Bradypus torquatus Illiger, 1811

Hayssen, Virginia, 2009, Bradypus torquatus (Pilosa: Bradypodidae), Mammalian Species 829 (1), pp. 1-5 : 1-4

Bradypus torquatus Illiger, 1811

Maned Three-toed Sloth

Bradypus didactylus Linnaeus, 1758:34 . Part.

Br [adypus]. torquatus Illiger, 1811:109 . No type locality, restricted to ‘‘the Atlantic drainage of Bahia, Espírito Santo, and Rio de Janeiro,’’ Brazil (Wetzel and Avila- Pires 1980:834); further restricted to ‘‘aos arredores de Salvador, Estado da Bahia, Brasil’’ ( Vaz 2003:3). First use of current name combination.

Ch [oloepus]. torquatus: Illiger, 1811:110 . Name combination.

Bradypus [( Choloepus )] torquatus: Desmarest, 1816:327 . Name combination.

[ Bradypus ] cristatus Hamilton-Smith , 1827: 278 in Griffith, Hamilton-Smith , and Pidgeon (1827). No type locality; identified as Brazil ( Swainson 1835:207) .

[ Bradypus ] melanotis Swainson, 1835:207. Type locality ‘‘ Brasil .’’

[ Bradypus ([ Acheus ])] Acheus torquatus: Lesson, 1840:270 . Name combination.

Bradypus crinitus Gray, 1850:67 . Type locality ‘‘ British Guiana,’’ now Guyana.

Bradypus affinis Gray, 1850:68 . Type locality ‘‘Tropical America.’’

Hemibradypus mareyi Anthony, 1907:220 . No type locality.

Hemibradypus torquatus: Menegaux, 1908:702 . Name combination.

Bradypus (Scaeopus) torquatus: Menegaux, 1909:27 . Name combination.

Scaeopus torquatus: Poche, 1908:569 . Name combination.

CONTEXT AND CONTENT. Order Pilosa , suborder Folivora , family Bradypodidae , genus Bradypus , subgenus Scaeopus . Synonymy is modified from Gardner (2005, 2008). Gray’s

(1850) type locality for Bradypus crinitus is far north of the current distribution of B. torquatus and is probably an error due to incomplete knowledge of the distribution of B. torquatus in the mid-1800s ( Gardner 2008). B. torquatus is monotypic.

NOMENCLATURAL NOTES. The generic name, Bradypus , is from the Greek for slow-footed. The species name, torquatus , is from the Latin for collared ( Borror 1960). Other common names are maned sloth, Atlantic forest maned sloth (Lara-Ruiz and Chiarello 2005), preguiça de coleira, aí-pixuna (Wetzel and de Avila-Pires 1980), paresseux a` collier ( Anthony 1953), and bicho preguic¸a (Oliver and Santos 1991).

DIAGNOSIS

Male Bradypus torquatus lack the middorsal speculum present in male B. variegatus ( Wetzel 1985) . Adults of B. variegatus lack the black mane present on adults of B. torquatus ( Wetzel 1985; Fig. 1 ). Skulls of B. torquatus have inflated pterygoid sinuses ( Fig. 2 ), whereas pterygoids of B. variegatus are not inflated ( Wetzel 1985).

GENERAL CHARACTERS

Pelage is uniformly pale brown over body and head except for long, black hairs (the mane) on base of neck that project over the shoulders ( Wetzel 1985). Males do not have a speculum. Pterygoid sinuses are inflated ( Wetzel 1985). In 2 samples, females were larger than males (mm or g; mean, SE, range, n [Lara-Ruiz and Chiarello 2005]; total length; mean, SD, range, n [ Pinder 1993], separate tail and head– body length, respectively): females: length of head and body, 680, 1.051, 590–752, 21; 629.8, 31.75, 590–672, 5; length of tail, 47.6, 5.03, 40–52, 5; mass, 6,900, 343, 5,100 –10,100, 21; 5,281.7, 655.76, 4,500 –6,200, 5; males: length of head and body, 646, 0.776, 620–720, 15; 550.4, 0.89, 550–552, 2; length of tail, 50.8, 1.79, 50–54, 2; mass, 6,150, 274, 4,600 –7,500, 15; 4,428, 327.06, 4,050 –4,900, 2. Measurements of 2 adults (mm or g) were total length, 500, 540; length of tail, 48, 50; length of hind foot, 100, 115; mass, 3,600, 4,150 ( Wetzel 1985).

Greatest length of skull of 10 adults was 77.2 mm (SD 5 3.2 mm; range 5 73.5–84.3 mm; n 5 10) and length of mandibular spout was 6.1 mm (SD 5 0.8 mm; range 5 4.8– 7.1 mm; n 5 8 — Wetzel 1985). Cranial measurements (mm, as illustrated by Anderson and Handley [2001]) of 1 adult female ( United States National Museum [USNM] 259473; Fig. 2 ) were: greatest length of skull, 78.35; posterior zygomatic breadth, 40.83; postorbital breadth, 24.22; length of squamosal process, 27.16; breadth of squamosal process, 4.67; length of maxillary toothrow, 23.43; postpalatal length, 36.49; palatal breadth, 17.34; depth of braincase, 32.51; breadth of antorbital bar, 3.93; length of descending jugal process, 14.59; diameter of external auditory meatus, 4.98; breadth of ascending mandibular ramus, 19.39. A detailed comparison of a skull of B. torquatus with 3 skulls of Bradypus (but not torquatus ) is available ( Santos 1977).

Both males and females have a black mane, but those of males are usually larger and darker, especially in the and Chiarello 2005). The clitoris resembles a small undeveloped penis (Lara-Ruiz and Chiarello 2005).

middorsum. The mane of females can appear as 2 discontinuous lateral tufts (Lara-Ruiz and Chiarello 2005). Neonates lack the mane of adults ( Pinder 1993).

DISTRIBUTION

Bradypus torquatus has a disjunct distribution ( Fig. 3 ) in the Atlantic coastal forests of southeastern Brazil (Lara- Ruiz et al. 2008). The historic distribution extended further north along the coast (from Rio Grande do Norte to Rio de Janeiro) and was not disjunct ( Gardner 2008; Wetzel and Avila-Pires 1980). No fossils are known (Patterson and Pascual 1968).

FORM AND FUNCTION

Hairs of Bradypus torquatus have neither a medulla nor pigment granules ( Aiello 1985). Individual hairs have transverse cracking that increases with age ( Aiello 1985). Algae occur in the transverse cracks of young and middleaged hair ( Aiello 1985). The central portion of teeth of B. variegatus is a modified orthodentine with numerous vascular canals and few or no dentinal tubules ( Ferigolo 1985). Illustrations of the telencephalon are available ( Anthony 1953). Testes are within the abdomen (Lara-Ruiz

ONTOGENY AND REPRODUCTION

Litter size is 1. The smallest infant captured had remnants of the umbilical cord and weighed 300 g (Lara- Ruiz and Chiarello 2005). Another small infant was 365 g (7% of maternal mass) when captured ( Pinder 1993). The heaviest suckling infant was 800 g (Lara-Ruiz and Chiarello 2005). The heaviest juvenile being carried was 1,600 g ( Pinder 1993). Infants do not have black manes, and determination of sex for both infants and juveniles by external features is not possible (Lara-Ruiz and Chiarello 2005). Neonates without manes are more camouflaged in their mother’s fur ( Fig. 4 ) than are juveniles with developing manes ( Pinder 1993).

One copulation was observed in September (Dias et al. 2008). Births may occur year-round ( Pinder 1993), but 15 of 20 births were estimated to occur between February and April (Dias et al. 2008), including a female that gave birth in February–March in 5 successive years (Lara-Ruiz and Chiarello 2005). Small neonates have been found with their mothers in April, May, and July (Lara-Ruiz and Chiarello 2005; Pinder 1993). A juvenile was caught in November, and 2 juveniles near weaning were caught in August and December ( Pinder 1993).

Neonates eat their 1st solid food at 2 weeks, but suckling continues until 2–4 months; young become independent at 9–11 months (Lara-Ruiz and Chiarello 2005). Growth does not stop at sexual maturity (Lara-Ruiz and Chiarello 2005).

ECOLOGY AND BEHAVIOR

Bradypus torquatus is an arboreal folivore endemic to the Atlantic coastal forests of Brazil (Lara-Ruiz and Chiarello 2005). It is sympatric with B. variegatus in the eastern coastal areas of Brazil below 1,500 m in elevation (Oliver and Santos 1991).

Home ranges of 3 animals were 0.5–6 ha ( Chiarello 1998a). Mean home-range size is 5.4–5.6 ha ( Chiarello 2008). Examination of these data estimates population density at 0.09–1.25 individuals/ha ( Chiarello 2008). Distance traveled on average was 24 m over 24 h, 5 m at night and 17 m during the day ( Chiarello 1998a).

Percentages of daylight behaviors for 3 animals (observed for 66 days over 14 months) were resting, 60–80%; feeding, 7– 17%; moving, 6–17%; and grooming, 1–6% ( Chiarello 1998a). Percentage of time feeding was 2 times higher in the dry (19%) than the wet season (9%— Chiarello 1998a). In the Poc¸o das Antas Biological Reserve in Rio de Janeiro, Brazil, B. torquatus is nocturnal ( Gilmore et al. 2001).

underfur, ticks Amblyomma varium and Boophilus underneath the thighs, and the coleopteran Trichilium in the lower back and thighs ( Pinder 1993). Most (83%) of the ticks were male ( Pinder 1993).

Bradypus torquatus has been successfully translocated ( Chiarello et al. 2004). A wild male B. torquatus lived at least 12 years (Lara-Ruiz and Chiarello 2005). B. torquatus can be tranquilized with a mixture of 1.3 mg /kg ketamine with 0.1 mg /kg acepromazine ( Pinder 1993).

GENETICS

Bradypus torquatus has a diploid number (2n) of 50 chromosomes and a fundamental number (FN) of 64 with 8 submetacentric or metacentric and 32 acrocentric autosomal pairs. The X chromosome is submetacentric, and the Y chromosome is metacentric (Jorge and Pinder 1990; Pinder 1993). For 19 individuals from 2 regions, a 332-base pair (bp) mitochondrial DNA fragment of the control region yielded 9 haplotypes with 16 polymorphic sites (Moraes- Barros et al. 2006). For 70 animals from 9 regions, a 370-bp mitochondrial DNA fragment from the control region yielded 6 haplotypes with 21 variable sites, and a 632-bp fragment of the cytochrome oxidase subunit yielded 5 haplotypes with 48 variable sites (Lara-Ruiz et al. 2008). Divergent genetic clusters were specific to different geographic regions (Lara-Ruiz et al. 2008). The 16S mitochondrial DNA from 3 B. variegatus and 2 B. torquatus estimates a split between the lineages 7.7 million years ago ( Barros et al. 2003).

Leaves from 21 species (16 trees and 5 lianas; 12 families, 15 genera) formed 99% of the diet of 3 animals ( Chiarello 1998b), measured as time spent feeding. Single animals ate leaves from 7–12 species, and young leaves were preferred over mature leaves ( Chiarello 1998b). Foraging on Ficus (Moraceae) , Mandevilla (Apocynaceae) , Micropholis venulosa (Sapotaceae) , and Prunus (Rosaceae) constituted 56% of feeding time ( Chiarello 1998b). Indivuduals are specialist folivores, but B. torquatus as a species is a generalist folivore ( Chiarello 2008). Diets of individual animals are composed of few plant species, but populations of individuals forage on many species.

Ectoparasites from the pelage of 28 B. torquatus included Cryptosis (Lepidoptera, a sloth moth) in the

CONSERVATION

Bradypus torquatus is listed as endangered by the International Union for the Conservation of Nature ( Chiarello et al. 2006) and vulnerable by the Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renova´ veis ( Costa et al. 2005). The main threats are habitat loss, continued population decline (Oliver and Santos 1991), a small geographic range, and the fragmented nature of its habitat (Aguiar and Fonseca 2008). Examination of genetic data suggests that the northern and southern distributions should be managed as separate species (Lara-Ruiz et al. 2008).

Figures

Fig. 1.—Mane of an adult male Bradypus torquatus from Santa Teresa municipality, state of Espírito Santo, Brazil. Used with permission of the photographer A. Chiarello, who retains the copyright.

Fig. 2.—Dorsal, ventral, and lateral views of cranium and lateral view of mandible of an adult female Bradypus torquatus (United States National Museum 259473). Greatest length of cranium is 78.35 mm.

Fig. 3.—Current distribution (brown with hatching) of Bradypus torquatus along the southeastern Atlantic coastal area of Brazil (Lara-Ruiz et al. 2008). Historic distribution extends further up the northeastern coast and is not disjunct (Gardner 2008).

Fig. 4.—Face of adult female Bradypus torquatus (top) and adult female with infant (bottom), both from Santa Teresa municipality, state of Espírito Santo, Brazil. Used with permission of the photographer A. Chiarello, who retains the copyright.