Wild Golden Lion Tamarins Research Articles

Intergroup food transfers in wild golden lion tamarins (Leontopithecus rosalia)

The transfer of food between adults is uncommon in primates. Although golden lion tamarins (Leontopithecus rosalia) are unique among primates in the extent to which they transfer food, reports of food transfers between adults have so far been restricted to captive or reintroduced individuals. Here, I report the first recorded events of adult–adult food transfers in golden lion tamarins between individuals belonging to different groups in the wild. Given that individuals emigrate from their natal group to find reproductive opportunities, I suggest that intergroup food transfers could be a way for individuals to estimate the quality or availability of potential mates or social partners. I propose an additional function of food transfers in wild golden lion tamarins: that they create and strengthen social bonds with individuals outside of the family group.

The role of food transfers in wild golden lion tamarins (Leontopithecus rosalia): Support for the informational and nutritional hypothesis

Callitrichidae is a unique primate family not only in terms of the large number of food transfers to infants but also for the prevalence of transfers that are initiated by the adults. It has been hypothesized that, as well as provisioning infants, callitrichid food transfers might function to teach the receiver what food types to eat. If food provisioning has a teaching function, we would expect successful food transfers to be more likely with food types that are novel to the juveniles. We would also expect juveniles to learn about foods from those transfers. We introduced different types of food (some familiar, some novel) to wild groups of golden lion tamarins (Leontopithecus rosalia). While novel foods were not more successfully transferred than familiar food in the experiment, transfers were more successful (i.e., the receiver obtained food) when the donor had previous experience with that food. Moreover, we found evidence suggesting that food transfers influenced the future foraging choices of juveniles. Our findings are consistent with the first and third criteria of the functional definition of teaching, which requires that tutors (the adults) modify their behavior in the presence of a naïve individual (a juvenile), and that the naïve individual learns from the modified behavior of the demonstrator. Our findings are also consistent with the provisioning function of food transfer. Social learning seems to play an important role in the development of young tamarins’ foraging preferences.

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.

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.

The impact of concomitant infections by Trypanosoma cruzi and intestinal helminths on the health of wild golden and golden-headed lion tamarins

A 4-year longitudinal epidemiological study was carried out to evaluate the effect of infection by Trypanosoma cruzi and three intestinal helminth species on the health of golden and golden-headed lion tamarins. We evaluated health using analysis of blood counts, serum proteins, electrophoretograms, electrocardiograms and a health ranking based on physiological parameters. Among the helminths, Trichostrongylidae was demonstrated as the most pathogenic, followed by Prosthenorchis sp.; concomitant infection by Spiruridae may exacerbate the negative effects of the other two helminths. T. cruzi infection was not highly detrimental to the health of the study animals and was correlated with increased resilience to helminths. Tamarins younger than 1-year of age or older than 4-years had lower health condition. Golden-headed lion tamarins were in lower health condition because of higher parasitic prevalence. Our data suggest that when parasite community pathogenicity and prevalence are high, natural selection will allow survival only of lion tamarins in the best health condition.

Ontogeny of provisioning in two populations of wild golden lion tamarins (Leontopithecus rosalia)

Provisioning weaned young is an important part of the cooperative rearing system of marmosets and tamarins (family: Callitrichidae). Juvenile callitrichids receive a substantial proportion of their diet from all adult group members, whereas juveniles of most other primate species only receive food from the mother infrequently via scrounging. We conducted a longitudinal study of provisioning to 21 young wild golden lion tamarins through their first year of life in two Brazilian reserves. Juveniles were predicted to experience higher provisioning rates at the site with mature forest (the presumed ancestral habitat) and in territories that contained a higher proportion of preferred habitat within the mature forest reserve. Key measures of provisioning did not differ substantially between habitat types. The rates at which juveniles begged for food were very similar across habitats, while the influence of habitat on the rates at which juveniles received food was small and varied across age groups. The most pronounced differences between the reserves were: adult resistance to food-transfer attempts was less frequent, food-offering calls before food transfer were more frequent, and the proportion of prey provisioned was higher in the reserve in which earlier successional-stage forest predominated. Within the mature forest reserve, begging success of young juveniles covaried positively with preferred habitat. Rather than overt caretaker–offspring conflict, an information–feedback loop between juveniles and adults appears to drive provisioning changes as juveniles mature. Direct measures of resource abundance are needed to help clarify the mechanisms by which forest successional stage influences provisioning.

Effects of Individual and Group Characteristics on Feeding Behaviors in Wild Leontopithecus rosalia

Studies have linked variation in feeding and foraging success to variation in survival and reproductive success, which makes exploring influences on feeding invaluable. In the current study, we quantified energy contents of foods consumed by wild golden lion tamarins (Leontopithecus rosalia, GLT) and feeding behaviors of 34 GLT from March 1998 to March 1999. Our objective was to test predictions regarding effects of characteristics of the 1) individual, 2) group, 3) environment, and 4) other behaviors on 3 feeding behaviors: feeding on plant matter, searching for prey, and feeding on prey. We hypothesized that environmental characteristics, e.g., resource availability, in addition to group characteristics e.g., group size, would influence feeding on plant matter, because several individuals in a group often consume fruit in the same fruit tree. We hypothesized that environmental characteristics and individual characteristics, e.g., age, would influence searching for and consuming prey because the individual often searches for and consumes prey while it is alone at a substrate. We used SAS mixed models to determine the relative influence of these characteristics on the feeding behaviors. We found that group characteristics more significantly influenced feeding on plant matter, while individual characteristics more significantly influenced searching for prey. The results emphasize the distinctly different influences of individual and group characteristics on feeding. That influences other than competition may affect feeding on plant matter warrants further exploration.

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.

Clinical, biochemical, and electrocardiographic aspects of Trypanosoma cruzi infection in free‐ranging golden lion tamarins (Leontopithecus rosalia)

Wild golden lion tamarins from the Biological Reserve of Poço das Antas, Rio de Janeiro, Brazil, have high prevalence of Trypanosoma cruzi infection leading us to clinically assess the disease in this endangered species. 34 tamarins were sampled for the presence of T. cruzi infection (through serology) and clinical evaluation (electrocardiography, blood counts and biochemical analysis). 32% of the sampled tamarins were T. cruzi positive, 45% of these displayed cardiac abnormalities. Main cardiac abnormality in infected tamarins was T wave low voltage; R wave low voltage and V3S wave high voltage were also found. The tamarins displaying T wave low voltage had high proportion of seric cardiac creatine kinase. Seric mean total protein was significantly higher in infected tamarins. Sampled tamarins displayed typical signs of T. cruzi infection, similar to experimentally infected primates and human natural infection. Potential risk of T. cruzi infection to this endangered species is discussed.

Provisioning in wild golden lion tamarins (Leontopithecus rosalia): benefits to omnivorous young

Provisioning may act to cushion weaned young from dietary insufficiency and errors during the period in which they are mastering complex foraging techniques or learning to identify appropriate dietary items. That is, young mammals who receive food from others may gain nutritional and/or informational benefits. I conducted a longitudinal study of 13 wild golden lion tamarins 11–56 weeks of age in six groups to evaluate hypotheses regarding the functions of provisioning. All members belonging to this primate taxonomic family (the Callitrichidae) are cooperative breeders and are known to provision their young more frequently than do other primate species, except humans. My results, together with experimental findings, suggest that juveniles receive both nutritional and informational benefits from being provisioned. My juvenile study subjects received animal prey (invertebrates and small vertebrates) from others more frequently than plant resources (fruits and hardened exudates). Apparently difficult-to-handle fruits were more likely to be transferred than readily processed fruits. These results support the nutritional benefits hypothesis because the young received items, particularly lipid- and protein-rich prey, that they might not otherwise have acquired. That juveniles fed independently on, and were provisioned with, the same fruits on the same day is counterevidence to the nutritional benefits hypothesis, however. The informational benefits hypothesis was supported because juveniles received a large variety of foods (including more than 20% of fruit species eaten) and received uncommon fruits that were easily acquired. Adults emitted food-offering calls to encourage the transfer of prey to juveniles, particularly when the prey was whole and alive.

Distinct patterns of Trypanosoma cruzi infection in Leontopithecus rosalia in distinct Atlantic Coastal Rainforest fragments in Rio de Janeiro – Brazil

Previous studies on infection of Trypanosoma cruzi in the Poço das Antas Biological Reserve population of wild free-ranging Leontopithecus rosalia have shown the presence of genotype T. cruzi II, associated in Brazil with human disease. Herein, this study has been extended, the infection being evaluated in L. rosalia of 3 different tamarin populations, inhabiting distinct forest areas located in the same Atlantic Coastal Rainforest. Edentata, Marsupialia, Rodentia and Chiroptera were examined exclusively in the Poço das Antas Biological Reserve. Excluding Chiroptera, T. cruzi infection was found in all orders. Biochemical and molecular characterization demonstrated that golden lion tamarins maintained stable infections by T. cruzi II. The isolates from the other mammals corresponded to T. cruzi I, suggesting independent transmission cycles occurring among the sylvatic mammals inside Poço das Antas Biological Reserve. Significant differences in the infection patterns presented by the 3 populations of wild and captive-born golden lion tamarins were noticed. In Poço das Antas a considerably higher number of positive haemocultures from tamarins with positive serological titres was observed in comparison to those obtained from other areas. The implications for conservation and public health of an active sylvatic cycle in the Atlantic Coastal Rainforest of Rio de Janeiro are discussed.

The role of scent marking in the social communication of wild golden lion tamarins, Leontopithecus rosalia

The role of scent marking in the social communication of mammals is widely variable. One reason for this variation is that the function of scent marking may vary with different ecological and social conditions. The purpose of this study was to test four nonexclusive hypotheses explaining the role of scent-marking frequency in different ecological and social contexts for wild golden lion tamarins. Relative to ecological contexts, we compared scent-marking frequency during seasons of abundant and scarce food resources. Relative to social contexts, we compared scent-marking frequency when groups were isolated and when groups were in the presence of neighbouring groups. We found that the tamarins used scent marking to mark the location of food resources. Additionally, males used scent marking to communicate intrasexual dominance within their groups, while females did not. Our results also indicate that alpha females increased their scent-marking frequency to communicate to members of other groups, while the presence of members of other groups did not elicit a similar response by alpha males. We did not find evidence for a territorial function of scent marking in golden lion tamarins. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour

Trypanosoma cruzi infection in Leontopithecus rosalia at the Reserva Biológica de Poco das Antas, Rio de Janeiro, Brazil.

Wild golden lion tamarins (Leontopithecus rosalia) - endangered primates that are native to the Brazilian Atlantic coastal forest - were surveyed for the presence of Trypanosoma cruzi with the use of Giemsa-stained blood smears, hemocultures and an indirect immunofluorescence assay (IFAT). Positive IFAT with titers ranging from 1:20 to 1:1280 were observed in 52% of the 118 wild tamarins examined and the parasite was isolated from 38 tamarins. No patent parasitemia was observed among the tamarins from which T. cruzi was isolated. Serum conversion and positive hemoculture was observed for three animals that had yielded negative results some months earlier, which indicates that T. cruzi is actively transmitted among tamarins. In contrast to observations with other sylvatic isolates, those from the tamarins were significantly more virulent and most of them produced mortality in experimentally infected Swiss mice. Some variation in the kDNA restriction profiles among the isolates was observed. Electrophoresis with GPI, G6PDH, IDH, MDH and ME enzymes showed a Z2 profile.

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.

Costs and benefits of territorial defense in wild golden lion tamarins, Leontopithecus rosalia

The costs and benefits of territorial defense were examined in a group of five wild golden lion tamarins, Leontopithecus rosalia, at Poco d'Antas Biological reserve, Rio de Janeiro, Brazil. I examined the effects of both interference and exploitative competition between groups of tamarins by comparing their use of space, time budgets and foraging success in different contexts of intergroup interactions and in quadrats shared and not shared by other groups. Tamarins spent more time moving and vocalizing, and less time feeding, foraging, and resting during intergroup encounters than in non-encounter contexts. Irrespective of intergroup distance, the group spent more time in overlapping areas of the range periphery than expected on the basis of quadrat availability. In those areas, however, foraging success per unit of foraging effort was lower than in exclusive areas of the range center. This suggests that access to high payoff central areas depended on costly defense (by both interference and exploitation) of the range periphery. Time and energy invested by the resident group in territorial defense (1) increased the availability of food in the range center, and (2) minimized food loss to neighboring groups in the range periphery. These benefits are likely to justify the costs of defense for an animal which depends on easily-depletable food supplies, such as prey in microhabitats and small concentrations of fruits and nectar.