Deterministic modelling of seed dispersal based on observed behaviours of an endemic primate in Brazil.

Plant species models are among the available tools to predict the future of ecosystems threatened by climate change, habitat loss, and degradation. However, they suffer from low to no inclusion of plant dispersal, which is necessary to predict ecosystem evolution. A variety of seed dispersal models have been conceived for anemochorous and zoochorous plant species, but the coupling between vegetation models and seed dispersal processes remains rare. The main challenge in modelling zoochoric dispersal is simulating animal movements in their complex habitat. Recent developments allow straightforward applications of hidden Markov modelling (HMM) to animal movements, which could ease generalizations when modelling zoochoric seed dispersal. We tested the use of HMM to model seed dispersal by an endangered primate in the Brazilian Atlantic forest, to demonstrate its potential simplicity to simulate seed dispersal processes. We also discuss how to adapt it to other species. We collected information on movement, fruit consumption, deposition, and habitat use of Leontopithecus chrysomelas. We analysed daily trajectories using HMM and built a deterministic Model Of Seed Transfer (MOST), which replicated, with good approximation, the primate's movement and seed deposition patterns as observed in the field. Our results suggest that the dispersal behaviour and short daily-trajectories of L. chrysomelas restrict the species' role in large-scale forest regeneration, but contribute to the prevalence of resource tree species locally, and potentially maintaining tree diversity by preventing local extinction. However, it may be possible to accurately simulate dispersal in an area, without necessarily quantifying variables that influence movement, if the movement can be broken down to step-length and turning angles, and parametrised along with the distribution of gut-transit times. For future objectives, coupling MOST with a DVM could be used to test hypotheses on tree species survival in various scenarios, simulating regeneration and growth at regional scales by including data on main dispersal agents over the area of interest, distribution of tree species, and land use data. The principal advantage of the MOST model is its functionality with data available from the literature as the variables are easy to parametrise. We suggest using the coupled model to perform experiments using only available information, but varying the numbers and species of seed dispersers, or modifying land cover or configuration to test for possible thresholds preventing the extinction of selected tree species.

Seasonal effects on testes size and sustained semen quality in captive golden-headed lion tamarins, Leontopithecus chrysomelas.

The golden-headed lion tamarin (Leontopithecus chrysomelas) is an endangered primate that, according to timing of births, there seems to have seasonal reproductive patterns in captive populations inhabiting the Southern Hemisphere. The extent to which male tamarins have circannual cyclic fluctuations in testicular functions, however, remains unknown. Changes in testis size and seminal variables, therefore, were evaluated during the rainy and dry seasons of the year in seven males. There was estimation of mating and birth seasons from the breeding colony using a 27 year database (229 birth records). Births were distributed throughout the year with peaks occurring in August-October and January-March (39.7 % and 30.5 % of all births, respectively). Semen collection using penile vibrostimulation was successfully induced in more than 96 % of the attempts regardless of the season (total of 75 ejaculates). Body mass did not vary significantly between seasons, but relative testes size was larger during the dry season. Values for none of the seminal variables (total sperm count, total and progressive motility, plasma membrane and acrosome integrity, and total sperm defects), however, were different during the rainy and dry seasons. These results indicate that testicular function in golden-headed lion tamarins may not be affected by daylength changes, and that seasonal patterns of female reproduction is perhaps more relevant for the reproductive timing of the species. Furthermore, the possibility of year-round production of ejaculates containing viable sperm broadens our perspective of preserving genetic diversity within the species because there is a greater opportunity for semen collection and freezing.

Individual behavioral differences and health of golden-headed lion tamarins (Leontopithecus chrysomelas).

Individual behavioral differences may influence how animals cope with altered environments. Depending on their behavioral traits, individuals may thus vary in how their health is affected by environmental conditions. We investigated the relationship between individual behavior of free-living golden-headed lion tamarins (Leontopithecus chrysomelas) responding to a novel object (to assess exploration-avoidance), and their habitat use and health status (endoparasitism; clinical measures: biometric data, heart rate, respiratory frequency, and temperature; fecal glucocorticoid metabolites). As parasite transmission can be affected by individual variation in social contact and social grooming, we also evaluated whether more sociable individuals show higher endoparasite loads compared with less sociable animals. Four groups living in landscapes with different levels of human disturbance were investigated: two in degraded forest fragments in an agricultural matrix (DFAM-higher disturbance), and two in a cocoa agroforestry system (cabruca-lower disturbance) in the Atlantic forest of South Bahia, Brazil. Using a subjective ratings approach, highly correlated adjective descriptors were combined to produce z-score ratings of one derived variable ("confidence"), which was selected to characterize the tamarins' exploration/avoidance responses during a novel object test. The higher the confidence score, the longer female tamarins spent foraging for prey independent of landscape, and the greater their body mass independent of sex and landscape. Only DFAM individuals showed intestinal parasite infection. Endoparasite loads were positively correlated with the number of grooming partners, suggesting an association between social grooming and transmission (more groomers = more endoparasites). Individual behavior, including in a test situation, may thus have some predictive value for behavior in a free-living context, and for its health consequences.

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

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

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.

Early reversal of ketamine/dexmedetomidine chemical immobilization by atipamezole in golden-headed lion tamarins (Leontopithecus chrysomelas).

BACKGROUND: A smooth and rapid recovery from anesthesia allowing safe release is desirable, especially for wild species. This study describes the clinical effects of the combination of dexmedetomidine and ketamine and the partial reversal with atipamezole in golden-headed lion tamarins. METHODS: Dexmedetomidine 10 µg kg-1 and ketamine 15 mg kg-1 were administered to 45 golden-headed lion tamarins undergoing vasectomy. Following surgery, animals were assigned to three groups: control (SAL; 0.9% NaCl), atipamezole 20 µg kg-1 (ATI20), and atipamezole 40 µg kg-1 (ATI40). RESULTS AND CONCLUSIONS: All animals presented great scores of sedation and muscle relaxation during the procedure. Recovery in the control group was smooth and uneventful. Salivation, muscle tremors, and head movements were observed in ATI 20 and ATI40. The administration of atipamezole did not change total recovery times (ATI20 69 ± 23 minutes; ATI40 72 ± 45 minutes; SAL 57 ± 23 minutes).

Unraveling the dispersal patterns and the social drivers of natal emigration of a cooperative breeding mammal, the golden lion tamarin.

The study of the social drivers of animal dispersal is key to understanding the evolution of social systems. Among the social drivers of natal emigration, the conspecific attraction, aggressive eviction, and reduced social integration hypotheses predict that sexually mature individuals who receive more aggressive behavior and are engaged in less affiliative interactions are more likely to disperse. Few reports have explored these proximate factors affecting emigration in cooperatively breeding species, particularly of Neotropical primates. In this study, we investigated the dispersal patterns and tested the social drivers of natal emigration in the golden lion tamarin (Leontopithecus rosalia) - an endangered species inhabiting Atlantic rainforests fragments in Brazil. We used behavioral and demographic data collected during 7 years from 68 groups of tamarins inhabiting 20 forest fragments. Our analyses from the 160 dispersing individuals showed that dispersal success is higher for males and for those engaged in parallel dispersal, but that males and females use different strategies to enhance their dispersal success, males immigrate into established groups while females form new groups. We did not find high levels of agonistic behavior among group members before natal emigration. Instead we found that conspecific attraction drives natal emigration in both sexes, while additionally the low level of affiliative interactions within the natal group triggers male emigration. We discuss natal emigration in the broader perspective of the cooperative breeding system and the implications of these findings for the conservation of the species.

Ultrasonographic aspects of the Leontopithecus gestation (Lesson, 1840-Callitrichidae, Primates).

BACKGROUND: There is a concern about conservation of endangered species today. Among this species, the Leontopithecus (Lesson, 1840) is outstanding. Its population has been whirling reduced. So far the reproductive physiology of Leontopithecus has few studies, it is fundamental requisite to preserve this species. Obstetric sonography has become an essential method in reproductive management of primates. METHOD: This method is very helpful to detect early pregnancy and evaluate some deficiency of fetal growth. In this study, 14 pregnancies were monitored using real-time abdominal sonography. During each evaluation, the number of fetus was recorded, gestational sac and heart beats were observed, and biparietal diameter was measured. RESULTS: The results showed that abdominal sonography is a reliable method for observation of gross morphological changes during pre-natal development and to estimate gestational age. No statistically differences were observed between twins and singletons. This study is the first investigation of pre-natal growth in Leontopithecus.

Preliminary findings on social and ecological correlates of a polyspecific association between a golden-headed lion tamarin (Leontopithecus chrysomelas) and Wied's marmosets (Callithrix kuhlii).

The advantages of living in a group include feeding benefits and/or predation avoidance, while the disadvantages are typically related to competition. One way to avoid competition while maintaining the benefits of living in a group is to form interspecific associations with species with relatively little dietary overlap. Here we report a stable association between a male golden-headed lion tamarin (GHLT), Leontopithecus chrysomelas, and a group of Wied's black-tufted-ear marmosets (WBTMs), Callithrix kuhlii. We collected ecological and behavioral data on a duo of GHLTs from May to August 2008, totaling 62 h of observations. On 19 August 2008, the radio-collared GHLT dispersed alone and was located on 28 August in association with WBTMs. To examine possible changes in GHLT ecology and behavior, we monitored the mixed-species group between September and December 2008, totaling 122 h of observations. We found that the GHLT's home range and daily path length decreased by about ten and three times, respectively, after joining the WBTM group, suggesting adaptations to the WBTMs' use of space. All non-agonistic behaviors recorded in the mixed group were directed from GHLT to the WBMTs, whereas all agonistic interactions were directed from the WBMTs to the GHLT, indicating a subordinate position of GHLT in the mixed group. In golden lion tamarins, reproductive success of subordinate adult males that remain in the group is higher than that of those that disperse and "prospect" for a breeding opportunity. If dispersing individuals are unable to find a mate and defend a territory, they will likely die within a year. The dispersing GHLT in this study assumed a subordinate role in a mixed-species group outside a GHLT territory. Apparently, the benefits of waiting for a dispersing female in a relatively safe situation may exceed the costs of prospecting elsewhere or being a subordinate.

Dispersal, group formation and kinship in the black-faced lion tamarin (Leontopithecus caissara).

We report on (i) new group formation, (ii) sex differences in dispersal and (iii) dispersal distance over 6 years for 3 social groups of the black-faced lion tamarin (Leontopithecus caissara) in the vicinity of Ariri, São Paulo state, Brazil. The groups were: Bina (monitored for 74 months), BM5 (52 months) and Teca (13 months). Each group was censused once a week and monitored for 3 days each month. Mating opportunities were found to be the incentive for young adult black-faced lion tamarins to either disperse or remain in their kin group. Young adults show delayed dispersal that is related to the cooperative breeding system characteristic of the Callitrichidae and to a low population density which hinders the formation of new breeding pairs. Our findings suggest that in L. caissara (i) both sexes disperse, (ii) successful immigration is related to breeding opportunities in an existing group, (iii) female immigration motivates male emigration and the formation of new groups, and (iv) emigrants tend to form new groups close to their natal groups. These patterns of dispersal and formation of new groups are efficient because the species has been able to avoid loss of genetic diversity despite their small population size.

Play behavior of the golden-headed lion tamarin in Brazilian cocoa agroforests.

During play, primates may become more vulnerable to predation. Our goal was to examine the potential role of predation risk on the play behavior of 3 groups of golden-headed lion tamarin, Leontopithecus chrysomelas, in shaded cocoa agroforest (cabruca) of Southern Bahia, Brazil. We identified the preferred (and safer) locations on vertical strata during playtime and investigated if frequency and duration of play differed according to group size. All groups preferred to play on the lower levels of vertical strata, which may be perceived as either a safer environment or as a more suitable location for play due to the vegetation structure. The smallest group played less than the others, while the largest group played more and for longer periods. Our data suggest that predation risk can influence where play takes place as well as its frequency and length.

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.

Chasing sounds.

Prior work with Wright and others demonstrated that rhesus monkeys recognized the relative relationships of notes in common melodies. As an extension of tests of pattern similarities, tamarins were habituated to 3-sound unit patterns in an AAB or ABB form that were human phonemes, piano notes, or monkey calls. The subjects were tested with novel sounds in each category constructed either to match the prior pattern or to violate the prior habituated pattern. The monkeys attended significantly more to a violation of their habituated pattern to a new pattern when human phonemes were used, and there was a trend difference in attention toward pattern violations with melodies. Monkey call patterns generated a variety of behavioral responses, were less likely to show habituation, and did not generate a strong attention reaction to changes in the patterns. Monkeys can extract abstract rules and patterns from auditory stimuli but the stimuli, by their nature, may generate competing responses which block processing of abstract regularities.

A comparison of the home range sizes of mainland and island populations of black-faced lion tamarins (Leontopithecus caissara) using different spatial analysis.

The critically endangered black-faced lion tamarin, Leontopithecus caissara, has a restricted geographical distribution consisting of small mainland and island populations, each with distinct habitats in coastal southeastern Brazil. Necessary conservation management actions require an assessment of whether differences in habitats are reflected in use of space by the species. We studied two tamarin groups on the mainland at São Paulo state between August 2005 and March 2007, and compared the results with data from Superagui Island. Three home range estimators were used: minimum convex polygon (MCP), Kernel, and the new technique presented dissolved monthly polygons (DMP). These resulted, respectively, in home ranges of 345, 297, and 282 ha for the 12-month duration of the study. Spatial overlap of mainland groups was extensive, whereas temporal overlap was not, a pattern that indicates resource partitioning is an important strategy to avoid intraspecific competition. L. caissara large home ranges seem to be dynamic, with constant incorporation of new areas and abandonment of others through time. The main difference between mainland and island groups is the amount and variety of sleeping sites. A better understanding of the home range sizes, day range lengths, and territorial behavior of this species will aid in developing better management strategies for its protection. Additionally, the presented DMP protocol is a useful improvement over the MCP method as it results in more realistic home range sizes for wildlife species.

Finite element analysis of performance in the skulls of marmosets and tamarins.

Reliance on plant exudates is a relatively rare dietary specialization among mammals. One well-studied example of closely related exudate feeders is the New World marmosets and tamarins. Whereas marmosets actively gouge tree bark with their incisors to stimulate the flow of sap, tamarins are opportunistic exudate feeders that do not gouge bark. Several studies of the dentaries and jaw adductors indicate that marmosets exhibit specializations for increased gape at the expense of bite force. Few studies, however, have looked to the cranium of marmosets for evidence of functional specializations. Using 3D finite element models of the marmoset Callithrix jacchus and the tamarin Saguinus fuscicollis, we investigated the performance of the cranium under loading regimes that mimicked unilateral molar biting and bark-gouging. We investigated three measures of performance: the efficiency with which muscle force is transferred to bite force, the extent to which the models are stressed (a predictor of failure), and the work expended by muscles as they deform the skull (total strain energy). We found that during molar biting the two models exhibited similar levels of performance, though the Saguinus model had slightly higher mechanical efficiency, a slightly lower state of stress, and expended more energy on deformation. In contrast, under the bark-gouging load, Callithrix exhibited much higher mechanical efficiency than Saguinas, but did so at the expense of more work and higher levels of von Mises stress. This analysis illustrates that differences in the shapes of the skulls of Callithrix and Saguinus confer differences in performance. Whether these aspects of performance are targets of selection awaits broader comparative analyses.

Morfologia macroscópica do aparelho reprodutor feminino de Leontopithecus cativos (Lesson, 1840) Primates-Callitrichidae / Gross morphology of the female genital tract of captive Leontopithecus (Lesson, 1840) Primates-Callitrichidae

Descreveu-se o sistema reprodutor feminino em três espécies de mico-leão Leontopithecus (Lesson 1840), cativos: L. rosalia, L. chrysopygus e L. chrysomelas. A vulva está delimitada pelos lábios vulvares menores e com clitóris conspícuo. A superfície do períneo urogenital apresenta elevações papilares mais concentradas nos lábios vulvares, conferindo-lhe aspecto rugoso. O vestíbulo vaginal constitui um tubo muscular de parede espessa que se estende da rima da vulva até o óstio da vagina. A vagina é um tubo muscular alongado e achatado dorsoventralmente, que comunica o vestíbulo vaginal ao colo uterino. O útero piriforme está localizado na porção caudal da cavidade abdominal. Craniolateralmente abrem-se tubas uterinas convolutas e ovários grosseiramente fusiformes de superfície lisa.

It is described the female genital tract of three species of lion tamarin: Leontopithecus rosalia, L. chrysopygus, and L. chrysomelas. Fifteen animals were selected from the Museum of the Center of Primatology of Rio de Janeiro - CPRJ/FEEMA. The vulva is delimited by the labia and has a conspicuous clitoris. The surface of the urogenital perineum has papillary elevations more concentrated in the labia, which results in a rough aspect. The vestibule is a thick-walled muscular tube, extending from the pudendal cleft to the vaginal orifice. The vagina is an elongated and flat muscular tube, which communicates dorsoventrally the vestibulum and the cervix of uterus. The pyriform uterus is located in the caudal portion of the abdominal cavity. Craniolaterally, the convolute uterine tubes open, enveloping the ovaries, which are roughly fusiform with a smooth surface.

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.

Frugivory and seed dispersal of golden lion tamarin (Leontopithecus rosalia (Linnaeus, 1766)) in a forest fragment in the Atlantic Forest, Brazil / Frugivoria e dispersão de sementes por Micos-Leões-Dourados (Leontopithecus rosalia) em um fragmento florestal na Mata Atlântica, Brasil

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.

A influência do mico-leão-dourado (Leontopithecus rosalia) como dispersor de sementes foi estudada através do monitoramento de dois grupos de micos de dezembro de 1998 a dezembro de 2000 (871,9 horas de observações) em um fragmento florestal no Sudeste do Brasil. Os micos consumiram frutos de 57 espécies de pelo menos 17 famílias. Eles ingeriram sementes de 39 espécies, e 23 destas foram colocadas para germinar no laboratório e/ou no campo. L. rosalia é um dispersor de sementes legítimo porque sementes de todas as espécies testadas germinaram após a ingestão, mesmo que em baixas porcentagens. Esses primatas não apresentam um efeito consistente na germinação final de sementes, porque beneficiam algumas espécies enquanto prejudicam outras. Sementes predadas ou digeridas foram procuradas nas fezes.

Tree and forest characteristics influence sleeping site choice by golden lion tamarins.

Lion tamarin monkeys are among a small number of primates that repeatedly use a few tree holes for the majority of their sleeping sites. To better understand why lion tamarins rely on tree holes as sleeping sites, we compared the physical characteristics of frequently used sleeping sites, infrequently used sleeping sites, and randomly selected forest locations at multiple spatial scales. From 1990 to 2004, we recorded 5,235 occurrences of sleeping site use by 10 groups of golden lion tamarins (Leontopithecus rosalia) in Poço das Antas Reserve, Rio de Janeiro State, Brazil. Of those, 63.6% were tree holes. Bamboo accounted for an additional 17.5% of observations. Frequently used tree holes were more likely to be found in living trees and their entrances were at lower canopy heights than infrequently used tree holes. We also found that frequently used sleeping sites, in comparison to random sites, were more likely to be found on hillsides, be close to other large trees, have a lower percent of canopy cover, and have larger diameter at breast height. Topography and small-scale variables were more accurate than were habitat-level classifications in predicting frequently used sleeping sites. There are ample tree holes available to these lion tamarins but few preferred sites to which they return repeatedly. The lion tamarins find these preferred sites wherever they occur including in mature forest and in relics of older forest embedded in a matrix of secondary forest.