Leontopithecus chrysomelas (Kuhl, 1820)

Russell A. Mittermeier, Anthony B. Rylands & Don E. Wilson, 2013, Callitrichiade, Handbook of the Mammals of the World – Volume 3 Primates, Barcelona: Lynx Edicions, pp. 262-346 : 343-344

45 .

Golden-headed Lion Tamarin

Leontopithecus chrysomelas

French: Tamarin-lion a téte dorée / German: Goldkopf-Lowenaffchen / Spanish: Titi lebn de cabeza dorada

Taxonomy. Midas chrysomelas Kuhl, 1820 ,

Brazil, forests of the rios Ilhéos, Pardo, and Belmonte. Restricted by P. Hershkovitz in 1977 to Ribeirao das Minhocas, left bank of upper Rio dos Ilhéus, upper Bahia State.

The lion tamarins were formerly considered to be subspecies of L. rosalia , but a comparative study of craniodental morphology of the genus by A. Rosenberger and A. F. Coimbra-Filho in 1984 concluded that the three taxa known at the time are heterogeneous and individually distinctive with a non-clinal distribution of characters. Anatomically, L. chrysomelas was found to be the most divergent, with a more robust body, relatively large and modified incisors, relatively small cheek teeth, and a unique cranial shape. A molecular genetic phylogeny of the genus by B. Perez-Sweeney and coworkers in 2008 found L. chrysomelas to be basal in the lion tamarin clade. Monotypic.

Distribution. E Brazil (Bahia), between the Rio de Contas (N limit) and the Rio Pardo, but also S of the Rio Pardo along its middle reaches to the Rio Jequitinhonha on the border between the states of Bahia and Minas Gerais. Introduced into the suburbs of Niteroi, Rio de Janeiro State.

Descriptive notes. Head-body 22-26 cm, tail 33-39 cm; weight 540-700 g (males) and 480-590 g (females). The Golden-headed Lion Tamarin’s fur is predominantly glossy black but with thick, long, golden-red and reddish-orange hairs on the front of the mane, forearms, hands, feet, thighs, and upper side of the proximal one-half of the tail.

Habitat. Coastal lowland tropical forest and coastal white sand forest characteristically abundant in piacava palms ( Attalea funifera). Golden-headed Lion Tamarins use secondary growth forest and abandoned rubber plantations, but they evidently prefer oldgrowth forest for its abundance of tree holes, which they use as sleeping sites, and epiphytic bromeliads, which are key foraging sites. They are adaptable and able to live in degraded and secondary forests, depending on sufficient year-round food sources and foraging sites. They are also able to occupy “cabruca” (cacao agroforest plantations, shaded with a few native trees left standing, along with cultivated fruit trees). Cabruca agroforest predominates in the eastern part ofits distribution. Food trees such as fig ( Ficus ), jackfruit ( Artocarpus heterophyllus), and Inga in cabruca can be important food sources, and given sufficient sleeping sites (tree holes) and foraging sites (epiphytic bromeliads), group can live in old cabruca, although predation risk in the more open vegetation and scantier trees is high. Golden-headed Lion Tamarins frequently go to the ground because of the broken/open canopy and open understory. Near the coast in the cacao growing region, there is no distinct dry season, with rainfall exceeding 2000 mm/year (heaviest rains in March—June), but in the western part of their distribution, forests are mesophytic with a distinct dry season, and forests in some areas are semi-deciduous, with rainfall as low as 1000 mm/year.

Food and Feeding. Diets of the Golden-headed Lion Tamarin include fruits, flowers, nectar, gums, and small animal prey, including principally arthropods but also snails, small frogs, lizards, small snakes, and bird eggs. Three groups studied for 2-5 years in Una Biological Reserve ate fruits from 71 species (32 families), nectar from four species of Manilkara (Sapotaceae) and Symphonia globulifera (Guttiferae), flowers from two species (one of them Mabea piriri, Euphorbiaceae ), and, infrequently, gum from gouge holes made by sympatric Wied’s Black-tufted-ear Marmosets ( Callithrix kuhlii ) and seed pods of Parkia pendula ( Fabaceae ). The main families providing fruits included Myrtaceae (Eugenia, Myrcia, Psidium, and Marlierea) , Melastomataceeae ( Miconia , Henriettea ), Moraceae ( Ficus, Brosimium ), Urticaceae (Pourouma) , Fabacae ( Inga ), and Bromeliaceae (Aechmea) . Ttypical of other callitrichids, Golden-headed Lion Tamarins concentrate on just a few species at a time. For example, in any one month, just three species can account for 70-75% of the feeding records on plant foods. With home ranges larger (40 ha or more) than sympatric marmosets (12-30 ha), Golden-headed Lion Tamarins are able to take more advantage of fruiting seasons of each species; they have more individual trees in their home range than, for example, Wied’s Black-tuftedear Marmosets that might have just one. Marmosets depend more on gum. Groups of Golden-headed Lion Tamarins living in cabruca have a less diverse diet offruits (20 or so species, including Myrtaceae and Sapotaceae ), but they benefit from access to cultivated trees that produce fruit for most of the year, including Inga affinis ( Fabaceae ), Ficus gomelleira, and the exotic Artocarpus heterophyllus (both Moraceae ). In 1999-2000, a study of three groups of Golden-headed Lion Tamarin using mature forest, cabruca, and secondary forest found 155 plants species from 49 families in their diets; they ate fruits from 94% of the species, nectar from 5%, and gum from 1%. Golden-headed Lion Tamarins ingest and disperse seeds of many of these species. Golden-headed Lion Tamarins forage for small animal prey in specific microhabitats: nooks and crannies, accumulations of leaf litter in palm crowns and vine tangles, and particularly epiphytic bromeliads (c.76% ofthe time). In cabruca areas, 97% of the foraging sites used by Golden-headed Lion Tamarins were bromeliads (they also eat their pineapple-like, multiple fruits). They forage mostly in the lower and middle canopy 10-20 m above the forest floor. Sympatric marmosets occur lower in the canopy/understory and are stalk-and-pounce, foliage gleaners at heights of 5-13 m above the ground; they almost never forage in bromeliads.

Breeding. Despite a lack of seasonality in rainfall in the coastal region, births of the Golden-headed Lion Tamarin are seasonal, occurring in October-April. Females generally give birth to twins or singletons, just once a year; only four of 15 females monitored for eight years at Una Biological Reserve bred twice per year. Reproductive parameters and mating systems are typical of the genus, as described for the Golden Lion Tamarin. The ovarian cycle is c.21 days, gestation is c¢.125 days, and postpartum ovulation occurs c.17 days later. Female Golden-headed Lion Tamarins do not conceal their reproductive status. They show proceptive sexual presenting, and males increase their frequency of anogenital sniffing and mounting during the fertile period. Males remain close to the female during this time, indicating mate-guarding.

Activity patterns. The Golden-headed Lion Tamarin spends ¢.30-38% of its time traveling, 20-25% stationary and resting, 18-25% foraging for and eating small animals, 12-18% foraging for and eating fruits, 10-15% in social activities, and 2% eating flowers and nectar. Overall, foraging and feeding take up ¢.25-35% of their day. They typically begin their day traveling and feeding on fruits or nectar. During the morning, they increase their foraging on animal prey and then tend to rest from c.11:00 h until 14:00 h. After that, foraging on animal prey and fruits resumes and continues until they retire to their sleeping sites at ¢.16:00-17:00 h. Golden-headed Lion Tamarins use a limited number of sleeping sites, and high rates of travel seen early and late in the day are the result of them going to and from these sites, sometimes traveling several hundred meters in the process. Tree holes are used most commonly, but they also sleep in large bromeliads and in dense vegetation and tangles of lianas.

Movements, Home range and Social organization. Groups of Golden-headed Lion Tamarins are generally 2-8 individuals (although sometimes as large as 15), with 1-3 adult males and one, sometimes two, adult females, along with infants, juveniles, and subadult offspring. They occupy home ranges of 40 ha (Lemos Maia Experimental Station) to as many as 200 ha (Una Reserve), depending on distribution and abundance of their food sources and foraging sites, which are related closely to the mosaic of vegetation types available to them. In Una, home ranges overlap is as much as 36%. They travel 1400-2175 m/day. In cabruca, a home range can be as small as 22-28 ha. Both males and females disperse from their natal groups. Male sibling pairs may set up new groups. It is probable that dispersal and formation of new groups follow the same pattern in the betterstudied Golden Lion Tamarin. The density of the Goldenheaded Lion Tamarin in Una Biological Reserve is 5 ind/km?, but densities were as high as 17 ind/km?* (0-9-3 groups/km?) in certain parts of the forest in nearby Lemos Maia Experimental Station. In cabruca vegetation, densities are higher at 17-21 ind/ km?*. Mammals seen attacking Golden-headed Lion Tamarins include the Tayra (Eira barbara), the Margay (Leopardus wiedii), and dogs. Raptors and snakes are no doubt also significant predators. Groups of Golden-headed Lion Tamarins and Wied’s Blacktufted-ear Marmosets sometimes travel together. This association is more common in open cabruca areas, especially when there are newborn twins in the groups, probably a response to the higher risk of predation there.

Status and Conservation. CITES Appendix I. Classified as Endangered on The IUCN Red List. The Golden-headed Lion Tamarins is threatened by loss of habitat through logging, charcoal production, agriculture, cattle ranching, highway construction, and urbanization. Humid forests in the eastern parts of their distribution were relatively well preserved until the 1970s. Land use was characterized by very large estates where cacao cultivation required only a small portion of the land and left wide expanses of forest intact. The predominant form of cultivation used native canopy trees to shade the cacao trees, so-called cabruca. Modern times brought efforts to maximize profits by clear-cutting the forest and planting rubber trees, fast-growing African Erythrina trees, or bananas to shade the cacao. The fall in price on the world cacao market and the introduction of a fungal disease (Witches’ Broom Disease) from the Amazon severely damaged the industry and the regional economy in the 1980s. Consequences included a diversification of crops (rubber, coconut, oil palm, and pepper), an increase in cattle ranching (clear-cutting for pasture), and a boom in charcoal and logging industries. Resulting rural unemployment caused an influx of squatters who used destructive slash-and-burn agriculture. In the western distribution of the Golden-headed Lion Tamarin, cattle-ranching has been predominant since the 1930s, and the forest is now largely destroyed and highly fragmented; only c.10% ofit remains in scattered fragments. In the early 1990s, the wild population of the Golden-headed Lion Tamarin was estimated to be 6000-15,000 individuals. Areas of cabruca were excluded as unsuitable (although important as corridors for wildlife between forest patches), but recent findings of the high densities of Golden-headed Lion Tamarins in old cabruca plantations indicate that the total population is probably larger. The first protected area for the Golden-headed Lion Tamarin was Una Biological Reserve, created in 1980 and expanded to encompass 18,500 ha in 2007. Various other protected areas have been established in recent years, including Serra das Lontras National Park and Una Wildlife Refuge. Lemos Maia and Canavieiras experimental stations of the regional cacao growing authority also have small populations of Golden-headed Lion Tamarins. There is a well-managed captive breeding program for the Golden-headed Lion Tamarin with a good founder stock, confiscated from illegal export in the early 1980s. Conservation and management of the Golden-headed Lion Tamarin is overseen by an international committee formed by the Brazilian government in 1985. Besides the Brazilian government, the principal motivation behind conservation measures for the Golden-headed Lion Tamarin has come from the Instituto de Pesquisas Socio-Ambientais do Sul da Bahia (IESB) , founded in 1994 specifically to protect it and the forests of the region.

Bibliography. Alger & Caldas (1994), Bach et al. (2001), Ballou (1989), Ballou et al. (2002), Baker et al. (2002), Cardoso et al. (2011), Catenacci et al. (2009), Coimbra-Filho (1969, 1970a, 1977, 1981), Coimbra-Filho & Mittermeier (1973, 1977b), De Vleeschouwer, Heistermann et al. (2000), De Vleeschouwer, Leus & Van Elsacker (2003), Dietz, de Sousa & Billerbeck (1996), French, De Vleeschouwer et al. (2002), French, Pissinatti & Coimbra-Filho (1996), Hankerson et al. (2006), Hershkovitz (1977), Holst et al. (2006), Kierulff, Raboy et al. (2002), Kleiman & Mallinson (1998), Kleiman & Rylands (2002), Kleiman et al. (1988), Mallinson (1984, 1989), Oliveira & Dietz (2011), Oliveira, Hankerson et al. (2010), Oliveira, Neves et al. (2011), Padua et al. (2002), Perez-Sweeney et al. (2008), Pinto & Rylands (1997), Pissinatti et al. (2002), Raboy & Dietz (2000, 2004), Raboy, Christman & Dietz (2004), Raboy, Neves et al. (2011), Rambaldi et al. (2002), Rosenberger & Coimbra-Filho (1984), Rylands (1989a, 1993c), Rylands, Kierulff & Pinto (2002), Rylands, Mallinson et al. (2002), dos Santos & Blanes (1999), Tardif, Santos et al. (2002).

Figures

On followinq pages 46 Black Lıon Tımarın (Leontopırhecus chrysopygus) 47 Black faced Lıon Tırrıarın (Leomopnhocus cmssamì

Distribution. E Brazil (Bahia), between the Rio de Contas (N limit) and the Rio Pardo, but also S of the Rio Pardo along its middle reaches to the Rio Jequitinhonha on the border between the states of Bahia and Minas Gerais. Introduced into the suburbs of Niteroi, Rio de Janeiro State.