History of the Golden Lion Tamarin
Captive Breeding Program
extracted from: Ballou, J. D., D. G. Kleiman, J. J. C. Mallinson, A. B. Rylands, C. Valladares-Padua, K. Leus. History, management and conservation role of the captive lion tamarin populations. In: Kleiman, D. G. and A. B. Rylands (eds). The Conservation Program of the Lion Tamarins. Smithsonian Institution Press.
Only a few marmosets and tamarins existed in zoos in the 19th and early 20th centuries and the first birth of a golden lion tamarin was recorded at the London Zoo on 13 November 1872. However, it was generally considered that the species was delicate in captivity and seldom successfully reproduced. A detailed account of the history of the golden lion tamarin in captivity outside Brazil is presented by Mallinson (1996). In 1962, Alceo Magnanini and Aldemar F. Coimbra-Filho first attempted breeding L. rosalia, in the hopes of establishing a reintroduction program; lion tamarins were already extinct throughout a large part of their original range (Coimbra-Filho and Magnanini 1968). In 1963, the project was moved to the Rio de Janeiro Zoo (Magnanini and Coimbra-Filho 1972; Magnanini et al. 1975) where Coimbra-Filho was the head of the Research Department (Coimbra-Filho 1965). Later, in 1972-1974, Coimbra-Filho and Magnanini established the Tijuca Biological Bank, sponsored by the International Union for the Conservation of Nature and Natural Resources (IUCN), the World Wildlife Fund (WWF) and the Brazilian Government, specifically for the conservation and captive breeding of lion tamarins (Coimbra-Filho and Mittermeier 1977; Coimbra-Filho et al. 1986).
By 1965, the international zoo community was becoming aware of the endangered status of the golden lion tamarin. Through the efforts of Clyde Hill of the San Diego Zoo, the American Association of Zoological Parks and Aquariums (AAZPA; later renamed the Association of Zoos and Aquariums, or AZA) formally recognized the golden lion tamarin as an endangered species in 1966 and agreed to support a ban on its importation to the United States. AAZPA also recommended that the species be included in the IUCN "Red Data Book" for rare and endangered species. In 1967, the International Union of Directors of Zoological Gardens and Aquariums (IUDZG; in 2000 renamed the World Zoo Organization - WZO), also pledged that its members would not import the species and furthermore would help to publicize the animal’s endangered status (Hill 1970).
In 1966, the Wild Animal Propagation Trust (WAPT), one of the earliest zoo-based organizations established to conserve endangered species, created a Golden Marmoset Committee. In 1969, under the direction of Donald Bridgwater, the Committee began to monitor the status of the captive golden lion tamarin population and to develop management policies, encourage loan agreements, and act as a clearing house for the exchange of individuals (Bridgwater 1972b).
In 1972, WAPT sponsored the ground-breaking conference "Saving the Lion Marmoset," at the Smithsonian Institution’s National Zoological Park (SNZP) that brought together 28 European, American and Brazilian biologists who reviewed and analyzed all available data on the lion tamarins and other callitrichids. Long-term recommendations for husbandry were developed for research and conservation activities, including support for the breeding program in Brazil, studies of breeding biology, protocols for captive husbandry and management, medical programs, hand-rearing guidelines, inter-institutional cooperation and the establishment of a studbook and a data bank to record all aspects of their captive propagation (Kleiman 1972; DuMond 1972).
Following this important meeting, SNZP made a major commitment to the captive propagation and conservation of the golden lion tamarin and launched a long-term investigation into the reproduction, social behavior, and husbandry of the species in captivity (Kleiman 1972). At the time, little was known about the zoo biology of Leontopithecus. A lack of knowledge about the mating and social system lead to uncertainty about whether they were best kept as monogamous or polygynous breeding groups (Kleiman 1977c; 1978b). Research on behavior and husbandry overseen by Kleiman began in earnest in the mid-1970s. The first international studbook on L. rosalia was published by Marvin Jones (1973), and subsequently maintained by Devra Kleiman. Jonathan D. Ballou, who developed one of the first computerized database systems for managing studbooks, took it over in 1983 (Ballou 1983-1996).
Until 1975, the reproductive trends of the golden lion tamarin population were disheartening. Population increase was minimal and the survivorship of both adults and young remained poor (Figure of the GLT Captive Population Size over time). During the period 1964-1974, there was a 1968 peak in numbers of L. rosalia in captivity outside of Brazil, but this was believed to be due to a flurry of last minute exports before trade was banned. The captive population declined from then on (Coimbra-Filho and Mittermeier 1977). In an analysis of breeding performance and survival outside of Brazil through the mid-1970s, Kleiman (1977a, 1977b) concluded "the breeding programme to date has had conspicuously poor success." It was clear that without a dramatic reversal over the next two to three years, it would be unlikely to achieve a self-sustaining captive population of golden lion tamarins (Kleiman and Jones 1978).
At the end of 1975, there were 83 L. rosalia in 16 institutions outside of Brazil, and the Tijuca Biological Bank, Rio de Janeiro, held a further 39 specimens (Kleiman 1977b). These populations increased little over the following three years, but by applying the results of captive research, and by using the studbook data to avoid inbreeding through the careful pairing of young animals, the numbers increased dramatically during 1979 and 1980.
By 1980, when the captive population was expanding exponentially, Kleiman organized zoos owning the specimens to begin seeding new zoos with breeding groups on loan. In an unusual decision for the time, the zoos having ownership of the majority of the captive population agreed to refrain from selling their stock to prevent the possibility of golden lion tamarins entering the animal trade. Then, in 1981, the zoos both owning and holding golden lion tamarins on loan agreed to formalize this arrangement and become part of an International Research and Management Committee (IRMC), with all decisions concerning the management of the captive population being in the hands of an elected sub-group. The IRMC consisted of representatives from the six institutions owning all the captive L. rosalia at the time, as well as elected representatives from zoos holding breeding pairs that were on loan. The first task of the Committee was to develop the Cooperative Research and Management Agreement (CRMA), which established the basis for the international captive breeding program. The CRMA stated, among other things, that: 1) All signatories of the agreement would pool their specimens to form a founding stock that would be managed as a single unit; 2) no specimen would be sold, traded or otherwise used in a commercial transaction; 3) all signatories would agree to abide by the management recommendations of the Committee, and no animals would be transferred to another institution or bred without the specific consent of the Committee; 4) each institution would submit data on an annual basis to the International Studbook Keeper; 5) any institution wishing to receive golden lion tamarins must be approved through a formal application procedure to the IRMC and sign the CRMA; 6) and that the agreement would remain in effect for the lifetime of the animals and their progeny.
All institutions holding L. rosalia at that time signed the agreement. The CRMA is still in effect and was the first such agreement to give management responsibility and authority of animals owned by and located at multiple institutions to a central oversight committee. The AZA was later to use the golden lion tamarin IRMC and the CRMA as the model for their Species Survival Plan (SSP©).
Since 1981, the IRMC has undergone several significant changes. On 28 September 1990, the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis (IBAMA - Brazilian Institute of the Environment and Natural Resources) formally recognized the Management Committee as the official advisory body to the Brazilian government on both captive and wild conservation issues for L. rosalia (Kleiman and Mallinson 1998; Rambaldi et al. this volume). On 31 December 1991, six of the seven institutions that owned the majority of the captive L. rosalia population agreed to transfer ownership of their animals to the Brazilian government. Monkey Jungle, Inc., in Miami, Florida, retained ownership of their animals for financial reasons, but still participates fully in the program and remains a signatory of the CRMA. As a result, the Brazilian government is the owner of all but a handful of the 489 existing specimens of captive golden lion tamarins. This may be the first example of a species in which the ownership (but not possession) of all but a very few captive animals by multiple international zoos was returned to the jurisdiction of the native country. With this transfer of ownership and the new responsibilities of the Committee, the membership has changed and now consists of officially appointed members, advisors, and elected representatives with expertise in both captive breeding and the conservation of lion tamarins in the wild.
The zoo population of golden lion tamarins has been managed globally since 1973, and in 1981 was one of the first species to be designated as part of the American Zoo and Aquarium Association's Species Survival Plan (SSP). The population is currently managed intensively by the now- International Committee for the Conservation and Management of Leontopithecus (ICCM) under the guidance of Jonathan Ballou, the Studbook Keeper.
Genetic and demographic management
The research conducted in the 1970s led to significant improvements in captive breeding success, and a rapid increase in the global population. By the late 1980s the population was reaching upwards of 500 individuals (Figure of the Growth of the Captive Population Over time). At this time, the management goal was for rapid population growth with little attention paid to genetics beyond avoiding close inbreeding. As a result, there were substantial differences in reproductive success among breeding pairs (e.g., one pair [#123 and #195 at SNZP] had been used extensively for behavioral research, and produced 55 offspring) (Figure 4-2). Because of the rarity of transferring individual lion tamarins between zoos at the time, the genetic contribution from many potential founders was not realized. The studbook shows that of 243 wild-caught individuals brought into the captive population internationally since 1960 (Ballou and Mickelberg 2001), many either failed or were not given the opportunity to reproduce, and consequently their lineages died out. By 1980, the captive population was descended from only 41 true founders (i.e., wild-caught animals that have left descendants in the 1980 population).
Although management objectives for the captive lion tamarins were still undefined, it was recognized that the population needed to be expanded, that inbreeding should be avoided and that the population should be managed as a single genetic unit. The overall intent was to secure a genetic and demographic reservoir for, but independent of, the wild population. The IRMC was able to meet these objectives as the population expanded globally.
By 1982, the importance of maintaining genetic diversity was widely recognized, and from then until 1989, management protocols attempted to equalize the genetic contribution of founders, in addition to the avoidance of inbreeding (Ballou and Foose 1996). Genetic management had to compensate for the differential reproduction among early breeding pairs since genes from the founders #123 and #195 mentioned above accounted for almost 2/3 of the diversity in the 1982 gene pool. The challenge to the management group was to identify (and preferentially breed) descendents from underrepresented founders. A detailed pedigree analysis of founder contributions was the basis for the first Global Masterplan in 1982, and a specific recommendation to breed, transfer, or place in non-breeding groups was made for all of the 328 individuals in the population.
The 1984 Workshop on Genetic Management of Captive Populations, held at SNZP’s Conservation and Research Center in Front Royal, Virginia, provided the basis for formalizing the genetic objectives for this and other captive breeding programs. Soulé et al. (1986) recommended that captive populations be of sufficient size to maintain 90% of the wild species genetic diversity for a period of 200 years. (The time frame was later shortened to 100 years.) Given data on species biology and number of founders, it was possible to calculate directly the population sizes needed to reach this objective (Ballou 1987). For golden lion tamarins, this resulted in a target population of about 500, and demographic objectives were developed to manage the population at this size.
As the population approached 500 individuals, reproduction was controlled through selective contraception and single-sex groupings (Ballou 1996). Currently, breeding is accomplished solely to maintain demographic and genetic stability and to provide animals for reintroduction. Presently zero population growth requires breeding only 40 pairs (16% of the population) per year so a majority of the population is always held in non-breeding situations. Careful consideration, therefore, has to be given as to which animals breed, how often and with whom.