Callithrix aurita (E.Geoffroy Saint-Hilaire, 1812)

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 : 315-316

18 .

Buffy-tufted-ear Marmoset

Callithrix aurita

French: Ouistiti oreillard / German: Gelbohr-Blischelaffchen / Spanish: Titi de orejas blancas Other common names: Buffy-tufted Marmoset, \ White-eared Marmoset

Taxonomy. Jacchus auritus E. Geoffroy Saint-Hilaire, 1812 ,

Brazil. Restricted by J. Moojen in 1950 to Silveira Lobo, Minas Gerais State .

A. Humboldt is often credited in various ways with the name of this species, but E. Geoffroy Saint-Hilaire is the rightful authority. Humboldt in 1812 (dated 1811 but actually published a year later) credited Geoffroy Saint-Hilaire for his 1812 publication in Tome 19 of Annales du Muséum d'Histoire Naturelle, where this species’ name first appeared. Humboldt’s nomenclatural act was a “name combination” in which he combined the name given by Geoffroy Saint-Hilaire with the genus Simia. There is some geographic variation. Individuals from Sao Paulo State tend to be paler than those from Rio deJaneiro State. Callithrix aurita and C. flaviceps are closely related, and A. F. Coimbra-Filho believes it was better to consider the latter subspecific. Close similarities exist in their dental morphology, behavior, pelage (infants of the two forms are practically identical in appearance), and long calls. Hybrid C. aurita x C. flaviceps can be found in Carangola, Minas Gerais State. Monotypic.

Distribution. SE Brazil in the states of Minas Gerais, Rio de Janeiro, and Sao Paulo, in the N extending to the Rio Doce State Park in Minas Gerais; its distribution is largely montane at elevations of 600-1200 m.

Descriptive notes. Head—-body 19-25 cm, tail 27-35 cm; weight 400-450 g. The Buftytufted-ear Marmoset is dark brown or black above with buffy speckling. Its underside is ocher. Eear tufts are short (c.2-5 cm) and yellowish-brown, as are hands and feet. There is a white blaze across the forehead and a red patch on the crown.

Habitat. Montane evergreen, semi-deciduous, secondary, scrubby forest, interspersed with stands of bamboo (Chusquea sp. and Merostachys sp.) at elevations up to 1200 m. The 35-ha home range of a group of Buffy-tufted-ear Marmosets studied in the Serra do Mar State Park, Sao Paulo, was composed of a mosaic of young, 12-m high, secondary growth (c.15 years old) with numerous bamboo stands, older 15-m high secondary growth (c.40 years old), and tall (20-25 m) forest, with and without bamboo stands. All recent occurrence records for the Buffy-tufted-ear Marmoset are in submontane and montane forest, although it evidently occurred in lowland forest near the Brazilian coast in the recent past. They forage and travel in the lower canopy and dense vegetation of the understory, 6-9 m above the ground.

Food and Feeding. Studies of the diet and feeding behavior of the Buffy-tufted-ear Marmoset have been conducted in a 17-ha forest patch on a farm in Monte Belo in the south of Minas Gerais and in the Bananal Ecological Station and Serra do Mar State Park (Nucleo Cunha) both in Sao Paulo. During a year at the Minas Gerais site, a group of four individuals ate fruits, seeds, and gums from 27 trees and vines in 16 families, the most important being Fabaceae (especially for gums) but also including Moraceae , Rubiaceae , and Cactaceae . The group fed on gums of 18 species, and gum-feeding accounted for ¢.50% oftheir feeding time; however, 82% was dedicated to Acacia paniculata, a spiny, leguminous vine. Although Buffy-tufted-ear Marmosets would bite at the vine, this was evidently ineffective in stimulating the flow of gum, and like the Buffy-headed Marmoset ( C. flaviceps ), they would mostly trapline for small exudations resulting from wind and insect damage. Fruits comprised 11% of the feeding time, with a focus on small juicy berries and seeds with arils. Maclura tinctoria (Moracae) was particularly important in the diet, and the small seeds of this plant, and of Rhipsalis (Cactaceae) , were found in their feces, indicating a role in dispersal. They also ate plant galls. Gums were eaten throughout the year, but less in the early wet season when fruits were more abundant. Fruit consumption dropped in the late wet season, and fruit was entirely absent in their diet through most of the dry season. Lepidopteran larvae, orthopterans ( Tettigoniidae and Katydidae), cockroaches, spiders, snails, and lizards ( Mabuya , Scincidae ) comprised the animal part of their diet. Time spent foraging for animal prey was quite constant throughout the year. During the early and late dry seasons, Buffy-tufted-ear Marmosets licked up immature hemipterans and their sugary excretions from the stems of a species of Euphorbiaceae . In the dry season, they occasionally followed swarms of army ant ( Labidus , Ecitoninae ) to pick off prey disturbed in the leaflitter. At Serra do Mar State Park, the diet included gums, fruits, insects (particularly Acrididae and Tettigoniidae ), opiliones (harvestmen), small frogs, lizards, and bird eggs and fledglings. During nine months, gums represented 54% of the time spent feeding on plant foods,fruits 31%, and fungi 15%. Fungi were eaten throughout the study but especially in March at the end of the wet season. Ten species were identified as gum sources, three of which were gouged: Prunus sellowii ( Rosaceae ), a common pioneer tree and the most important (78% of the gum-feeding records); a vine Paullinia carpopoda (Sapindacaeae); and two Qualea (Vochysiaceae) trees, visited very occasionally. The second most important species was Inga marginata ( Fabaceae ), the gum of which was exuded due to insect attack (wood-boring insects). Fruits were eaten from 21 plant species. All fruits were sweet and succulent, except for those from Rollinia sylvatica ( Annonaceae ). Among the most important fruits in the wet and dry seasons were Rhipsalis (Cactacaeae) and three species of Inga . Ficus enormis ( Moraceae ), Myrcia ct. fallax ( Myrtaceae ), Casearia decandra (Flacourticaeae), and Solanum cf. excelsum ( Solanaceae ) were also important in the wet season. The Buffy-tuftedear Marmoset does not appear to eat nectar. Fungal fruiting bodies (at least three species) from the culms and leafy branches of bamboos were eaten throughout the year. At the Fazenda Barreiro Rico, Sao Paulo, the Buffy-tufted-ear Marmoset gouged holes and fed on the gum of Astronium graveolens ( Anacardiaceae ).

Breeding. Births of the Buffy-tufted-ear Marmoset have been recorded in the early wet season. The minimum interbirth interval is a little more than five months, indicating postpartum ovulation. A 16-month study of a group of 6-11 individuals in the Serra do Mar State Park recorded five births, four of them in the early wet season when food resources were abundant, especially insects. Three of the births were of singletons rather than twins, and infant survival was low. One of the group’s males copulated with two females, both of which gave birth, indicating polygynous breeding. The dominant female (judged by aggressive interactions) had a higher breeding success. All group members carried infants, but breeding females carried offspring exclusively for 10-28 days after the birth, unlike other marmosets where the mother passes infants to other group members even on the day of the birth. It is possible that this was to avoid infanticide by one of the other breeding females.

Activity patterns. A group of seven individuals studied in the Serra do Mar State Park spent ¢.39% ofits time foraging for animal prey, 18% traveling, 16% eating (plant foods), ¢.6% resting, and 20% in other activities, largely social within the group or interacting with other groups. More time was spent foraging for animal prey (generally 27-30% of the time budget) than is typical of some other species of marmosets. There waslittle difference in these figures between the wet and dry seasons, although there was some variation between months. The group tended to be active for shorter periods in the hot-dry season (nine hours) than in the cool-wet season when they were active for up to 10-5 hours. In the wet season, individuals were active at ¢.06:30-19:00 h. In the dry season, they began the day later at ¢.07:30 h and retired earlier at ¢.16:30 h. When it was cold and raining, they tend to begin their day later. Sleeping sites were always associated with dense vegetation such as bromeliads, vine tangles, and bamboo at heights of c.11 m above the ground.

Movements, Home range and Social organization. Group size of the Buffy-tufted-ear Marmosetis typically 4-8 individuals, but it can be as large as eleven, including 1-2 adults of each sex. Home range sizes of groups were 11 ha and 16-5 ha in two forest fragments in the Fazenda Lagoa, Monte Belo (Minas Gerais), 35 ha at Serra do Mar State Park, and 40 ha at the Bananal Ecological Station. In the group studied in the Serra do Mar, 16% of 35-ha home range overlapped with two other groups, and individuals used c.4-2 ha on any one day, and 22-23 ha in each month. Daily movement averaged about 959 m (range 580-1400 m). They traveled and foraged mostly at ground level to 5 m above the ground, but feeding on fruits, resting, and social behaviors occurred typically at 4-9 m above the ground. The most common expression of social behavior is grooming, carried out largely when the group is resting. Grooming is mostly between adults, and adults are the most common groomers. The younger the individual, the more it is groomed and the less it grooms. Agonistic behaviors include pilo-erection, staring, hitting, and biting. Agonistic interactions are largely contests for food and protecting infants when other individuals try to take them or interact with them. The jararaca (Bothrops jararaca), a venomous pit viper, has been seen attacking and swallowing a Buffy-tufted-ear Marmoset. Densities of the Buffy-tufted-ear Marmosets in an area of the Serra do Mar State Park (Nucleo Cunha) were 20-23 ind/km?. Further studies in the Serra do Mar State Park (nucleos Cunha /Indiaia and Santa Virginia) provided estimates of 7-5 ind/km?* (2-2 groups) and ¢.1386 individuals in 251 km? offorest (taking into account the extent of favorable habitats). In the Fazenda Barreiro Rico, it was rare, with one estimate indicating no more than 8-12 individuals in 2250 ha of forest, although a later survey estimated 15 ind/km?®. A density estimate in a 230-ha forest on another farm in Sao Paulo (Fazenda Sao José) was of 3-5 ind/ km?. Surveys in the Rio Doce State Park, Minas Gerais, provided estimates of relative abundance of 0-02-0-08 ind/km. These populations inhabit harshly seasonal forest in terms of temperature (dry season winter temperatures can be freezing) and rainfall, and they are undoubtedly restricted in their numbers by availability of key resources, particularly in the dry season when there is little or no fruit.

Status and Conservation. CITES Appendix I. Classified as Vulnerable on The IUCN Red List. The extremely small distribution of the Buffy-tufted-ear Marmosetis considerably threatened by habitat destruction, dating back to the earliest days of European colonization in the 1500s. Introduced Common Marmosets ( Callithrix jacchus ), otherwise native to north-eastern Brazil, have invaded many parts of its former distribution in Rio de Janeiro and Sao Paulo. It occurs in the following protected areas: Serra da Bocaina, Serra dos Orgaos , and Itatiaia national parks and Cantareira, Rio Doce, Serra do Brigadeiro (possibly hybrids with the Buffy-headed Marmoset) state parks. It also occurs in Bananal State Ecological Station and private reserves in Fazenda Monte Alegre, Minas Gerais, and Fazenda Barreiro Rico, Sao Paulo.

Bibliography. Bernardo & Galetti (2004), Brandao (1999), Brandao & Develey (1998), Coimbra-Filho (1971, 1972, 1984, 1986b, 1990, 1991), Coimbra-Filho et al. (1993b), Corréa (1995), Corréa & Coutinho (1997), Corréa et al. (2000), Cosenza (1993), Cosenza & de Melo (1998), Coutinho (1996), Coutinho & Corréa (1995), Ferrari & Mendes (1991), Ferrari, Corréa & Coutinho (1996), Hershkovitz (1977), Martins (1998a, 1998b, 2000), Martins & Setz (2000), Mendes et al. (2009), Milton & de Lucca (1984), Mittermeier et al. (1982), Moojen (1950), Muskin (1984a, 1984b), Natori (1986), Norris et al. (2011), Olmos & Martuscelli (1995), Rylands & de Faria (1993), Rylands, Coimbra-Filho & Mittermeier (1993, 2009), Rylands, da Fonseca et al. (1996), Santos & Martins (2000), Stevenson & Rylands (1988), Torres de Assumpcéao (1983).

Figures

On following pages 19 Buffy-headed Marrnoset (Cal/:rhnx flawcepsá 20 Geoffroy s Tuftedear Mamıoset (Ca/Iırhnx gooflroyı), 21 Wıed s Black tufted-ear Mannoset (Callıthrıx kuhlıı), 22 Block-tufted-ear Marmoset (Callnhnx penıcıllata) 23 Common Mannoset (Calhthnx ¡aochusf

Distribution. SE Brazil in the states of Minas Gerais, Rio de Janeiro, and Sao Paulo, in the N extending to the Rio Doce State Park in Minas Gerais; its distribution is largely montane at elevations of 600-1200 m.