Golden lion tamarin

SOCIAL ORGANIZATION AND BEHAVIOR

Because golden lion tamarins were studied extensively in captivity before data from long-term studies had accumulated, there are some discrepancies about wild tamarin behavior and considerable conflict about their true social structure and mating behaviors. Additionally, the only habituated population of wild golden lion tamarins that has been studied over extended periods is found at Poço das Antas, and therefore represents most of the conclusions made about wild tamarin social structure (Baker et al. 2002). Further research in the field may lead to new understanding about wild golden lion tamarin behavior.

In the wild, golden lion tamarins have been observed living in groups of two to 11 individuals (Dietz & Baker 1993). Historically, most groups had, on average, about five members, but average group size has decreased in recent years because of the effects of predators (Bales pers. comm.). In these small groups, they exhibit cooperative rearing of offspring; all members of the group help a mother tamarin carry, care for, and provide solid food for her infants (Dietz & Baker 1993). The social structure of groups varies and includes either one adult male and one female (about 50% of the groups), two to three males and one female (about 40% of the groups), or one male and two females (about 10% of the groups) (Baker et al. 1993; Dietz & Baker 1993). In addition to these dominant, breeding adults, there are subadults, juveniles, and infants of both sexes which are usually the offspring of the breeding pair(s). If there are more than two adult males within the group, one maintains dominance over the other by physical fighting, lunging and displacing the subordinate animal, and displays such as “arch-walking” where the dominant male arches his back as he walks quadrupedally along a branch (Baker et al. 1993). Dominance relationships between adult males and females are determined by which animal has been on the group territory the longest period of time. For example, a newly immigrated male has not been on the territory as long as a female who inherited her mother’s breeding position and she will therefore be dominant over him, displacing him at feeding sites (Bales 2000). In captivity, golden lion tamarins are usually housed in family groups with just one breeding pair and their offspring of various ages. At around two years old, offspring may be removed from the social group and paired with an unrelated member of the opposite sex to begin their own family group (Cohn 1997).

Females within the wild group are generally related to each other, usually as mother-daughter or as sisters, while adult males may be non-natal. This configuration exists because of the dispersal patterns of young golden lion tamarins; both males and females disperse by the age of four, but if the breeding female within a group dies or disappears before a young female has dispersed, she will inherit her mother’s breeding position in the group and the adult breeding male in the group, presumably her father, will leave (Baker & Dietz 1996). Young male golden lion tamarins, however, usually do not inherit their father’s breeding position and disperse, forming roaming, single-sex groups looking for immigration opportunities. These roaming bands do not have specific territories and usually move between groups in home ranges that overlap multiple groups (Kleiman et al. 1988; Baker & Dietz 1996). Young males have been recorded inheriting their natal territories, but they are more likely to disperse and find a new territory (Bales per. comm.). Males have significantly higher success of joining a group after dispersing from their natal groups compared to females. More than 70% of females that leave their natal groups die or disappear before joining another group and becoming the breeding female (Dietz & Baker 1993).

Patterns of immigration are highly sex-biased, with males representing 85% of the immigration events (Baker & Dietz 1996). Adult males immigrate into a neighboring group from a roaming band if the dominant breeding male of a group dies or disappears, leaving a “vacancy,” or immigrant males may hostilely take over the breeding position and eject a resident breeding male from his group (Baker & Dietz 1996). When there is a hostile takeover, often two immigrant males (usually brothers) will move into a group and only one of them will become the breeding male and behaviorally suppress the other through dominance interactions (Baker et al. 2002). Another reason a breeding “vacancy” may become available is if the breeding female in a group dies or disappears and her daughter subsequently becomes the dominant breeder. Rather than the dominant male mating with his probable daughter, he leaves the group and an immigrant, unrelated male takes his place (Baker et al. 2002).

In general, the dominant male and female within the group behaviorally restrict mating opportunities between other adult group members (Baker et al. 2002). In groups with two breeding females, they are usually mother and daughter and both will mate with the dominant male (Dietz & Baker 1993). If intruders from a roaming band attempt to move into the territory, the dominant male and female are quite aggressive towards them. Breeding males in an established wild group generally chase male intruders away, while both females and males will chase female intruders away (Baker & Dietz 1996; Baker et al. 2002). This severe aggression toward female intruders may be what limits their success in dispersing from their natal groups (Cohn 1997). In captivity, males rarely show aggression toward intruders of either sex while dominant females are highly intolerant of female intruders and agonistically display at, chase, charge, grab, and attack them (French & Inglett 1989).

Golden lion tamarins exhibit territorial behavior not only as a form of mate defense, restricting access to the breeding female or male within the group, but also as home range defense. They are highly territorial and act to distinguish home range boundaries and keep other groups from exploiting food resources within their territory (Peres 2000). Most encounters between neighboring golden lion tamarin groups occurs during the first few hours of the morning as the monkeys emerge from their sleeping sites and begin to vocalize and wait for responses from other groups (Peres 1991; 2000). Long-range calling to one another increases in frequency as groups move closer to each other, but if groups do encounter each other face-to-face, usually the type of vocalizations change and increase in frequency and intensity and eventually escalate to fighting between the adult males of each group (Peres 1991). Aggressive interactions between males include posturing, chasing, displays, and fights. These encounters occur over an invisible territory boundary and usually end as the groups lose interest (Peres 1991).

REPRODUCTION

Golden lion tamarins have a monogamous mating system both in captivity and in the wild. Even when there are multiple males and one female, only one male and one female reproduce. On some occasions, golden lion tamarins are polygynous, where one male mates with two females, usually a mother-daughter pair (Baker et al. 1993; Dietz & Baker 1993; French et al. 2002). In this case, both females can produce offspring, though it is quite rare when it occurs (Dietz & Baker 1993).

Wild lion tamarins are seasonal breeders and they time reproduction and parturition with seasonal variation in rainfall (French et al. 2002). The peak period of reproductive activity occurs from late March through mid-June (the end of the rainy season) and the majority of births occur between September and February (the rainy season) (Kleiman et al. 1988; French et al. 2002). This pattern corresponds to the period of highest fruit availability and foraging opportunities for insects and other vertebrate prey (Dietz et al. 1994a). Because nursing is extremely energetically expensive, female golden lion tamarins have adapted a system of birth and nursing during the time of year with the lowest amount of nutritional stress (French et al. 2002). In captivity, golden lion tamarins do not exhibit seasonal birth patterns like their wild counterparts, but births are not distributed evenly throughout the year, either. The breeding season lasts from about March to September and no litters are produced during the winter months (French et al. 2002).

Female golden lion tamarins reach sexual maturity between 15 and 20 months of age, though because of their social structure, usually do not reproduce until they are 30 months old (Kleiman et al. 1988; Dietz et al. 1994a). In the wild, female golden lion tamarins first reproduce between two and six years of age, but the average age of first reproduction is 3.6 (Bales et al. 2001). The ovarian cycle lasts about 19 days and there is neither menstruation nor any external signs of estrus. Golden lion tamarins are anovulatory during the non-breeding season and therefore will not conceive except during the breeding season (French et al. 2003). Like many callitrichids that are cooperative breeders, the dominant female physiologically suppresses ovulation in subordinate group members, and a female in the group will not reproduce unless she occupies the social status of breeding female (French et al. 2003). With only one breeding male per group, younger females may not have the opportunity to mate with him because their mother, the dominant breeding female, acts aggressively to prevent mating or, if the male is likely the father of the younger female, she may avoid mating with him as an adaptation to avoid incest (French et al. 2002). Compared to females, little is known about male reproductive development, but male puberty is thought to occur around 28 months of age (Kleiman et al. 1988; French et al. 2002).

Copulations occur throughout the ovarian cycle, with the peak number of copulations occurring during the highest period of fertility (Kleiman 1977). Males solicit females by approaching and sniffing them more frequently, grooming more often, and displaying by tongue-flicking to entice the receptive female. The female also increases the number of approaches towards and sniffing of the male in the days just before peak receptivity (Kleiman 1977; Kleiman et al. 1988). Gestation lasts about four months (125 days), and within a month after parturition females begin to cycle normally, though they will not conceive until the following breeding season (French et al. 2002). If a female gives birth early enough in the season and the infants die, she is able to conceive again that year, but generally, wild golden lion tamarins only give birth to one litter per year unless food resources are extremely abundant, and even then second litters are born only about 20% of the time. The average interbirth interval is 311 days (Dietz et al. 1994a). In captivity, about one-third of females produce two litters per year and there has been a report of three litters being born to one female in a year (Dietz et al. 1994a).

PARENTAL CARE

As cooperative breeders, callitrichid mothers are not the only ones that care for infants and juveniles in the group. All members of the group take turns carrying and providing solid food for the infants (Kleiman et al. 1988; Bales et al. 2002; Tardif et al. 2002). Though they forgo breeding opportunities by remaining in the group and not breeding, younger group members benefit from cooperative rearing of infants because they gain valuable parental experience and invest in the survival of their younger brothers and sisters, thereby increasing their inclusive fitness (Kinzey 1997; Bales et al. 2000; Tardif et al. 2002). One of the reasons this system of cooperative breeding may have evolved is the tendency for callitrichids to give birth to twins. A golden lion tamarin mother would not be able to successfully carry and feed two or three infants on her own without sacrificing the infants’ well-being. By enlisting the help of other group members, she is able to raise the infants with assistance as all members of her family take turns carrying and caring for her offspring (Tardif et al. 2002). Other infant care behaviors exhibited by group members include foraging tutoring, huddling with young at night and during periods of rest to reduce heat loss, protection against predators through increased vigilance, grooming, and playing to increase socialization (Rapaport & Ruiz Miranda 2002; Tardif et al. 2002; de Oliveira et al. 2003). The role of helpers and the experience level of the mother are crucial in the survival of infants (French et al 1996; Santos et al. 1997). Infants are most vulnerable during the first week of life and survival is particularly related to the parental and helping experience of the mother. A female that is nulliparous has lower offspring survivorship than one that is multiparous and a female with previous helping experience has higher offspring survivorship than one that has never carried or cared for an infant (French et al. 1996).

Data on infant development from captive studies provides information about parent/offspring interactions in golden lion tamarins. The dependent infant phase in golden lion tamarins lasts from one to four weeks and is characterized by relying on the mother for transport and nursing. Infants in this stage are dorsally carried almost constantly by the mother while other group members intensely interested in the infants touch, sniff, and mouth them (Hoage 1982). Infants lean or reach off their mother during this time and are interested in other group members and their environments. They are able to vocalize and do so if they are dislodged from their mothers or are rejected by other potential carriers. After week three, mothers rapidly decrease the amount of time spent carrying the infants and the father and other group members over the age of one become the primary transporters. As they grow, infants begin to spend more time off of carriers, moving independently. By week four, about 10% of their time is spent off carriers (Hoage 1982).

Weeks five through 16 are the advanced infant stage and infants spend increasingly less time being carried and more time moving independently and exploring their environment. By week 11 they spend about 80% of their time off of carriers (Tardif et al. 2002). Mothers and other group members reject the infants’ attempts at being carried starting at week five, though fathers are generally more tolerant than other group members and will carry infants into week 12 (Tardif et al. 2002). It is during the advanced infant phase that weaning begins (around week five), and by week 12, they cease nursing. Infants begin to try solid food before they are weaned, but during the weaning period, intake of solid food increases because they beg group members or are given food by their caretakers (Hoage 1982). Food transfer to young golden lion tamarins lasts throughout their development, until about 21 months of age, though the amount and frequency of food shared by older group members significantly decreases after nine months of age (Tardif et al. 2002). Infants and juveniles receive fruit, insects, and animal prey from older members of the group and are sometimes taught where and how to catch prey by older group members (Rapaport & Ruiz-Miranda 2002).

The young juvenile phase lasts from weeks 17 through 28 and it is during this time that young golden lion tamarins play with and groom other group members. By the time they reach the advanced juvenile phase, weeks 29 through 40, the mother has probably given birth to a new set of twins and the juveniles begin to exhibit great interest in their younger siblings (Hoage 1982). The young subadult phase lasts from about 41 to 52 weeks and tamarins exhibit almost the full suite of adult behaviors, including first sexual behaviors. This stage lasts until sexual maturity at which point the golden lion tamarins will be true adults (Hoage 1982).

COMMUNICATION

Golden lion tamarins use visual, vocal, and chemical systems to communicate to other members of their group and conspecifics. The repertoire of visual signals is limited compared to the other communication forms, but includes both postural and facial expressions that act as signals to nearby individuals (Kleiman et al. 1988; Kinzey 1997). Visual signals are not very efficient means of communication for small-bodied animals that live in dense forests, nonetheless they exhibit tongue flicking, arch-walking, tail thrashing, rump displays and piloerection in sexual and social contexts (Kinzey 1997; Ruiz-Miranda & Kleiman 2002). Most visual signals are used during territorial encounters, social interactions, and reproductive events (Ruiz-Miranda & Kleiman 2002).

Often accompanying visual signals but more importantly serving as long-distance communication are vocal signals. There are six discrete categories of vocalizations in golden lion tamarin communication: tonal, clucks, trills, atonal, multi-syllable, and combination (Ruiz-Miranda & Kleiman 2002). Tonal vocalizations include the “whine” and “peep” calls and serve as alarm and affiliation calls. “Whines” are given in reaction to the presence of predators while “peeps” are sounded by solitary young after being reunited with the group or by any group member upon finding food (Kleiman et al. 1988; Boinski et al. 1994; Ruiz-Miranda & Kleiman 2002). “Clucks” signal reaction to the presence of a novel item or are giving during foraging bouts. They also can signal aggression when golden lion tamarins encounter neighbors or intruders and are given while chasing or mobbing predators (Kleiman et al. 1988; Boinski et al. 1994). “Trills” have multiple purposes but mainly serve to indicate the location of the caller to other individuals over long distances. Atonal calls such as “rasps” or “screeches” are heard mostly during playing or as playing escalates to fighting (Kleiman et al. 1988; Boinski et al. 1994). Multisyllable calls include the most important vocalizations for group cohesion, the “short” and “long calls.” These are typically heard as golden lion tamarins leave their sleeping sites in the morning to localize their neighbors and are heard throughout the day as individuals keep in vocal contact with other group members (Peres 1991; Ruiz-Miranda & Kleiman 2002). Combination calls also serve multiple purposes and include “trill-rasps,” “trill-whines,” and “cluck-whines.” These are used by juveniles begging for attention, protection, or food or by group members as they defend their territory against intruders or predators (Ruiz-Miranda & Kleiman 2002).

The most specialized form of communication exhibited by golden lion tamarins is the chemical communication system relayed by scent marking surfaces throughout their territories. Scent glands on their chest and around their genitals are activated as they are rubbed along a surface, leaving behind chemical signals to other group members and conspecifics (Ruiz-Miranda & Kleiman 2002; Miller et al. 2003). Some of the purposes of scent marking include conveying reproductive status and individual identification, social regulation, location of food resources, and parent-offspring interactions. Reproductive males and females do most of the scent marking among golden lion tamarins and the behavior is rarely seen among juveniles or nonreproductive individuals still in their natal group (Hoage 1982; Ruiz-Miranda & Kleiman 2002). Dominant males within a group scent mark to signify social status and reinforce dominance to other group members; this behavior may be linked to behavioral suppression of reproduction seen among subordinate males. Both males and females mark specific sites on their way to food areas within their home ranges and on the edges of their territories probably to facilitate relocation of food resources among members of the group (Miller et al. 2003). Marking fruit trees and the paths to food resources is much higher during the wet season and could be due to seasonal rain abundance washing away scent marks more frequently than during the dry season (Miller et al. 2003).

Content last modified: December 1, 2010

Written by Kristina Cawthon Lang. Reviewed by Karen Bales and Lisa G. Rapaport.

INTERNATIONAL STATUS

For individual primate species conservation status, please search the IUCN Red List.
Also search the current scientific literature for primate conservation status (overall as well as for individual species), and visit CITES (Convention on International Trade in Endangered Species of Wild Fauna and Flora).

Conservation information last updated in 2010 follows, for comparison:

While great strides have been made to pull the golden lion tamarin away from the brink of extinction, they are still very much at risk. The extremely limited range in which the golden lion tamarins are found is within the most devastated and highly threatened ecosystem on Earth. Only about 7% of the former Atlantic Forest remains, and where it does exist, it is highly fragmented and subject to fuelwood harvesting, illegal logging, plant and animal poaching, mining, urbanization and infrastructure development, and the introduction of alien species (Galindo-Leal & de Gusmão Câmara 2003).

CONSERVATION THREATS & POTENTIAL SOLUTIONS
Threat: Human-Induced Habitat Loss and Degradation

Habitat loss and degradation is the primary historical and current threat to golden lion tamarins. Lumber extraction, agriculture, cattle ranching, and charcoal production have annihilated the Atlantic Forest and forced the remaining forest species into tiny pockets of forest, highly fragmented and isolated from one another (Kierulff et al. 2003). The pattern of unsustainable forest destruction has a long history starting with European colonization in 1500. Widespread exploitation of brazilwood as a ship-building material coupled with deliberate clearing of forest for settlement and agriculture wiped out extensive areas of forest (de Gusmão Câmara 2003). Cattle-raising was another colonial process that resulted in habitat destruction as herds were driven through forests and pastureland was cleared. Throughout the 18th and 19th centuries, massive sugarcane plantations, mining activities, and coffee cultivation further eliminated the forests of the region as demand for such products in the global economy fueled the destruction (de Gusmão Câmara 2003). But even with the massive amount of damage inflicted on the forests during the previous centuries, nothing compares to the devastation seen in the 20th century.

Growing human populations and industrialization characterized the first half of the century. Railroads built across the country opened up new areas for cultivation, disorganized exploitation of timber with little regard to regeneration, and the expansion of urban areas. Infrastructure was necessary to support a rapidly growing urban population and the timber industry eliminated nearly all of the Brazilian Atlantic Forest (de Gusmão Câmara 2003). An international oil crisis in the 1970s put further pressure on the remaining coastal forests as alcohol distilled from sugarcane was used as an alternate fuel source. Plantations of sugarcane, nonnative pine, and eucalyptus took over most of the landscape during this time period as the reliance on alcohol for fuel and the paper and pulp industry exploded (de Gusmão Câmara 2003). Forest destruction continues in the region as the ever-growing human population looks to more areas for settlement and more supplies from the shrinking reserve. Golden lion tamarins are found in the most densely populated area of Brazil and the human population continues to expand. All of the activities throughout the last 500 years have adversely affected numerous forest-dependent species, including the golden lion tamarin as their habitats have been destroyed and they are forced into increasingly smaller patches of land in their ranges.

Potential solutions

Despite centuries of uncontrolled exploitation and little tangible protection even with the establishment of protected areas starting in the 1980s, the Atlantic Forest continues to be destroyed. Conviction to protect the remaining remnants of the region is growing among Brazilians and needs to continue if protection is to succeed in the face of strong economic interests, including agriculture and timber industries (de Gusmão Câmara 2003). The Brazilian constitution has newly added provisions specifically protecting the Atlantic Forest through enactment of laws. Legislation strictly protecting the biome through prohibition of cutting down and exploiting any vegetation in any ecosystem in the region was proposed in 1990 but is still being discussed in Congress and was no doubt slowed by politically influential developers (de Gusmão Câmara 2003). Given the constitutional requirement to protect the Atlantic Forest, the Brazilian Congress must pass enabling legislation to stop rampant forest destruction as soon as possible. There exist governmental agencies and organizations that are charged with the protection and conservation of forests and other ecosystems, including the Ministry of the Environment and the National Council on the Environment, that need the legal support to continue to effectively arrest habitat destruction (de Gusmão Câmara 2003). Economic interests in developing the Atlantic Forest region continually defeat environmental interests and this pattern must be stopped by international pressure and lobbying as well as decreased incentives for Brazilian agribusinesses to destroy forests for plantations or pastures.

Apart from the legislative changes that must occur to protect the remaining forests, focus on reestablishing corridors between fragmented pockets of forest as well as broad-scale reforestation efforts must be undertaken (Kleiman & Rylands 2002). Establishing habitat corridors between isolated subpopulations is an important focus in order to increase genetic variability in the total population and to allow for natural dispersal and group formation. Reforestation can be accomplished either through natural revegetation of a once-cleared area or through aggressive restoration planting of saplings. Propagating and raising native saplings can be a long and expensive process. Furthermore, once saplings are mature enough to survive outside of a greenhouse, planting needs to be done in such a pattern that mimics the structure of a natural forest rather than in rows like a plantation (Lugo 1988).

Finally, efforts to increase the golden lion tamarin population through translocation and captive breeding and reintroduction should continue in order to deter the effects of human-induced habitat destruction and degradation. Reintroduction is broadly defined as the return of animals that have spent any portion of their life in captivity back to the wild and is used in cases of extreme endangerment to supplement populations that are critically small or to reestablish wild groups of animals that are extinct in their former ranges (Beck et al. 1991; Kierulff et al. 2002b). In 1984, the first captive-born golden lion tamarins were returned to the wild (Beck et al. 1991). The captive population of golden lion tamarins has been maintained since the late 1970s and careful selection of breeding partners has made the captive population self-sustaining (Ballou et al. 2002). The reintroduction of these animals involved extensive training in captivity to teach them how to locomote through the forest, find and collect insects from small crevices, find and collect water from bromeliads and other sources, and introducing them to predators to gauge appropriateness of response (Beck et al. 1991). After having been trained in captivity at the National Zoological Park, tamarins were transported to Brazil, where they spent six months in quarantine to ensure they were not carrying any diseases or parasites that might infect wild tamarins with which they might come into contact (Beck et al. 1991). After the quarantine period, the captive-born golden lion tamarins were released from their cages into Poço das Antas Biological Reserve and other private lands surrounding the reserve and were supplemented with food items and sleeping sites as well as veterinary support to ensure their survival. Over time as reintroduced groups learned about natural foods and the resources within their territories, they become less reliant on food provisioning and eventually were no longer provisioned (Beck et al. 1991; Kierulff et al. 2002b). To date, about 40% of the total wild population of golden lion tamarins represents captive breeding and reintroduction efforts. Starting with 18 captive-born individuals, the population has grown as those founders produced wild-born offspring (Kierulff et al. 2002b).

A program of translocation of golden lion tamarins has been another approach to protect threatened subpopulations by moving them from a degraded area to a protected reserve or private land. Translocation involves moving wild animals from one area of their natural range to another area of suitable habitat (Kierulff et al. 2002b). This is often done an emergency basis as groups come under threat from imminent habitat destruction or other danger. Being able to move wild populations into protected areas may prevent those groups from being lost completely (Kierulff et al. 2002b). Translocated individuals have a high rate of survival and most causes of death are related to injuries obtained while fighting with another group or predation (Kierulff et al. 2002b).

Threat: Invasive Alien Species

Rapidly expanding international trade and travel coupled with ongoing changes in land use and climate in Brazil has had far reaching effects on the diversity of native flora and fauna as nonnative species are introduced and are either purposely cultivated or thrive and outcompete other species. Problematic new species include pine species, sand olive, patient lucy, guava tree, white ginger, and eucalyptus (Reaser et al. 2003). When these are planted they usurp native species and often spread so successfully that they create vast areas of monocultures. Golden lion tamarins have not evolved with these species and cannot always use the fruits they bear and may be restricted from moving within vast tracts of these plants (Coimbra-Filho & Mittermeier 1977).

Potential solutions

Once nonnative invasive species have taken root, it is often very difficult to remove them or control their spread to other areas (Reaser et al. 2003). Well-coordinated international policies are necessary to limit the transport and spread of some of these species and need to include border patrol agencies, intergovernmental organizations, agriculture and forestry industries, and nongovernmental organizations. Furthermore, for those species that are purposely imported and planted for economic purposes, it is necessary to remove the fiscal incentives to plant these species or encourage systems of multi-cropping and shade growing to provide alternate income earning opportunities (Coimbra-Filho & Mittermeier 1977).

Threat: Harvesting (hunting/gathering)

Golden lion tamarins have been a popular pet and kept in captivity since the sixteenth century (Ballou et al. 2002). Their export continued for the pet trade, zoo exhibits, and biomedical research throughout the twentieth century. From 1960 to 1965, it was estimated that they were exported at a rate of 200 to 300 animals per month, a serious depletion of the already compromised population (Coimbra-Filho & Mittermeier 1977). Though it has been illegal to transport or sell golden lion tamarins in Brazil since 1968 and the international trade has been restricted since 1975, invariably some monkeys are still trapped and sold into the pet trade because of continuous demand (Ballou et al. 2002). Not only have they been trapped and sold as pets, but golden lion tamarins have been subject to hunting pressure, further decreasing their numbers in the wild (Kierulff et al. 2003).
Potential solutions

Growing in popularity as a flagship species, one that captures the attention of many people and signifies a conservation effort in an area, golden lion tamarins have successfully been used in conservation education programs in Brazil and other countries (Padua et al. 2002). One of the benefits of using an easily recognized and likeable species is the ability to raise awareness about conservation efforts and educate people about individual species and the ecosystems in which they live (Dietz et al. 1994b). Through education and outreach efforts in areas surrounding Poço das Antas, educators have been successful in teaching local communities about the unique primate population in their region. This has been substantiated by the return of over 20 illegal pet golden lion tamarins and the decrease of hunting of these monkeys (Padua et al. 2002). Returned and confiscated pets are rehabilitated and often returned to the wild (Kierulff et al. 2003). Conservation education efforts should continue to involve community members in monitoring the animals, teaching them about tamarin ecology and behavior, and patrolling reserve borders.

Threat: Accidental Mortality

The only data on accidental mortality of golden lion tamarins come from studies on captive-born, reintroduced animals. Losses due to eating toxic fruit and head injuries due to falls have been recorded and are attributed to the naivete of the animals about appropriate food sources and the inability to move between trees on the thin ends of branches (Beck et al. 1991). Another source of accidental mortality in reintroduced golden lion tamarins is death caused by bee stings (Bales pers. comm.).

Threat: Pollution

While there is scant data on the adverse effects of pollution on golden lion tamarins, throughout their region, water quality and habitat are degraded due to acid rain caused by nearby centers of industry with no pollution or emissions control in effect (Aguiar et al. 2003). One case of a golden lion tamarin poisoned by insecticides sprayed near a biological reserve and resulting in death has been reported. Presumably the animal ingested contaminated insects (Pissinatti et al. 2002). It is plausible that a situation like this could occur again, especially in forest fragments near plantations, though there have been no other reports.

Potential solutions

Legislation by the Brazilian government and enforcement by officials could have some effect in controlling the pollutants released by industrial factories and sites that are the leading causes of acid rain. Plantation owners should be restricted from spraying insecticides within a certain distance of forests to decrease the likelihood of contaminating insects, a food source for golden lion tamarins. Education programs about the effects of insecticide on native species, including plants, animals and insects, could also help change patterns of use among some agriculturalists.

Threats: Changes in Native Species Dynamics

Predators of golden lion tamarins include hawks, owls, boa constrictors, and small cats. Normally a group only loses one or two individuals per predation event (Franklin & Dietz 2001). At Poço das Antas, predators have contributed significantly to the loss of golden lion tamarins. Entire groups, up to 10 individuals, are being sought after in their sleeping sites at night and eaten with the only evidence left behind being a few remains and the radio collar used by researchers to track the monkeys. In one year alone, five groups were taken by predators, reducing the population from 350 individuals to 220 in the reserve (Franklin & Dietz 2001). This represents a serious threat to the largest wild population of golden lion tamarins as the population is decreasing, group size is decreasing, infant survival to weaning is decreasing, and tamarin density within the reserve is decreasing (Franklin & Dietz 2001; Rylands et al. 2002a). Unfortunately, it is not clear what kind of animal is responsible for the carnage or if these predation events represent a change in predator-prey dynamics because of the loss of habitat (Franklin & Dietz 2001). It may be that because there is so little habitat remaining and predators are restricted to unnaturally small ranges that they have changed their foraging patterns thus adversely affecting the golden lion tamarins.

Parasites and pathogens represent another threat to wild golden lion tamarins and may change the native species dynamics of a population. Parasitic infections caused by eating rodents or coming in contact with cockroaches and some species of beetles may cause sickness or death in some cases (Pissinatti et al. 2002). Ticks, chiggers, and mites are the most commonly found ectoparasites among golden lion tamarins but probably have little to no effect on the overall health of individual monkeys.

Potential solutions

One effort to identify the predators responsible for killing entire groups included stationing heat/motion cameras at sleeping trees in an attempt to capture the predator on camera, but no definitive evidence has been found (Franklin & Dietz 2001). If a predator is identified, biologists may be able to modify the sleeping sites, which are used repeatedly by groups of tamarins, in order to “predator-proof” them according to the type of predator involved. Expanding forest fragments may be another method of decreasing predation pressure on golden lion tamarins so predators have larger areas in which to hunt and may not rely as heavily on the highly endangered animals.

Threat: Intrinsic Factors

Genetic studies on the small population of golden lion tamarins have revealed high levels of inbreeding and low levels of genetic diversity despite scientists’ best efforts to manage proper breeding in captivity and through translocation. These patterns occur because golden lion tamarins mate with relatives they do not recognize as kin or because they do not reject them as mates (Dietz et al. 2000). This may be compounded by the fact that in small, isolated fragments, individuals have limited dispersal opportunities and are unable to enter groups that do not have their relatives. Both inbreeding depression and loss of genetic diversity have potentially serious consequences in small, fragmented populations because they may be responsible for decreased survivability or poor recruitment (Dietz et al. 2000). Inbred infants at Poço das Antas have lower survival rates than those of non-inbred infants and survivability decreases with higher rates of inbreeding. About 10% of all infants at the reserve are inbred, but this may be an underestimate because researchers assumed that all adults at the beginning of the study were unrelated (Dietz et al. 2000). Currently, this rate of inbreeding is not a threat to the viability of the population at the reserve but may not be a good indicator of other levels of inbreeding of wild golden lion tamarins groups. Because Poço das Antas is the largest reserve with the highest number of golden lion tamarins in Brazil and inbreeding levels are at about 10%, it is reasonable to assume that other forest fragments containing tamarins may be so small that inbreeding occurs at even higher rates (Dietz et al. 2000).
Potential solutions

Genetic management of all golden lion tamarin populations may be necessary to prevent inbreeding depression from negatively impacting the survival of the species (Dietz et al. 2000). While the levels at Poço das Antas are not a hazard to the survivability of the population, models of areas with less than 50 individuals project that inbreeding depression may decrease the probability of survival of an entire population to only 60% (Dietz et al. 2000). Collecting genetic material, creating pedigrees, and managing the population based on level of relatedness in forest fragments is one way to assess the true threat of inbreeding depression and avoid its negative effects. Translocation of individuals or groups between forest fragments may enhance genetic diversity as tamarins from geographically distant forests are unlikely to be related. This is expensive and risky, though, because researchers need to be careful to avoid serious aggressive encounters between groups that might jeopardize individual tamarins (Beck et al. 1991).

Threat: Human Disturbance

Poço das Antas is surrounded by pasture maintained by cattle-raising landowners and parts of the reserve are subject to destruction by fires. Fires started by landowners to clear pasture land spread to nearby forest areas and can be especially destructive if they reach peat bogs, areas of high acidity and gaseous emissions (Pessamílio 1994).
Potential solutions

One preventative measure is to plant a buffer of vegetation between forested areas and ranches which can act as a barrier to spreading fires. Another important component of keeping fires from spreading and destroying large areas of the reserve is to train park personnel as fire monitors and firefighters. The reserve is already equipped with fire detection infrastructure and equipment including lookout towers, fixed and portable radio-telephones, and fire-fighting equipment. The reserve’s meteorological station can be helpful in the event of a fire to determine wind direction and other variables affecting the spread of a wildland fire (Pessamílio 1994). Being prepared for a fire in the reserve is crucial, but so is educating surrounding land owners in proper burning techniques, including how to execute controlled burns and what time of year burns are least likely to get out of control. Given that the US Forest Service is already involved in training of reserve staff in firefighting techniques, perhaps they could lend their expertise to surrounding ranch owners about fire safety and management to decrease the risk of fire.

SPECIAL NOTES

Captive breeding and reintroduction of endangered species resulting in viable wild populations has been met with limited success (Beck et al. 1994). In general, as a conservation tool, it has been expensive and rarely met the goal of creating self-sustaining populations except for a few notable instances: the North American red wolf, the Arabian oryx, and the golden lion tamarin (Beck et al. 1991; Kierulff et al. 2002b). The success of the golden lion tamarin reintroduction program can be attributed to dedicated researchers doing follow-up studies of behavioral deficiencies and survivability of captive-born reintroduced tamarins. Armed with the behavioral and mortality data, managers were able to make adjustments in the pre-release training, including novel food foraging, structural changes to enclosures to more adequately mimic forest conditions, and introduction of a variety of predators to measure fear and alarm responses (Beck et al. 1991; Stoinski & Beck 2004). Post-release support was also modified based on the results of behavioral studies and included food supplementation, provision of nest boxes for sleeping sites, and veterinary care and intervention when necessary (Beck et al. 1991; Stoinski & Beck 2004). This type of approach is a good model for other species reintroductions, both primates and other animals, and perhaps can be useful in saving other critically endangered species from certain extinction.

Content last modified: December 1, 2010

Written by Kristina Cawthon Lang. Reviewed by Karen Bales and Lisa G. Rapaport.

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VIDEO & WEBCAMS

• Golden Lion Tamarins  (2:19, narrated; National Geographic Kids; Flash)

IMAGES

	Leontopithecus rosalia Photo: Lisa G. Rapaport
	Leontopithecus rosalia Photo: Lisa G. Rapaport
	Leontopithecus rosalia Photo: Lisa G. Rapaport
	Leontopithecus rosalia Photo: Lisa G. Rapaport
	Leontopithecus rosalia Photo: Lisa G. Rapaport
	Leontopithecus rosalia Photo: Lisa G. Rapaport
	Leontopithecus rosalia Photo: Lisa G. Rapaport
	Leontopithecus rosalia Photo: Luiz Claudio Marigo
	Leontopithecus rosalia Photo: Luiz Claudio Marigo
	Leontopithecus rosalia Photo: Primates in Art & Illustration Collection
	Leontopithecus rosalia Photo: R. Sim-Dumais
	Leontopithecus rosalia Photo: R. Sim-Dumais
	Leontopithecus rosalia Photo: R. W. Van Devender
	Leontopithecus rosalia Photo: Richard Day
	Leontopithecus rosalia Photo: Roy Fontaine