Golden lion tamarin

The golden lion tamarin (Leontopithecus rosalia; Portuguese: mico-leão-dourado [ˈmiku leˈɐ̃w do(w)ˈɾadu, - liˈɐ̃w -]), less commonly known as the golden lion marmoset, is a small New World monkey of the family Callitrichidae. Endemic to the Atlantic coastal forests of Brazil, the golden lion tamarin is an endangered species.^[5] The geographic range is entirely within the state of Rio de Janeiro. A 2022/2023 census estimated about 4,800 individuals living in the current primary area of occurrence in the non-coastal area of the São João and Macaé river basins,^[6] with unknown but smaller additional numbers in limited coastal forests^[7] and to the west of the primary area of occurrence.^[8][9] There is a captive population maintaining about 490 individuals among 150 zoos.^[3][10][11]

Golden lion tamarin[1][2]
Male at Copenhagen Zoo, Copenhagen, Denmark
Female at the Bronx Zoo, New York, United States
Conservation status
Endangered  (IUCN 3.1)[3]
CITES Appendix I (CITES)[4]
Scientific classification
Kingdom:	Animalia
Phylum:	Chordata
Class:	Mammalia
Order:	Primates
Suborder:	Haplorhini
Infraorder:	Simiiformes
Family:	Callitrichidae
Genus:	Leontopithecus
Species:	L. rosalia
Binomial name
Leontopithecus rosalia (Linnaeus, 1766)
Synonyms
Jacchus rosalia brasiliensis Fischer, 1829 Jacchus rosalia guyannensis Fischer, 1829 Leontocebus leoninus Pocock, 1914 Leontopithecus aurora Elliot, 1913 Leontopithecus marikina Lesson, 1840 Simia rosalia Linnaeus, 1766

Physical characteristics

Closeup on the golden lion tamarin's face

The golden lion tamarin gets its name from its bright reddish orange pelage and the extra long hairs around the face and ears which give it a distinctive mane.^[12] Its face is dark and hairless. The bright orange fur of this species does not contain carotenoids, which commonly produce bright orange colors in nature.^[13] The golden lion tamarin is the largest of the callitrichines. It is typically around 261 mm (10.3 in) and weighs around 620 g (1.37 lb). There is almost no size difference between males and females. As with all callitrichines, the golden lion tamarin has claw-like nails, instead of the flat nails found in other monkeys and apes, although callitrichines do have a flat nail on the big toe.^[14] Tegulae enable tamarins to cling to the sides of tree trunks. It may also move quadrupedally along the small branches, whether through walking, running, leaping or bounding.^[15] This gives it a locomotion more similar to squirrels than primates.

Habitat and distribution

The golden lion tamarin has a limited current area of occupancy, as most of the original habitat in the Brazilian state of Rio de Janeiro has been lost to deforestation.^[7] Today, the species is confined to fragments of forest within the state, including Poço das Antas Biological Reserve, União Biological Reserve, other protected areas, and privately owned lands. Most of the area of occupancy is characterized by vegetation types classified as dense broadleaf evergreen or seasonal deciduous and semi-deciduous forest,^[16] with some tamarins living in areas closest to the coast found in a sandy soil forest type called “arboreal restinga”.^[17] Golden lion tamarins are thought to occur primarily in low elevation forests, up to 150^[18] or 300^[19] meters above sea level, but a 1990-1992 survey identified two groups above 500 meters,^[20] and reports from the recently identified western geographic area include records above 700 meters.^[9][21]

Golden lion tamarin population estimates in the 1960's and 1970's ranged from only 100 to 600,^[22][23] although these estimates were not based on range-wide censuses. The first such census, carried out 1990-1992, counted about 560 wild individuals^[24][20] and there were about 100 additional individuals from the reintroduction program living in the wild.^[20] Since then, following conservation efforts including reintroduction of zoo-born animals^[25][26] and translocation of wild individuals from small, at-risk forest fragments^[26] (both largely to areas then unoccupied by tamarins), reforestation with a particular focus on connecting separated areas of habitat,^[27][28] and community-based conservation and engagement programs,^[29][30] the population has grown significantly. Most recently, a 2022/2023 census estimated about 4,800 golden lion tamarins living in the current primary area of occurrence in the non-coastal area of the São João and Macaé river basins,^[6] with unknown but smaller additional numbers in limited coastal forests^[7] and to the west of the primary area of occurrence.^[8][9]

Behaviour and ecology

The golden lion tamarin is active for a maximum of 12 hours daily. It uses different sleeping dens each day.^[31][32] By frequently moving their sleeping nests around, groups minimize the scent left behind, reducing the likelihood of predators finding them.^[33] The first activities of the day are traveling and feeding on fruits. As the afternoon nears, tamarins focus more on insects. By late afternoon, they move to their night dens. Tamarin groups use hollow tree cavities, dense vines or epiphytes as sleeping sites. Sites that are between 11 and 15 m (36 and 49 ft) off the ground are preferred. The golden lion tamarin tends to be active earlier and retire later in the warmer, wetter times of the year as the days are longer.^[31] During drier times, it forages for insects longer as they become scarcer.^[31][32]

Golden lion tamarins are characterized by using manipulative foraging under tree barks and epiphytic bromeliads. Their sites of foraging are usually distributed around their home ranges, which are large territories (averaging 123 hectares (300 acres) in which multiple foraging sites are located, to find sufficient resources over long periods of time. These areas are sufficient in size that even if there is overlap between the home range of two different groups, the interactions are minimal due to the distribution of the foraging sites (they spend 50% of their time in approximately 11% of their home range).^[34]

Leontopithecus rosalia in Singapore Zoo

The golden lion tamarin has a diverse, omnivorous diet consisting of fruits, flowers, nectar, bird eggs, insects and small vertebrates. They rely on microhabitats for foraging and other daily activities and tamarins will use bromeliads, palm crowns, palm leaf sheaths, woody crevices, lianas, vine tangles, tree bark, rotten logs, and leaf litters.^[31][32] The golden lion tamarin uses its fingers to extract prey from crevices, under leaves, and in dense growth; a behavior known as micromanipulation.^[35] It is made possible by elongated hands and fingers. Insects make up to 10–15% of its diet. Much of the rest is made of small, sweet, pulpy fruits. During the rainy season, the golden lion tamarin mainly eats fruit; however, during drier times, it must eat more of other foods like nectar and gums.^[31] Small vertebrates are also consumed more at these times as insects become less abundant.

Social structure

Family groups may consist of up to eight members.

Golden lion tamarins are social and groups typically consist of 2-8 members. These groups usually consist of one breeding adult male and female but may also have 2–3 males and one female or the reverse.^[36] Other members include subadults, juveniles and infants of either sex. These individuals are typically the offspring of the adults. When there is more than one breeding adult in a group, one is usually dominant over the other and this is maintained through aggressive behavior. The dominance relationship between males and females depends on longevity in the group. A newly immigrated male is subordinate to the resident adult female who inherited her rank from her mother.^[37] Both males and females may leave their natal group at the age of four, however females may replace their mothers as the breeding adult, if they die, which will lead to the dispersal of the breeding male who is likely her father. This does not happen with males and their fathers. Dispersing males join groups with other males and remain in them until they find an opportunity to immigrate to a new group. The vast majority of recruits to groups are males.^[38] A male may find an opportunity to enter into a group when the resident male dies or disappears. Males may also aggressively displace resident males from their group; this is usually done by two immigrant males who are likely brothers. When this happens, only one of the new males will be able to breed and will suppress the reproduction of the other. A resident male may also leave a vacancy when his daughter becomes the breeding female and he must disperse to avoid inbreeding.^[39] Golden lion tamarins are highly territorial and groups will defend their home range boundaries and resources from other groups.^[40]

Tamarins emit "whine" and "peep" calls, which are associated with alarm and alliances respectively.^[41] "Clucks" are made during foraging trips or during aggressive encounters, whether directed at conspecifics or predators.^[42] "Trills" are used to communicate over long distances to give away an individual's position. "Rasps" or "screeches" are usually associated with playful behavior. Tamarins communicate through chemicals marked throughout their territories. Reproductive males and females scent mark the most and their non-reproductive counterparts rarely do so. Dominant males use scent marking to show their social status and may suppress the reproductive abilities of the other males.

Reproduction

The mother provides transportation at the early stages of the infant's life.

The mating system of the golden lion tamarin is largely monogamous. When there are two adult males in a group only one of them will mate with the female. There are cases of a male mating with two females, usually a mother and daughter.^[36] Reproduction is seasonal and depends on rainfall. Mating is at its highest at the end of the rainy season between late March to mid-June and births peak during the September–February rains.^[43] Females are sexually mature between the ages of 15–20 months but it is not until they are 30 months old that they can reproduce.^[42] Only dominant females can reproduce and will suppress the reproduction of the other females in the group.^[44] Males may reach puberty by 28 months.^[43] Tamarins have a four-month gestation period. Golden lion tamarin groups exhibit cooperative rearing of the infants. This is due to the fact that tamarins commonly give birth to twins and, to a lesser extent, triplets and quadruplets. A mother is not able to provide for her litter and needs the help of the other members of the group.^[45] The younger members of the groups may lose breeding opportunities but they gain parental experience in helping to rear their younger siblings.^[37] In their first 4 weeks, the infants are completely dependent on their mother for nursing and carrying. By week five, the infants spend less time on their mother's back and begin to explore their surroundings. Young reach their juvenile stage at 17 weeks and will socialize other group members. The sub-adult phase is reached at 14 months, when a tamarin first displays adult behaviors.

Ecosystem role

Vocalizing.

The golden lion tamarin has a mutualistic interaction with 96 species of plants found in the Atlantic Forest. This interaction is based on seed dispersal and food sources for the tamarins. The tamarins show repeat visits to those plants with abundant resources. They tend to move around their territories, and therefore, seeds are dispersed to areas far from the parent shadow, which is ideal for germination. Their seed distribution is important to forest regeneration, and genetic variability and survival of endangered plant species.^[46]

Predation

There are only a few published reports confirming identities of successful predators on golden lion tamarins, with these cases including a boa constrictor (Boa constrictor)^[31](p 158), a small cat identified as an ocelot (Felis pardalis)^[47], and a feral dog (Canis familiaris)^[47], the latter two incidents involving reintroduced zoo-born golden lion tamarins. However, circumstantial evidence suggests that additional species are golden lion tamarin predators as well: raptors^[41]; capuchin monkeys (Cebus/Sapajus nigritus)^[41][48]; coatimundis (Nasua nasua)^[48]; and tayra (Eira barbara)^[48][49].

Tayra were strongly suspected as the primary predator in a series of deaths and disappearances in Poço das Antas Biological Reserve.^[48] From 1995 to 2000, a sharp increase in predation was noted in the golden lion tamarin study population in the reserve, substantially reducing the estimated reserve population from 350 to 220 individuals during this period.^[48] At least during this period, most documented predation appeared to have occurred overnight, at or in proximity to sleeping sites.^[48] Multiple authors have discussed the role of sleeping site selection in relation to (overnight) predation, noting that tree holes, a den type frequently used by golden lion tamarins, may provide greater protection from predators than other sleeping site types^[48][50][51], although most of the documented events at the Poço das Antas reserve occurred at such tree hole sleeping sites.

Wild golden lion tamarins approach and mob some arboreal and terrestrial predators, e.g., snakes and tayra, as well as perched raptors^[41], but are reported to retreat quietly from capuchin monkeys^[41]p 240. Golden lion tamarins also use alarm vocalizations in reaction to predators. Calls associated with terrestrial/arboreal predators are reported to differ from those associated with flying predators in both captive situations^[52][53][54] and the wild^[41].

Conservation

Aerial view of Poço das Antas Biological Reserve.

The geographic range of and available habitat for golden lion tamarins have both shrunk drastically in the five centuries since the arrival of Portuguese explorers in Brazil in 1500.  However, there are no estimates of the size of the population pre-1500, and the first published estimates did not appear until the 1970’s. By then, golden lion tamarin population estimates ranged from only 100 to 600 surviving individuals^[22][23], although these estimates were not based on range-wide censuses. The first such census, carried out in 1990-1992, counted approximately 560 wild individuals^[20][24] and there were about 100 additional individuals from the reintroduction program living in the wild^[20]. Since then, the population has grown significantly, following conservation efforts that include reintroduction of zoo-born animals^[25][26] and rescue and translocation of wild individuals from small, at-risk forest fragments^[26] (both largely to areas then unoccupied by tamarins), reforestation with a particular focus on connecting separated areas of habitat,^[27][28] and community-based conservation and engagement programs^[29][30]. Most recently, a 2022/2023 census estimated more than 4,800 golden lion tamarins living in the current primary area of occurrence in the non-coastal area of the São João and Macaé river basins^[6], with unknown but smaller additional numbers in limited coastal forests^[7] and to the west of the primary area of occurrence^[8][9].

The Associação Mico-Leão-Dourado (Golden Lion Tamarin Association) is a Brazilian not-for-profit focused on conservation of golden lion tamarins in the primary area of occurrence (the non-coastal area of the São João and Macaé river basins). The Association has identified a number of ongoing threats to continued recovery of the species^{[27][28][55][56]}. Key threats include: habitat loss and fragmentation; hunting and trapping for the pet trade (see ^[57] for recent incidents); the recently highlighted threat of a yellow fever or other disease epidemic^[58] and the potential impact of non-native species, most notably the introduced marmoset species that are now found in many of the forest areas occupied by golden lion tamarins^[59][60][61], and a feral population of introduced golden-headed lion tamarins (Leontopithecus chrysomelas) within 50 km of the geographic range of the golden lion tamarin, presenting a threat of hybridization (most of the golden-headed lion tamarins were removed between 2015 and 2018 ^[62][63]).

Although not specifically identified in Association publications, climate change may also present a threat to long-term survival for golden lion tamarins. Meyer and co-authors^[64] used climate change modeling to estimate how much of the historic geographic ranges of the four lion tamarin (Leontopithecus) species would be suitable for their survival in 2050 and 2080. They concluded that the amount of climatically suitable habitat for golden lion tamarins would be severely reduced by 2050 and insufficient for population survival by 2080. The authors stressed caution in interpreting and acting on this conclusion because of numerous uncertainties in the modeling process.

Key events in the conservation of golden lion tamarins outlined below describe past and ongoing efforts to address many of these threats.

1970’s: Following their field studies, which indicate a small, declining wild population of golden lion tamarins, Adelmar Coimbra-Filho and Alceo Magnanini champion efforts that result in the 1974 creation of the federal Poço das Antas Biological Reserve.^[23][65][66] In 1980, there were an estimated 75 to 150 golden lion tamarins living within the reserve.^[67]

1983: The Golden Lion Tamarin Conservation Program begins activities in Brazil, launching the first systematic field studies of behavioral ecology of golden lion tamarins in the Poço das Antas Biological Reserve, later expanding to the União Biological Reserve and reintroduction sites, and initiating a community-based environmental education program in the area surrounding Poço das Antas.^{[24][30][52][68][69]} The program’s successor, the Associação Mico-Leão-Dourado (Golden Lion Tamarin Association), a Brazilian not-for-profit, was launched in 1992 and is active today.

1984: The first zoo-born tamarins are reintroduced into the wild.^[25][62][52] Reintroductions, totaling 146 zoo-born golden lion tamarins, continue between 1984 and 2000. Additional details appear in a separate section below.

1994 (through 1997): Forty-three wild tamarins are rescued from small, at-risk forest fragments and translocated to the site of the future União Biological Reserve.^[26][70] Additional details appear in a separate section below.

1997: Reforestation efforts are begun by the Associação Mico-Leão-Dourado, with a focus on creating forested corridors to connect separated forest fragments^[71], and thus connect separated subpopulations of golden lion tamarins. By 2022, the Association had planted a total of 4.4 km² (1.7 miles²) with native forest trees, in Poço das Antas Biological Reserve and on 15 private farms with tamarins.^[27][28]

1998: A second federal protected area for golden lion tamarins, the União Biological Reserve, is created^[26][66]. This area had been the release site for tamarins translocated from smaller forest fragments in 1994-1997.

2003: Golden lion tamarin conservation status improves from Critically Endangered to Endangered in the IUCN Red List of Threatened Species.^[56]

2007-2024: The Associação Mico-Leão-Dourado acquires several privately held properties.^{[72][73][74][75]} Each provides opportunities for reforestation to establish critical forest connections between separated golden lion tamarin subpopulations.  

2016: The Associação Mico-Leão-Dourado adopts an overall 2025 goal of 2,000 wild golden lion tamarins living in 25,000 ha (61,766 acres; 250 km², 97 miles²) of connected and protected habitat, which computer modeling suggests would achieve 100% probability of species survival for the next 100 years, with retention of 98% of (then current) genetic diversity during that period.^[55]

2016-2019: An outbreak of yellow fever causes extensive mortality among golden lion tamarins, killing approximately 30% of the wild population, including most or all of the tamarins in the Poço das Antas Biological Reserve.^[58] The Brazilian primatological and public health communities recognize yellow fever as an existential threat to nonhuman primate populations, and develop a dosage of surplus human yellow fever vaccine appropriate for smaller body size animals.^[76] After the Rio de Janeiro Primate Center tests the vaccine’s efficacy and safety on lion tamarins housed there^[76], Associação Mico-Leão-Dourado biologists begin vaccinating wild tamarins in 2021, apparently the first such program for wild individuals of an endangered primate^[77]. As of the end of 2024, 489 individuals had been vaccinated.^[75]

2020: Wildlife passageways across the recently widened highway BR-101 are completed, including one land bridge (in process of being forested) and ten canopy overpasses.^[27][78] BR-101 runs adjacent to a portion of Poço das Antas Biological Reserve and between the two sections of União Biological Reserve, as well as separating Poço das Antas and one section of União from relatively large tamarin subpopulations on the northern side of the highway. The company that designed and constructed the highway expansion was legally required to fund these mitigating actions to maintain and expand fragment connectivity and reduce traffic-related wildlife deaths on this busy^[79] highway. Tamarins were already using two of the canopy overpasses by late 2021.^[78]

2022/2023: The fourth census of wild golden lion tamarins shows an estimated population of more than 4,800 in the species’ primary area of occurrence, indicating rapid recovery from the yellow fever epidemic.^[6]

Reintroduction

In the early 1980’s, the Smithsonian National Zoological Park and the Rio de Janeiro Primate Center initiated a program to reintroduce captive-born golden lion tamarins to bolster the existing wild population, thought to be no more than 600 individuals at the time^[22][23]. From 1984 to 2000, as part of the Golden Lion Tamarin Conservation Program (and later the Associação Mico Leão Dourado), 146 captive-born and seven confiscated wild-born golden lion tamarins were released into the wild. Seventeen of these were released in the Poço das Antas Biological Reserve , early in the program, and the remainder on 20 privately owned ranches and farms in the species’ historic area of occurrence (Kleiman et al. 1986, 1990, 1991.^{[6][25][26][62][70][80][52][81][82]} The animals had been born at or lived in 43 different zoos and research centers in Brazil, Europe, and the United States. None of the release sites, including the specific release sites in Poço das Antas, was thought to have wild golden lion tamarins at the time of the reintroductions.

The reintroduced captive-born golden lion tamarins all had pre-release veterinary examinations. Those from Europe or the United States were quarantined for 30 days, either at one of several designated zoo quarantine facilities before shipment or at the Rio de Janeiro Primate Center after arrival in Brazil. All of the captive-born individuals were acclimated for at least 24 hours in outdoor cages at the reintroduction sites before their release.^[25] The animals were monitored on five or six days per week for at least three months after being released. Most were given supplementary food and artificial shelter boxes for at least several months, and were captured and returned to the release site if they got lost.^[25] This intensive post-release support improved early survival rate, although efforts to train tamarins in survival-critical skills pre-release did not appear to affect post-release survival.^[25]

Over time, some of the reintroduced golden lion tamarins and/or their offspring were translocated to eight other privately owned locations^[30] and recovery of forests on private lands has also allowed the tamarins to expand on their own to additional ranches and farms. As of 2022, 22 of the farms and ranches with golden lion tamarins were official private nature reserves.^[28] At the time of the most recent census, in 2022/2023, there were estimated to be 2,256 surviving descendants of reintroduced golden lion tamarins, representing almost half (46%) of the total estimated population in the species’ primary area of occurrence, in the non-coastal area of the São João and Macaé river basins in the Brazilian state of Rio de Janeiro (calculated from ^[6], Supplementary Material).

Golden lion tamarin on the Brazilian Real R$20 banknote.

Translocation

During a 1990-1992 survey, a number of golden lion tamarin groups were identified in very small and/or immediately imperiled forest fragments in the Rio de Janeiro State municipalities of Cabo Frio, Búzios, Saquarema, and Araruama.^[20] Between 1994 and 1997, under the administration of the Associação Mico-Leão-Dourado (Golden Lion Tamarin Association), 43 individuals from some of these forest remnants, in Cabo Frio, Búzios, and Saquarema (6 family groups and one single individual), were rescued and translocated to the location of what would become (in 1998) the União Biological Reserve^{[26][70][83][84][62]}). The reserve lies within the species’ historic area of occurrence but had no resident golden lion tamarins at the time. The two primary goals of the translocation program were to rescue imminently threatened golden lion tamarins and to add genetic diversity to the more protected part of the population.^[26][70]

The population at the União reserve has grown substantially since the initial translocations. The population had already grown to 120 by December 2000,^[26] and to more than 220 in 30 family groups by 2006.^[70] The most recent census, carried out in 2022-2023 estimated that there were 473 descendants of the original translocated golden lion tamarins.^[6] This represented 10% of the total estimated 2022-2023 population of 4,869 in the species’ primary area of occurrence in the non-coastal area of the São João and Macaé river basins (calculated from ^[6], Supplementary Materials).