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PubMed2003

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/km(2) to 2.35 groups/km(2) (2.17 individuals/ km(2) to 8.53 individuals/km(2)). Six of the isolated groups found during the survey were successfully translocated to a forest of 2400 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.

Animals↗
PubMed2001

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

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

Animals↗
PubMed2003

Characteristics of reproductive biology and proximate factors regulating seasonal breeding in captive golden-headed lion tamarins (Leontopithecus chrysomelas).

Reproduction is highly demanding in terms of energy expenditure, and the costs and benefits associated with postponing or investing in a reproductive effort are crucial determinants of an individual's fitness. Understanding the reproductive potential of a species under varying ecological conditions offers important insights into the dynamics of its social system. This study provides the first detailed analysis of the reproductive potential of wild- and captive-born golden-headed lion tamarins (Leontopithecus chrysomelas) under captive conditions, based on studbook data compiled during 1984-2000. Litters produced by wild-born females breeding in captivity are similar in size to litters observed in the wild, but smaller than litters of captive-born females. The more stringent ecological conditions experienced by wild-born females during maturation may result in a lifelong effect on litter size. However, interbirth intervals are shorter for wild-born than captive-born females. The relatively smaller burden of infant care that results from having smaller litters may allow wild-born females to sustain the next pregnancy sooner. Reproduction in the Brazilian captive population is highly seasonal for both wild-born females and females born in captivity in Brazil. Changes in photoperiod over a year provide a proximate explanation for changes in the proportion of conceptions and births per month. Outside Brazil, breeding occurs year-round, and no clear birth peak is apparent. Information from field reports that could be used to relate this finding to ecological factors, such as resource availability, is unavailable.

Animals↗
PubMed2001

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.

Age Factors↗
PubMed2002

Does the milk of Callitrichid monkeys differ from that of larger anthropoids?

The generalization that anthropoid primates produce dilute milks that are low in protein and energy is based primarily on data from large monkeys of the families Cebidae and Cercopithecidae, as well as humans. The marmosets and tamarins (Callitrichidae) are not only much smaller in body size, but also typically raise multiple offspring during a relatively brief lactation. We hypothesized that selection for small body size and high reproductive rate might favor secretion of milk of higher energy and protein concentrations. To test this hypothesis, 46 milk samples collected from 10 common marmosets (Callithrix jacchus, ca. 350 g) were assayed for dry matter (DM), crude protein (CP), fat, and sugar; and gross energy (GE) was calculated from these constituents. We also assayed five samples collected from three golden lion tamarins (Leontopithecus rosalia, ca. 700 g) and six samples collected from a single pygmy marmoset (Cebuella pygmaea, ca. 150 g) over two lactation periods. All samples were collected between days 10 and 57 post partum, representing mid lactation for these species. The milks of these three species were similar, containing 14.0%, 16.1%, and 13.7% DM; 2.7%, 2.6%, and 2.9% CP; 3.6%, 5.2%, and 3.7% fat; 7.4%, 7.2%, and 7.8% sugar; and 0.76, 0.90, and 0.82 kcal/g for common marmosets, golden lion tamarins, and the pygmy marmoset, respectively. These species produced milks with energy values that were within the range reported for large anthropoids, albeit with slightly higher protein concentration. However, milk composition did vary substantially among individual common marmoset females, especially in the proportion of milk energy derived from fat. In contrast, CP as expressed as a percent of GE was remarkably constant among common marmoset females. Callitrichid milk appeared to be similar to that of larger anthropoid primates in GE, but was higher in CP and in the proportion of GE from CP. However, the small sample sizes for the golden lion tamarin and the pygmy marmoset, and the wide variation in milk composition found among common marmoset females cautions against definitively characterizing the milks of callitrichids from these data.

Animals↗
PubMed2004

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.

Acclimatization↗
PubMed2004

Diet, foraging, and use of space in wild golden-headed lion tamarins.

Lion tamarins (Callitrichidae: Leontopithecus) are small frugi-faunivores that defend large home ranges. We describe results from the first long-term investigation of wild golden-headed lion tamarins (L. chrysomelas; GHLTs). We present data about activity budgets, daily activity cycles, diet, daily path length, home range size, home range overlap, and territorial encounters for three groups of GHLTs that were studied for 1.5-2.5 years in Una Biological Reserve, Bahia State, Brazil, an area characterized by aseasonal rainfall. We compare our results to those from other studies of lion tamarins to identify factors that may influence foraging and ranging patterns in this genus. Ripe fruit, nectar, insects, and small vertebrates were the primary components of the GHLT diet, and gums were rarely eaten. Fruit comprised the majority of plant feeding bouts, and the GHLTs ate at least 79 different species of plants from 32 families. The most common foraging sites for animal prey were epiphytic bromeliads. The GHLTs defended large home ranges averaging 123 ha, but showed strong affinities for core areas, spending 50% of their time in approximately 11% of their home range. Encounters with neighboring groups averaged two encounters every 9 days, and they were always aggressive. Data about time budgets and daily activity cycles reveal that the GHLTs spent most of their time foraging for resources or traveling between foraging sites distributed throughout their home ranges. The GHLTs spent much less time consuming exudates compared to lion tamarins in more seasonal environments. Additionally, the GHLTs had much larger home ranges than golden lion tamarins (L. rosalia), and did not engage in territorial encounters as frequently as L. rosalia. GHLT ranging patterns appear to be strongly influenced by resource acquisition and, to a lesser extent, by resource defense.

Age Factors↗
PubMed2004

Isolation and identification of fungi from vaginal flora in three species of captive Leontopithecus.

The ability to reproduce in captivity is an essential component of lion tamarin (Leontopithecus) conservation programs. However, infections such as vaginitis, cervicitis, and endometritis are important diseases that may influence the reproduction of these animals. Therefore, it is important to detect continuous or occasional vaginal microbial populations, and to understand their potential role as an endogenous source of infection [Collins, 1964; Blue, 1983; Pugh et al., 1986]. Vaginal swabs were collected from 25 female tamarins of the three currently available species (L. rosalia, L. chrysopygus, and L. chrysomelas) at the Center of Primatology in Rio de Janeiro, Brazil. The swabs were processed according to standard mycological protocols, and isolates were biochemically characterized. Fungal isolates were recovered from 16 animals (64.0%). The results showed that 70.6% of the isolated microorganisms consisted of yeast, including three species of Candida (mainly C. glabrata). We suggest that this species is a resident member of the normal vaginal flora in Leontopithecus. Filamentous fungi (mainly from Trichosporon, Aspergillus, and Penicilliumgenera) constituted 29.4% of the isolates, and were considered to be transitory contaminants of the genital area. We suggest that colonization of the vaginal environment is related to the endocrine pattern associated with the reproductive status of these animals, but not to parity.

Animals↗
PubMed2005

Interpopulation differences in exudate feeding of pygmy marmosets in Ecuadorian Amazonia.

Local variations in fruit- and leaf-eating have been reported for some primate species; however, similar variations in exudate-feeding of pygmy marmosets, one of the most specialized neotropical primate species, have not been studied. In our 3-year study of four populations of pygmy marmosets in northeastern Ecuador, we characterized their exudate-feeding behavior by describing the use of exudate sources. We tested whether the use of exudate species was related to ecological factors such as the availability of exudate species in an area. We estimated the daily activity budgets of the groups with 1-hr scan samples and found significant interpopulation differences in the time spent on exudate feeding. We recorded a total of 18 exudate species used in the four populations; however, the populations differed in the total number of species used and in the preferred species. The most commonly used plant species were Sterculia apetala at San Pablo, Cedrela odorata at Sacha, Inga marginata at Amazoonico, and Parkia balslevii at Zancudo. We recorded the presence and abundance of the 18 exudate species in 90-m transects in the home range of each group and in one additional control area that contained no marmosets, for each population. Differences in the most-used exudate species among populations did not appear to be related to the availability of these species in each population, i.e., the marmosets did not use at random the exudate species available within their range, nor did they use more often the exudate species that were more abundant in their home ranges. One implication of our results for conservation is that protecting exudate resources based on data from only one area will not be sufficient to preserve pygmy marmosets in all populations.

Animals↗
PubMed2005

Age differences in neophilia, exploration, and innovation in family groups of callitrichid monkeys.

The prevailing assumption in the primate literature is that young or juvenile primates are more innovative than adult individuals. This innovative tendency among the young is frequently thought to be a consequence, or side effect, of their increased rates of exploration and play. Conversely, Reader and Laland's [International Journal of Primatology 22:787-806, 2001] review of the primate innovation literature noted a greater reported incidence of innovation in adults than nonadults, which they interpreted as (in part) a reflection of the greater experience and competence of older individuals. Within callitrichids there is contradictory evidence for age differences in response to novel objects, foods, and foraging tasks. By presenting novel extractive foraging tasks to family groups of callitrichid monkeys in zoos, we examined, in a large sample, whether there are positive or negative relationships of age with neophilia, exploration, and innovation, and whether play or experience most facilitates innovation. The results indicate that exploration and innovation (but not neophilia) are positively correlated with age, perhaps reflecting adults' greater manipulative competence. To the extent that there was evidence for play in younger individuals, it did not appear to contribute to innovation. The implications of these findings for the fields of innovation and conservation through reintroduction are considered.

Age Factors↗
PubMed2005

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 Poço 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.

Animals↗
PubMed2003

Comparative functional analysis of skull morphology of tree-gouging primates.

Many primates habitually feed on tree exudates such as gums and saps. Among these exudate feeders, Cebuella pygmaea, Callithrix spp., Phaner furcifer, and most likely Euoticus elegantulus elicit exudate flow by biting into trees with their anterior dentition. We define this behavior as gouging. Beyond the recent publication by Dumont ([1997] Am J Phys Anthropol 102:187-202), there have been few attempts to address whether any aspect of skull form in gouging primates relates to this specialized feeding behavior. However, many researchers have proposed that tree gouging results in larger bite force, larger internal skull loads, and larger jaw gapes in comparison to other chewing and biting behaviors. If true, then we might expect primate gougers to exhibit skull modifications that provide increased abilities to produce bite forces at the incisors, withstand loads in the skull, and/or generate large gapes for gouging. We develop 13 morphological predictions based on the expectation that gouging involves relatively large jaw forces and/or jaw gapes. We compare skull shapes for P. furcifer to five cheirogaleid taxa, E. elegantulus to six galagid species, and C. jacchus to two tamarin species, so as to assess whether gouging primates exhibit these predicted morphological shapes. Our results show little morphological evidence for increased force-production or load-resistance abilities in the skulls of these gouging primates. Conversely, these gougers tend to have skull shapes that are advantageous for creating large gapes. For example, all three gouging species have significantly lower condylar heights relative to the toothrow at a given mandibular length in comparison with closely related, nongouging taxa. Lowering the height of the condyle relative to the mandibular toothrow should reduce the stretching of the masseters and medial pterygoids during jaw opening, as well as position the mandibular incisors more anteriorly at wide jaw gapes. In other words, the lower incisors will follow a more vertical trajectory during both jaw opening and closing. We predict, based on these findings, that tree-gouging primates do not generate unusually large forces, but that they do use relatively large gapes during gouging. Of course, in vivo data on jaw forces and jaw gapes are required to reliably assess skull functions during gouging.

Anatomy, Comparative↗
PubMed2003

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.

Adaptation, Biological↗
PubMed1975

Phylogenetic implications of comparative primate growth rates.

Growth data from a number of species of Old and New World primates have been analyzed by calculating instantaneous relative growth rates. Species discussed are the New World species Saimiri sciureus and Saguinus nigricollis, and the Old World species Pan troglodytes and Macaca mulatta. The analysis of the perinatal growth data indicated that differences in relative growth rates are present during early periods of growth. More specifically, it was found that the closer taxonomically a species is to man the greater the deceleration of growth during the first postnatal year. It is suggested that this may be a general primate trend.

Age Factors↗
PubMed1983

Functional implications of skeletal diversity in two South American tamarins.

This study examines the relationship between positional behavior and morphology for two closely related South American tamarin species, Saguinus fuscicollis illigeri and Saguinus oedipus oedipus. Although never systematically documented, the two species are suspected of exhibiting highly similar yet subtly different locomotor behaviors with a greater propensity for climbing, springing, and more powerful leaping in S. oedipus. Fourteen measurements reflecting biomechanical structuring were taken from the postcranial skeleton of 28 individuals of each species. The data were reduced to principal component scores and subjected to a multiple analysis of variance to determine the extent of intergroup skeletal variation. Areas of significant skeletal diversity were interpreted functionally. The results suggest that the differences in functional patterning among the two species is consistent with the behavioral hypothesis. It is concluded that subtle changes in positional behavior may be capable of altering skeletal morphology.

Analysis of Variance↗
PubMed1984

The ecological role of the callitrichidae: a review.

The marmosets and tamarins fill a unique ecological role among the anthropoid primates, one that has not been fully recognized. Many misconceptions--that they are primitive, monogamous, territorial, and squirrellike--pervade the literature. These misconceptions are largely the result of misinterpreting laboratory studies which have not been confirmed with identified animals in natural habitats. Recent field studies, reviewed here, indicate that marmosets and tamarins have a highly derived ecological role, are not monogamous, feed largely on insects and plant exudates, and have uniquely specialized positional behavior involving clinging to vertical tree trunks in order to feed on exudates. Accompanying these behavioral traits are a number clawlike nails on all digits except the hallux, and a three-cusped upper molar morphology. These form a suite of characteristics unique among the living primates, many of which are related to their ecological role. We believe that the marmosets and tamarins are members of a guild of exudate feeders in which plant exudates are an important component of the diet. It is within this framework of a primate foraging guild that we can best understand many of their morphological and behavioral adaptations.

Animals↗
PubMed1984

Ecological distinctions between sympatric species of Saguinus and Sciurus.

Tamarins are small New World monkeys that have been described as "squirrellike." Squirrels, along with bats and birds, are the taxa most likely to utilize resources similar to those used by primates in the tropical forest canopy. In this paper we compare differences in ecology, diet, locomotion, and habitat utilization between sympatric populations of tamarins (Saguinus oedipus) and tree squirrels (Sciurus granatensis) in Panama. Data presented indicate that although there is some degree of resource overlap, patterns of habitat utilization differ significantly. Rather than being "squirrellike," the Panamanian tamarin exhibits a pattern of locomotor and feeding behavior consistent with that found in other arboreal primates.

Animals↗
PubMed1985

Forelimb anatomy of New World monkeys: myology and the interpretation of primitive anthropoid models.

The forelimbs of 12 genera of New World monkeys, two genera of Old World monkeys, and a gibbon were dissected. Of the 54 muscles examined, 19 exhibited significant intergeneric variation. We present arguments for which morphologies are primitive and which are derived within platyrrhines and within anthropoids. We conclude that the forelimbs of Cebus apella and Callicebus moloch represent good models of the ancestral anthropoid morphology. Thus among living anthropoids they are most appropriate for comparisons with early fossil anthropoids. They are also useful for determining whether myological anomalies of human aneuploids are atavistic. Wagner tree analyses were conducted to assess the value of these myological characters in phylogenetic studies of platyrrhines. In most respects the Wagner trees were consonant with phylogenies previously proposed, although some hypothesized trees are less parsimonious than others in explaining our data. There is an unexpected number of derived features shared by Aotus and the Atelines. There are marked dissimilarities in forelimb musculature between Aotus and Callicebus.

Alouatta↗