Bradypus variegatus Schinz, 1825

Voss, Robert S. & Fleck, David W., 2017, Mammalian Diversity And Matses Ethnomammalogy In Amazonian Peru Part 2: Xenarthra, Carnivora, Perissodactyla, Artiodactyla, And Sirenia, Bulletin of the American Museum of Natural History 2017 (417), pp. 1-1 : 1-

Bradypus variegatus Schinz, 1825

Figures 7–9

VOUCHER MATERIAL (TOTAL = 4): Nuevo San Juan (MUSM 11075, 23811), Orosa (AMNH 73758, 73759).

OTHER INTERFLUVIAL RECORDS: Actiamë ( Amanzo, 2006), Jenaro Herrera (Pavlinov, 1994), Río Yavarí-Mirím (Salovaara et al., 2003), San Pedro (Valqui, 1999).

IDENTIFICATION: Four living species of bradypodid sloths are currently recognized, of which one ( B. pygmaeus Anderson and Handley, 2001 ) is an insular endemic, another ( B. tridactylus Linnaeus, 1758 ) is restricted to northeastern Amazonia (east of the Rio Negro and north of the lower Amazon), a third ( B. torquatus Illiger, 1811 ) is endemic to the Atlantic forest of southeastern Brazil, and the fourth ( B. variegatus ) is thought to range throughout most of Central America and tropical South America ( Anderson and Handley, 2001; Gardner, 2008).

Although Bradypus variegatus (the “brownthroated three-toed sloth” of English usage) and B. tridactylus (the “pale-throated three-toed sloth”) are the only currently recognized species of Amazonian bradypodids (Wetzel, 1985a; Anderson and Handley, 2001; Gardner, 2008), Amazonian threetoed sloths have received no modern revisionary attention, and there is little compelling evidence to support current taxonomic usage. In particular, the extensive distribution of B. variegatus (from Hon- duras to northern Argentina), substantial geographic variation in morphology (see below), and preliminary genetic evidence from gene-sequencing studies (e.g., Moraes-Barros and Arteaga, 2015; Ruiz-García et al., 2017) all suggest that brownthroated three-toed sloths include several distinct taxa. Seven South American subspecies of B. variegatus were recognized by Gardner (2008), but no explicit justification for sloth trinomial nomenclature has yet been provided by any author.

The type locality of Bradypus variegatus is assumed to be somewhere in the Atlantic Forest of southeastern Brazil (Wetzel and Kock, 1973), and specimens that are morphologically similar to Atlantic Forest material have been collected throughout southeastern Amazonia, from the vicinity of Belém westward to the left (west) bank of the Tapajos. Sequence data analyzed by Moraes-Barros and Arteaga (2015) and Ruiz- García et al. (2017) likewise suggest that southeastern Amazonian and Atlantic Forest populations of brown-throated three-toed sloths are closely related. Additionally, photographs of the holotype skull (SMF 4313; available online from the Senkenberg Naturmuseum database) closely match the craniodental morphology of southeastern Amazonian specimens that we examined. In the paragraphs that follow, we assume that southeastern Amazonian three-toed sloths represent the nominotypical form, B. variegatus variegatus .

Three-toed sloths from the Yavarí-Ucayali interfluve and others that we examined from western Amazonia fit the description of Bradypus variegatus in the inclusive sense that this binomen is currently applied (e.g., by Wetzel and Avila-Pires, 1980; Wetzel, 1985a; Anderson and Handley, 2001; Gardner, 2008). Traits that support the identification of western Amazonian three-toed sloths as belonging to the B. variegatus complex include (1) the presence of a speculum in adult males (a speculum is absent in B. torquatus ); (2) absence of a mane of long black hair (present in B. torquatus ); (3) the consistently brownish coloration of the throat (the gular fur is whitish or yellowish in B. tridactylus ); (4) the absence of large foramina in

the anterior part of the mesopterygoid fossa (present in B. tridactylus and B. torquatus ); and (5) large size ( B. pygmaeus is much smaller). However, other phenotypic characters distinguish western Amazonian material from southeastern Amazonian specimens of B. variegatus .

In western Amazonian specimens of brownthroated three-toed sloths, the anteriormost maxillary teeth (the “pseudo-incisors” of Thomas, 1917) are large and procumbent; the rostrum is correspondingly broad; the nasal bones are short, often exposing the nasal orifice and the projecting pseudoincisors in dorsal view; and the postorbital process of the jugal is well developed (figs. 7A, 7B, 8A). The co-ossified mandibles are likewise distinctive, entirely lacking any trace of the median anterior process (symphysial spout) seen in other sloths, but with a deep symphysis that often extends posteriorly between the third pair of teeth (fig. 9A). By contrast, the pseudoincisors of southeastern Amazonian specimens are much smaller and nonprocumbent; the rostrum is narrower; longer nasal bones conceal the nasal orifice from dorsal view but extend the orifice such that it is visible from below; and a postorbital process of the jugal is absent or indistinct in most examined specimens (figs. 7C, 7D, 8B). Additionally, the mandibles of all examined specimens from southeastern Amazonia have a small but distinct symphysial spout, and the symphysis only extends posteriorly between or just beyond the second pair of teeth (fig. 9B). On average, skulls from western Amazonia are substantially larger than those from southeastern Amazonian in all measured dimensions ( table 4 ), but most measurements exhibit overlapping variation; an exception is rostral breadth, which is diagnostically greater in western Amazonian material than in specimens from southeastern Amazonia. We have not been able to discover any pelage or other external differences between three-toed sloths from western and southeastern Amazonia, which both seem to be highly variable (e.g., in pelage coloration).

Western Amazonian three-toed sloths are usually associated with the epithet infuscatus (e.g., by Thomas, 1928; Gardner, 2008), a convention that we follow despite misgivings about the application of this name. According to Wagler (1831: 611), Bradypus infuscatus was based on a single specimen collected by “Herr von Spix” (= Johann Baptist Ritter von Spix) on the border between Brazil and Peru (“Brasilia versus Peru ”). Based on Spix’s known itinerary (Vanzolini, 1981; Hershkovitz, 1987), it seems reasonably certain that the holotype (by monotypy, a specimen in the Zoologische Staatssammlung München, ZSM 1162; Wetzel and Kock, 1973) was collected at or near Tabatinga, on the left (north) bank of the upper Amazon, just across the river from Peru and the mouth of the Yavarí (fig. 1). 2 We have not examined this specimen, which consists only of a mounted skin (A. van Heteren, personal commun., 2016); the skull was said to be missing in the original description (Wagler, 1831) and has not been recovered.

Based on the geographic distribution of examined material with the morphological traits described above, it is plausible that B. v. infuscatus is the proper trinomen for this form, but without confirmatory evidence (e.g., DNA sequence data obtained from the holotype skin) it is hard to be sure. Possible junior synonyms include brachydactylus Wagner, 1855; macrodon Thomas, 1917; codajazensis Lönnberg, 1942; and subjuruanus Lönnberg, 1942 (for type localities, see Gardner, 2008). Of these nominal taxa, we have only examined the holotype of macrodon (BMNH 80.5.6.56), which exhibits all the diagnostic craniodental traits of the western Amazonian phenotype as described above.

Given the distinct morphologies associated with western Amazonian specimens on the one hand and southeastern Amazonian specimens on the other, we would be inclined to call these distinct species. However, we are provisionally using trinomial nomenclature because there are intermediate phenotypes, suggestive of intergradation, in central Amazonia. Based on specimens we examined with the morphological distinctions described and illustrated above, Bradypus variegatus variegatus occurs along the right (south) bank of the Amazon from the vicinity of Belém westward to the left (west) bank of the Tapajós, whereas B. v. infuscatus occurs in eastern Ecuador, eastern Peru, and southern Venezuela (fig. 10). Only a few specimens are available from the wide (ca. 1300 km) central-Amazonian gap between these morphologically diagnosed taxa, but those we examined are difficult to assign with certainty to either form. For example, three BMNH specimens from Codajás (on the north bank of the upper Amazon west of Manaus; fig. 10: locality 8a) have small pseudoincisors, long nasals, narrow rostrums, and short mandibular symphyses (like B. v. variegatus ), but they have well-developed postorbital jugal processes and lack symphyseal spouts (like B. v. infuscatus ). Pending a much-needed revision of the brownthroated three-toed sloth complex, trinomial nomenclature seems like the appropriately conservative option.

ETHNOBIOLOGY: The three-toed sloth has only one name, mëinkançhuşh. It is not analyzable and there are no cognates in other Panoan languages. No subtypes are recognized by the Matses. The Matses do not hunt three-toed sloths, eat them, or keep them as pets. The Matses generally will not even look directly at them, because if a hunter looks at a three-toed sloth it can make his children ill. Therefore, the Matses know very little about the natural history of this species.

MATSES NATURAL HISTORY: The three-toed sloth is similar to the two-toed sloth, but it has three claws on its front feet, a short tail, a smaller head, a striped face, and a spotted back. Its face looks like that of a little person.

Three-toed sloths are found mostly beside rivers in stands of cecropia trees (Cecropia spp. [ Moraceae ]). They are rarely encountered in Matses territory (where large stands of cecropia trees are absent).

It makes no nest. It is nocturnal and diurnal. It swims slowly but effectively across rivers. It climbs along lianas and branches upside-down. It sits in thickets. It is solitary. It eats mostly cecropia tree leaves and also eats fig-tree ( Ficus sp. [ Moraceae ]) fruits.

REMARKS: The Matses do not have a lot to say about three-toed sloths—doubtless because this species is seldom seen and never hunted for food—and their few observations seem intended primarily to distinguish this species from the superficially similar two-toed sloth (a primary game species). This intent is explicit in the comparative phrasing of their morphological descriptions, but diagnostic comparisons are also implied by their remarks that three-toed sloths are both nocturnal and diurnal (two-toed sloths are exclusively nocturnal), and that three-toed sloths swim (whereas two-toed sloths do not, at least according to the Matses; see below).

The widespread notion that three-toed sloths have a close relationship with trees of the genus Cecropia has been called a myth by Montgomery (1983), who averred that Bradypus are simply easier to see in the relatively open, sunlit crowns of cecropia trees than in the denser crowns of other tree species. However, it should be noted that Montgomery’s research on sloths (e.g., Montgomery and Sunquist, 1978) was carried out on an island with very little early-successional vegetation (the preferred seral stage of Cecropia spp.), where an essentially captive population of sloths may have had no choice but to forage in habitats that would have been avoided by unconstrained animals. Subsequent studies from mainland habitats seem to agree with earlier reports that young cecropia leaves are a preferred forage for Bradypus , perhaps due to their low fiber content, high nutrient value, and lack of defensive secondary compounds (Urbani and Bosque, 2007). Therefore, the Matses observation that riparian stands of cecropia trees are the primary habitat of threetoed sloths merits credibility despite Montgomery’s (1983) dismissal of essentially similar observations in the older literature.

Figures

FIG. 7. Dorsal and ventral cranial views of Bradypus variegatus infuscatus (A, B, AMNH 76497) and B. v. variegatus (C, D, AMNH 95105). Both skulls lack the premaxillae, which are only loosely attached in bradypodid sloths and are often lost in specimen preparation. Cranial sutures are fused in AMNH 76497, whereas most sutures persist in AMNH 95105 (a younger adult); the conspicuous shape differences between these specimens, however, are not age dependent.

FIG. 8. Lateral views of skulls and mandibles of Bradypus variegatus infuscatus (A, AMNH 76497) and B. v. variegatus (B, AMNH 95105).

FIG. 9. Dorsal views of mandibles of Bradypus variegatus infuscatus (A, AMNH 76497) and B. v. variegatus (B, AMNH 95105).

Tables

TABLE 4 Craniodental Measurements (mm) of Three-toed Sloths (Bradypus variegatus ssp.)

	B. v. infuscatus a	B. v. variegatus b
Condyloalveolar length	74.3 ± 3.1 (69.6–80.9) 24	66.8 ± 2.4 (61.3–71.5) 25
Rostral breadth	21.1 ± 1.3 (18.6–25.1) 24	16.5 ± 0.8 (14.7–17.9) 26
Least interorbital breadth	23.8 ± 1.0 (21.8–25.6) 24	21.6 ± 1.7 (18.0–24.9) 25
Least postorbital breadth	24.3 ± 1.8 (21.1–28.6) 24	21.8 ± 1.6 (18.0–24.9) 26
Anterior zygomatic breadth	48.7 ± 2.0 (44.9–53.3) 19	42.6 ± 2.1 (37.0–46.3) 25
Posterior zygomatic breadth	48.2 ± 2.5 (43.0–54.9) 24	42.8 ± 2.1 (38.5–46.7) 26
Maxillary toothrow	26.8 ± 1.1 (25.1–29.1) 24	23.8 ± 0.9 (22.7–25.7) 26
Greatest diameter of pseudoincisor	4.0 ± 0.4 (3.2–5.0) 24	2.5 ± 0.4 (1.9–3.4) 24

Craniodental Measurements (mm) of Three-toed Sloths ( Bradypus variegatus ssp.)

a The mean plus or minus one standard deviation, the observed range (in parentheses), and the sample size for measurements of the following series from western Amazonia: AMNH 71822, 73572, 73574, 73758, 73759, 74429, 76408, 76495, 76497, 78515, 188196; BMNH 80.5.6.56, 80.5.6.58; FMNH 20132, 70812, 86896; LSUMZ 12304; MUSM 8301, 8302, 11075, 33610; MVZ 155186, 157796, 157797.

b The mean plus or minus one standard deviation, the observed range (in parentheses), and the sample size for measurements

of the following series from southeastern Amazonia: AMNH 75140, 95101, 95102, 95104–95106, 95325, 95326, 95328, 96244– 96246, 96250, 96252, 96253, 96255, 133415, 133419, 133426, 133432, 133438; BMNH 4.7.4.92, 4.7.4.110, 4.7.4.111; FMNH 92079, 94551.