HMW 8 - Family text: Bradypodidae (Three-toed Sloths)

Family text: 

Class Mammalia

Superorder Xenarthra

Order Pilosa

Suborder Folivora

Family BRADYPODIDAE (Three-toed Sloths)

  • Medium-sized arboreal folivores with long limbs, three long claws on forelimbs and hindlimbs, short vestigial tails, and foregut-fermenting digestive systems.
  • 55–85 cm.
  • Neotropical Region.
  • Low-elevation tropical forests.
  • 1 genus, 4 species, 4 taxa.
  • 1 species Critically Endangered, 1 species Vulnerable; none Extinct since 1600.

Systematics

The suborder Folivora contains two families of tree sloths: Megalonychidae, the two-toed sloths, and Bradypodidae, the three-toed sloths. Megalonychidae includes an early Neotropical radiation of the giant ground sloths that speciated from the rest of the Choloepus genus 10–20 million years ago; however, a poor fossil record and lack of molecular resolution have prevented a clear determination of Bradypodidae relative to extinct giant ground sloth lineages. Bradypodidae and Megalonychidae diverged from each other during the Oligocene–Miocene 20–30 million years ago.

The family Bradypodidae contains the single genus of Bradypus and four species: the Brown-throated Three-toed Sloth (B. variegatus), the Pale-throated Three-toed Sloth (B. tridactylus), the Maned Three-toed Sloth (B. torquatus), and the most recently described Pygmy Three-toed Sloth (B. pygmaeus), an island endemic. The Maned Three-toed Sloth is the sister group of the other three species of Bradypus and is an endemic species in the Atlantic Forests of coastal Brazil. It diverged from the other species of Bradypus 19–21 million years ago. Some researchers have advocated that because of its deep divergence time and relative distinctness, the Maned Three-toed Sloth should be placed in its own genus, Scaeopus.

The Brown-throated Three-toed Sloth and the Pale-throated Three-toed Sloth diverged 5–6 million years ago. The Brown-throated Three-toed Sloth has an extensive distribution in the Neotropics, extending from Nicaragua to the Atlantic Forests in southern Brazil. The Pale-throated Three-toed Sloth has a more restricted distribution, confined to the north-central region of South America. The Brown-throated Three-toed Sloth and the Pale-throated Three-toed Sloth appear to occur sympatrically in north-central Brazil and central Venezuela.

The Pygmy Three-toed Sloth is restricted to Isla Escudo de Veraguas in the islands of Bocas del Toro; the island is only about 4 km2 and 18 km from the coast of Panama. This island population of three-toed sloths was described as a distinct species based on morphometric analyses. It has a notably smaller body size (2·5–3·5 kg) compared with mainland and other populations of the Brown-throated Three-toed Sloth. More recent molecular analyses provide different conclusions regarding taxonomic status of the Pygmy Three-toed Sloth. Mitogenomic work found that the Pygmy Three-toed Sloth was a distinct lineage that diverged from the Brown-throated Three-toed Sloth and the Pale-throated Three-toed Sloth eight million years ago. This work, however, only included Brown-throated Three-toed Sloths from South America and not from neighboring populations in Central America. Another study that included mitochondrial DNA analysis of Pygmy Three-toed Sloths with Brown-throated Three-toed Sloths from neighboring Central America did not find support for a deep split for Pygmy Three-toed Sloths. Despite the current uncertainty of the taxonomic status of the Pygmy Three-toed Sloth, it is treated here as a distinct species.

Morphological Aspects

Because all species in the genus Bradypus are strict arboreal folivores, their morphology is associated with an arboreal lifestyle. Notably, all four species of three-toed sloths have a suite of adaptations to minimize energetic expenditures and optimize size to persist in a tightly constrained niche. Three-toed sloths are medium-sized mammals that possess ruminant-like, foregut-fermenting digestive systems and peg-like, simple, and ever-growing teeth that lack enamel. They have small heads with eyes oriented anteriorly. Although not visible, three-toed sloths have small pinnae and small vestigial tails. They have three long claws on all limbs, with those on the forelimbs 1–2 times longer than those on the hindlimbs.

Three-toed sloths weigh between more than 2 kg and about 10 kg; the Pygmy Three-toed Sloth is the smallest (2·5–3·5 kg), and the Maned Three-toed Sloth is the largest (4·6–10·1 kg). In general, female three-toed sloths are larger than males. Uniquely, three-toed sloths have additional cervical vertebrae (eight or nine cervical vertebrae) and fibrinous adhesions that anchor the abdominal organs to the lower ribs. This appears to prevent the weight of the abdominal contents from pressing on the lungs when an individual is hanging in an inverted position.

Three-toed sloths are gray to brown in color with long, coarse hair. Their hair is oval-shaped (0·4 mm wide), with irregular transverse fissures that soak up water when it rains. Dorsal hairs create a suitable microenvironment for mutualistic algae in the genus Trichophilus spp. to grow and become abundant. The presence of algae causes their hair to have a green tinge, which creates a camouflage against the green background of the tropical forest. In addition to algae and other microbiota, three-toed sloths harbor abundant populations of flightless sloth moths (Pyralid spp.) in their fur. Male Brown-throated Three-toed Sloths and male Pale-throated Three-toed Sloths have a dorsal speculum of shorter cream to orange colored hair, with a dark stripe running vertically down the center of it. The contrast of the dorsal stripe appears to become accentuate with age. Maned Three-toed Sloths do not have a dorsal speculum, but they do have a pronounced black mane—hence their common name.

Habitat

Three-toed sloths are distributed in Neotropical forests from Honduras through Central America and as far south as Bolivia, Paraguay, south-eastern Brazil, and northern Argentina. Throughout their collective distributions, they occupy vertically and horizontally complex forests. Three-toed sloths can reach relatively high densities, even constituting a majority of the non-volant mammalian biomass within these forests. Three-toed sloths are also capable of persisting in agricultural landscapes if overhead canopy trees are maintained. Three-toed sloths do not occur above at elevations of about 1000–2000 m, which appears to be a consequence of energetic constraints.

All three-toed sloths are strict folivores, and they use many different tree species. Individual three-toed sloths will specialize in a few species of trees and even spend a disproportionate amount of time resting and foraging in just a few individual trees, or “modal” trees, in their home ranges. Genera of trees that are commonly used by three-toed sloths include Cecropia and Coussapoa (both Urticaceae), Micropholis (Sapotaceae), Ficus (Moraceae), and Prunus (Rosaceae).

General Habits

Low levels of activity are characteristic for all species of three-toed sloths. Individual three-toed sloths spend most of their time resting or eating in forest canopies. Adult three-toed sloths typically sleep for 15–18 hours/day, often resting in the crotch of a tree. Three-toed sloths are active diurnally and nocturnally, but they appear to be more regularly active during the daylight hours. Three-toed sloths exhibit large swings in their body temperatures (i.e. heterothermy), and therefore, they behaviorally adjust to ambient temperatures throughout the day. Individuals have been observed in the mornings ascending to top of forest canopies, presumably to warm in full sunlight and descending into shade as daytime temperatures increase. The large fluctuations in body temperature result in significant energetic savings and likely contribute to their very low metabolic rates. Three-toed sloths have the lowest daily energetic expenditure recorded for any non-hibernating mammal. In addition to behavioral adaptations to thermoregulate, their long, coarse, and dense hair likely reduces thermal conductance and buffers them against changes in ambient temperatures. The fact that sloth hair, due to cracks in shafts of hair, also absorbs large quantities of water might further increase the mass-specific heat of the hair and further reduce changes in body temperature.

About once a week, adult three-toed sloths descend to bases of trees where they create superficial depressions on the ground with their vestigial tails and deposit their dung. After defecating, three-toed sloths cover their latrines with leaf litter and ascend back into the forest canopies. This ritualized behavior is risky and energetically costly for three-toed sloths. Nevertheless, these costs appear to be at least partially offset by the benefits that this behavior yields. By regularly descending a tree to defecate, a three-toed sloth transports phoretic (symbiotic) “sloth moths” (Pyralidae) to their oviposition sites in sloth dung, which promotes moth colonization of sloth fur. Moth detritus acts as fertilizer and increases levels of inorganic nitrogen in sloth fur, which fuels algal growth that gives three-toed sloths their greenish tinge and likely increases their concealment in tree canopies.

Three-toed sloths are vulnerable to many predators, and they primarily rely upon concealment in the canopy to evade predation. Several terrestrial predators including cats such as Jaguars (Panthera onca), Margays (Leopardus wiedii), and Ocelots (L. pardalis); dogs such as Coyotes (Canis latrans) and domestic dogs; large snakes (e.g. anaconda, Eunectes spp.); and raptors (spectacled owls, Pulsatrix perspicillata, and harpy eagles, Harpia harpyja) are known to prey on three-toed sloths. In addition to predation, three-toed sloths are susceptible to starvation, especially during the rainy season, and tropical diseases. Nevertheless, three-toed sloths are relatively long-lived have high annual survival rates and reach 12–15 years in the wild; some individuals likely have considerably longer lifespans.

Communication

Vocal communication occurs between mother three-toed sloths and their young, and young will often call when separated from their mother. Calls of juvenile three-toed sloths are brief whistles (shorter than one second) that rise from 1·9 kHz to 2·6 kHz. Adult female three-toed sloths also use vocalizations to communicate with other conspecifics during the breeding season, presumably calling out to attract potential mates. Adult males involved in agnostic interactions have also been heard emitting short high-pitched calls.

Although three-toed sloths have poor visual acuity and visual discrimination, males possess some sexual ornamentation, such as the colorful specula with black central stripes on the Brown-throated Three-toed Sloth and the Pale-throated Three-toed Sloth, and the dark mane on the Maned Three-toed Sloth. It also seems possible that patches on the fur act in olfactory communication; specifically, black fur may act as a “boilerplate,” volatilizing pheromones for communication as has been observed in other species of mammals such as carnivores and ungulates.

Food and Feeding

All species of three-toed sloths are strict arboreal folivores. Individuals typically consume leaves from their modal trees where they spend most of their time. Consequently, diets of three-toed sloths vary geographically and include leaves from a variety of plant species from many families. While individual three-toed sloths can specialize on only a few species of trees, the population as a whole is a generalist. The diet of the Pale-throated Three-toed Sloth has been reported as almost exclusively containing leaves of dioecious species of Cecropia, but it has been observed consuming leaves from other tree species. The Brown-throated Three-toed Sloth selects leaves from species of Cecropia, but it also consumes leaves from more than 50 other species of trees.

The Maned Three-toed Sloth appears to be selective of the plants it consumes. Leaves from 21 species of Neotropical plants (16 species of trees and five lianas) were consumed—a small proportion of total trees available—with Micropholis venulosa (Sapotaceae), Mandevilla sp. (Apocynaceae, a liana), Ficus sp. (Moraceae), and Prunus sp. (Rosaceae) constituting the most important species. All three-toed sloths select and eat a disproportionate amount of young leaves, presumably because of their nutritional value.

Species of two-toed sloths and three-toed sloth are foregut-fermenting mammals, and three-toed sloths have one of the slowest rates of digestion and fermentation. The gut microbiota has been studied in Brown-throated Three-toed Sloths and appears to be a specialized community of microflora dominated by the bacterial phyla Proteobacteria and Firmicutes.

Breeding

All species of three-toed sloths have annual birth pulses in their reproductive cycles. They breed seasonally, and gestation is about six months long. Females give birth to one young over a six-month period that peaks in about late February. The neonate is dependent on its mother, clinging to her venter for 100 days or more. During this time, young consume leaves as early as two weeks old, but nursing continues until they are 2–4 months old. The relatively short time to independence for juvenile three-toed sloths enables females to breed in most years. Females have little variation in their reproductive output between years. In one field study, an average of 75% of adult females produced young each year. Juvenile survival can be high, but it decreases immediately following independence from the mother.

Most of what is known about the mating structure and strategies of three-toed sloths comes from a single site, a shade-grown agroecosystem in Costa Rica occupied by Brown-throated Three-toed Sloths. The mating structure there is strongly polygynous, with males excluding male competitors from their core home ranges and thereby obtaining a strong reproductive advantage. Most reproductively aged males did not sire offspring, with only 25% of resident adult males siring offspring. Notably, one male Brown-throated Three-toed Sloth sired more than 50% of all juveniles. Their sedentary lifestyle, small home ranges, and use of modal trees appears to facilitate polygyny because multiple females can persist in small patches of habitat and be monopolized by a single male. Females, however, use important strategies such as, most notably, switching mates among breeding seasons and shifting their home ranges during estrus.

Movements, Home range and Social organization

All species of sloths climb slow and deliberately and position themselves on the undersides of branches when moving. In a single day, an individual will move only 20–40 m. In general, daytime movements are longer than nighttime movements. Three-toed sloths are capable, however, of longer forays and have been observed moving hundreds of meters in less than a day. All three-toed sloths descend from trees to the forest floor about once a week to defecate.

Home range size for adult three-toed sloths is small, ranging from less than 1 ha to nearly 20 ha, and does not differ between the sexes or relative to breeding status. Home ranges of adult sloths often overlap each other, although adult males appear to maintain exclusive use of core areas in their home ranges. Home ranges of male three-toed sloths overlap with many females but not each other, and home ranges of adult females overlap each other.

Three-toed sloths are primarily solitary, although small groups can be observed. Occasionally, individual three-toed sloths are aggressive to conspecifics if they occupy the same tree. Three-toed sloths swim and can use rivers to disperse. Juveniles strongly select for forest cover during dispersal from their natal areas, and they avoid agricultural habitat types and often used forested riparian corridors to disperse.

Estimating densities of three-toed sloths is challenging because of their ability to conceal themselves within forest canopies. In general, densities of three-toed sloth range from 0·1 ind/ha to 8·5 ind/ha. These densities appear to be a function of habitat type, with three-toed sloths reaching their greatest density in intact native forest compared with other forests under various management practices.

Relationship with Humans

Sloths have been harvested by several indigenous groups across Central America and South America, although harvest rates generally appear to be low and infrequent. Some indigenous groups have taboos against eating sloths. Sloths (English), “perezoso” (Spanish), and “preguiça” (Portuguese)—all generally meaning “lazy”—have long been recognized for their apparent laziness, no doubt an oversimplification of their very slow movements. One of the earliest references comes from a Spanish knight (1526) who referred to sloths with an ironic moniker of “little quick Pedro” and described them as “the stupidest animal that can be seen in the world.” The famous French naturalist and philosopher Georges-Louis Leclerc, Comte de Buffon, observed that “one more defect and they could not have existed.” More recently, perceptions of sloths have changed dramatically. Three-toed sloths now engender strong feelings among the public and are even featured on currency (Costa Rica) and in merchandise, commercial advertising, and movies. They have also become one of the symbols of conservation activities in parts of Latin America.

Status and Conservation

The status of three-toed sloths differs by species. The Brown-throated Three-toed and the Pale-throated Three-toed Sloth are locally abundant and occur in many protected areas of various sizes. They also appear capable of reaching relatively high densities and, at least for the Brown-throated Three-toed Sloth, reasonably viable populations in agriculture landscapes provided that intact patches of forest and overhead canopy trees are maintained and connected by strips of forested areas along riparian areas.

The Maned Three-toed Sloth is classified as Vulnerable on The IUCN Red List. It is endemic to the Atlantic Forests of south-eastern Brazil and persists in three isolated subpopulations that are separated by forest clearings and deciduous forest encroachment, both of which act as a barrier to interactions among these populations. The relative isolation of each subpopulation is reflected by the genetic structure observed across the subpopulations and the relatively low levels of genetic variably within each subpopulation. Continued loss of suitable forest is a threat to the persistence of Maned Three-toed Sloth in its constrained distributional range. The Pygmy Three-toed Sloth has an extremely constrained distribution—only occurring on a small island on the Caribbean coast of Panama—and given its small size and isolation, it is classified as Critically Endangered on The IUCN Red List.

 

Bibliography

Anderson & Handley (2001), Beebe (1926), Britton (1941), Chiarello (1998b), Cliffe et al. (2014), Delsuc et al. (2004), Fountain et al. (2017), Garcés-Restrepo et al. (2017), Gardner (2008), Gibb et al. (2016), Goffart (1971), Greene (1989), Higginbotham et al. (2014), McNab (1978), Mendel (1985), Montgomery & Sunquist (1974, 1978), Moraes-Barros et al. (2011), Noss et al. (2008), Pauli & Peery (2012), Pauli, Carey & Peery (2017), Pauli, Mendoza et al. (2014), Pauli, Peery et al. (2016), Suutari et al. (2010), Voirin (2015), Waage & Best (1985), Waage & Montgomery (1976).