecus rosalia) in an effort to understand how energy intake and expenditure might influence physical condition and therefore reproductive performance. We used focal animal sampling to record behavioral data and conducted energy analyses of foods consumed by GLTs to estimate intake and expenditure. We used two-tailed Wilcoxon signed-rank tests to compare intake in the reproductive vs. nonreproductive period and expenditure in the reproductive vs. nonreproductive period. Energy intake decreased during the reproductive period compared to the nonreproductive period. While total expenditure did not vary significantly across the two periods, females spent more time and therefore expended significantly more energy engaged in energetically inexpensive behaviors (i.e., sleeping or being stationary) during the reproductive period compared to the nonreproductive period. We suggest that reproductive female GLTs may adopt a reproductive strategy that includes high intake prior to pregnancy and lactation, and energy conservation during pregnancy and lactation.     

Provisioning of Young in Golden Lion Tamarins (Callitrichidae, Leontopithecus rosalia): A Test of the Information Hypothesis

Provisioning of young after weaning or fledging is a highly variable phenomenon. Among cooperative breeders, such as marmosets and tamarins, both parents and natal adults may provision immatures. Experiments designed to measure the effects of food familiarity on food-transfer interactions were conducted on zoo-living golden lion tamarin, Leontopithecus rosalia , families to test one proposed benefit of provisioning to recipient young — that immature callitrichids learn food preferences through exposure to food items obtained from older group members. Adults transferred to immatures foods that were known to adults, but novel to immatures, and foods that were novel to all more frequently than foods that were familiar to both adults and immatures. Results suggest that adults alter their behavior such that learning by immatures is fostered. Immatures also were less likely to reject new foods acquired from other group members, compared with those obtained independently, suggesting the possibility that immatures attend to food transfer to facilitate incorporation of new foods into the diet. In contrast, anecdotal accounts of wild marmoset and tamarin food transfer have indicated that infants receive from adults foods that primarily are high in lipids and/or protein, as expected if provisioning acts to supplement nutrition. These apparently contradictory findings may reflect the differing effects of the captive and wild environment on food-transfer behavior or may point to a dual function of provisioning dependent on age of the recipient.     

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.     

Stereology of the myocardium in Leontopithecus (Lesson, 1840) callitrichidae - primates

Rare morphological features of the Leontopithecus cardiovascular system have been reported in the literature. The samples analyzed in this study came from 33 specimens of Leontopithecus from the collection of the Center of Primatology of Rio de Janeiro-FEEMA (CPRJ-FEEMA). Morphometry and stereological data were obtained from all animals. Adult body weights of L. rosalia were the lowest, the greatest being those of L. chrysopygus caissara; body weights of L. chrysomelas and L. c. chrysopygus were similar and in between those of the two former species. Cardiomyocytes (left ventricular myocardium) were bigger in adults than in infants. The myocardium of L. rosalia showed focal fibrosis, fatty vacuoles, and hyalinization. In L. chrysomelas the myocardium showed areas of fibrosis and presence of mononuclear cells. Fibrosis and areas of congestion were observed in L. c. chrysopygus; areas of disorganization and vascular congestion were found in L. c. caissara. In L. rosalia infants, a greater density of vessels per myocardial area and a greater length density of vessels were observed as compared with those of L. chrysomelas. In adults, L. chrysomelas showed greater density of connective tissue in the myocardium than L. c. chrysopygus and L. c. caissara did. In L. rosalia, cardiomyocyte nuclei had a greater area density than those of the other forms of Leontopithecus. These characteristics may explain the faster development of L. rosalia infants as compared with that of L. chrysomelas and L. c. chrysopygus kept under the same handling conditions at the CPRJ-FEEMA.     

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.     

Comparative chromosome morphology in three Callitrichid genera: Cebuella, Callithrix, and Leontopithecus

A G-band karyotypic analysis was carried out in individual species groups of three Callitrichid primate genera: Cebuella, Callithrix, and Leontopithecus. Within Callithrix, the karyotypes of the morphologically distinct and geographically isolated morphotypes C. jacchus jacchus and C. jacchus penicillata were identical. Within the lion tamarin genus, Leontopithecus, the karyotypes of the three morphotypes (L. rosalia rosalia, L. rosalia chrysomelas and L. rosalia chrysopygus) were also indistinguishable from one another. These results are consistent with the taxonomic designation of subspecies rank to the different morphotypes. A comparison of type specimens among the three Callitrichid genera showed that their phyletic radiation has been paralleled by a limited number of chromosome rearrangements and a relatively high amount of karyotypic invariance. A fusion/fission event has been postulated to account for the difference in diploid number between Cebuella (2n = 44) and the other species (2n = 46). The karyotype of Callithrix jacchus was found to be more directly derived from Cebuella than was that of Leontopithecus. These findings differ from the previous proposition that Leontopithecus might have diverged from a common Callitrichid ancestor before the emergence of the genus Callithrix.     

Distribution and ecology of the genusLeontopithecus lesson, 1840 in Brazil

The three forms of the genusLeontopithecus are found only in restricted localities in the States of Rio de Janeiro (Leontopithecus rosalia rosalia), Bahia and Espirito Santo (Leontopithecus rosalia chrysomelas) and São Paulo (Leontopithecus rosalia chrysopygus) in southeastern Brazil. All three are gravely threatened with extinction, mainly by destruction of primitive forest habitat. Diet ofLeontopithecus ssp. consists of fruit, buds, small vertebrates and insects. Group size varies from two to eight, but temporary congregations of up to 15–16 have been observed. Within the forest, the animals frequent the middle layers of the canopy, between three and ten meters above the ground.     

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.