Mammalian Diversity And Matses Ethnomammalogy In Amazonian Peru Part 2: Xenarthra, Carnivora, Perissodactyla, Artiodactyla, And Sirenia Author Voss, Robert S. Author Fleck, David W. text Bulletin of the American Museum of Natural History 2017 2017-10-27 2017 417 1 1 http://www.bioone.org/doi/10.1206/00030090-417.1.1 journal article 10.1206/00030090-417.1.1 0003-0090 5407771 Choloepus hoffmanni Peters, 1858 VOUCHER MATERIAL (TOTAL = 10): Nuevo San Juan (AMNH 268225, 268226, 273184; MUSM 5072, 11077, 11079, 11080, 15346), Orosa (AMNH 73760, 73761). OTHER INTERFLUVIAL RECORDS 3 : Actiamë ( Amanzo, 2006 ), Choncó ( Amanzo, 2006 ), Estación Biológica Quebrada Blanco ( Heymann et al., 2011 ), Itia Tëbu ( Amanzo, 2006 ), Jenaro Herrera (Pavlinov, 1994), Río Yavarí-Mirím (Salovaara et al., 2003), San Pedro (Valqui, 1999). IDENTIFICATION: The genus Choloepus has received no modern revisionary attention. The current recognition of two valid species and the application of their names are largely based on diagnoses provided by Wetzel and Avila-Pires (1980) that were subsequently incorporated in dichotomous keys by Wetzel (1985a) and Gardner and Naples (2008) . According to these sources, C. didactylus (with type locality in Surinam ) is a widespread Amazonian species, whereas C. hoffmanni (with type locality in Costa Rica ) occurs in Central America, trans-Andean South America, and western Amazonia. Mapped 3 Unvouchered records of two-toed sloths are sometimes identified as “ Choloepus sp. ” (e.g., by Salovaara et al., 2003), but sometimes as C. didactylus (e.g., by Heymann et al., 2011 ). In the absence of evidence for the presence of a second species of Choloepus in the Yavarí-Ucayali interfluve, we assume that all of these sightings were of C. hoffmanni . TABLE 5 Diagnostic Cranial Traits of Choloepus didactylus and C. hoffmanni a

C. didactylus	C. hoffmanni
Preorbital osteology	maxilla contacts frontal	lacrimal contacts nasal
Posterior mesopterygoid foramenb	absent	present
Mesopterygoid ratio (AMB/PMB)c	>2.0	<2.0

a After Wetzel and Avila Pires (1980), Wetzel (1985a), and Gardner and Naples (2008) ; see illustrations in Wetzel (1985a). b Opening into pterygoid sinus (see text). c Ratio of anterior mesopterygoid breadth (AMB) to posterior mesopterygoid breadth (PMB). geographic ranges (in Wetzel, 1985a; Gardner and Naples, 2008 ) suggest that both species occur in northeastern Peru , so either C. didactylus or C. hoffmanni might occur in the Yavarí- Ucayali interfluve; alternatively, the two species might be sympatric in our region. According to the literature cited above, Choloepus didactylus and C. hoffmanni can be distinguished by several cranial characters ( table 5 ): (1) On the dorsal surface of the rostrum, just anterior to the orbit, either the maxillary bones contact the frontals, or the lacrimals contact the nasals; because most cranial sutures are fused in fully adult sloths, this is a character that can only be scored from immature specimens. (2) In the rear of the mesopterygoid (“interpterygoid”) fossa, a pair of large foramina—one on each side—that communicate with the pterygoid sinuses is either present or absent; unlike the preceding character, this feature can be scored from both immature and adult specimens. (3) The ratio between the anterior (widest) and posterior (narrowest) transverse dimensions of the mesopterygoid fossa is said to be taxonomically diagnostic. Additionally, pelage differences are said to distinguish C. didactylus from C. hoffmanni , but we experienced considerable difficulty in evaluating pelage traits, none of which appear to offer an unambiguous basis for character scoring, so we do not consider them further here. In order to evaluate the allegedly diagnostic cranial traits of Choloepus didactylus and C. hoffmanni , we examined series of specimens from regions where these species occur allopatrically (table 6). Of the three characters described above, only the presence/absence of posterior mesopterygoid foramina consistently distinguishes eastern Amazonian specimens ( C. didactylus ) from Central American material ( C. hoffmanni ). Although the mean difference in computed mesopterygoid ratios between these samples is obviously significant, the observed ranges overlap, so specimens cannot be sorted consistently by this criterion. Similarly, although most eastern Amazonian specimens exhibit maxillary-frontal contact, over 20% exhibit lacrimal-nasal contact (which appears to be a fixed trait in Central American material). Nevertheless, these results provide compelling evidence of phenotypic divergence, and they are consistent with the current recognition of two species of two-toed sloths, albeit with somewhat less distinct recognition criteria than suggested by the literature cited above. The ten voucher specimens we examined from the Yavarí-Ucayali interfluve are all referable to Choloepus hoffmanni as that species is currently recognized by these criteria. All the immature specimens (juveniles and subadults: AMNH 73761, 268225, 273184; MUSM 11077, 11080) exhibit lacrimal-nasal contact, and all the specimens that preserve an intact mesopterygoid region ( N = 9) have paired posterior foramina that open into the pterygoid sinuses. All of the four adults we measured ( table 7 ) have mesopterygoid ratios <2.0. Interestingly, almost all the two-toed sloths we examined from the north bank of the Amazon (directly opposite the Yavarí-Ucayali interfluve) are referable to Choloepus didactylus by the criteria discussed above, as are all the specimens TABLE 6 Morphological Trait Frequencies in Allopatric Populations of Choloepus didactylus and C. hoffmanni

Preorbital osteologyc			Posterior mesopterygoid foramenc
LN contacte	MF contact f	bothg	present	absent	bothg	Mesopterygoid ratiod
C. didactylus a	3 (23%)	9 (69%)	1 (8%)	29 (97%)	1 (3%)	2.09 ± 0.16 (1.85–2.50) 15
C. hoffmanni b	27 (100%)	53 (100%)	1.57 ± 0.19 (1.26–1.96) 25

a From the Guianas and southeastern Pará: AMNH 133405, 133410, 133414, 133416, 133417, 133427, 133439, 133444, 133446, 133447, 133449, 133452, 133453, 265952; BMNH 1904.7.4.94–1904.7.4.98, 1910.5.4.42, 1952.1175, 1952.1176; FMNH 21730, 34326, 34711, 41208, 93177, 95447–95450. b From Nicaragua, Costa Rica, and Panama: AMNH 2857/3780, 10274, 18895, 18896, 18897, 22703, 24441, 26900, 26901, 26905, 26907, 26908, 26912, 26913–26916, 26918–26922, 26925, 26934, 28475, 29440, 29608, 29643–29652, 29829, 30765, 131821–131823, 135331, 135332, 135490, 135524, 135925, 137280, 137281, 139772, 139773, 140333, 141856, 141857. c Table entries are numbers of specimens scored (percentage in parentheses). d Computed from adult measurements; table entries are the sample mean plus or minus one standard deviation, the observed range (in parentheses) and the sample size. Descriptive statistics for the C. hoffmanni sample excludes one outlier (AMNH 26915) with a mesopterygoid ratio of 2.59 (>5 standard deviations from the mean). e Bilateral lacrimal-nasal contact. f Bilateral maxillary-frontal contact. g Asymmetrical trait expression. we examined from eastern Ecuador . By contrast, both C. didactylus and C. hoffmanni occur south of the Amazon in Peru , but they occur at different localities. Therefore, although the ranges of these species overlap, we have yet to find any place where they are actually sympatric. Possibly they occur in different forest types , a hypothesis that merits testing in the field. ETHNOBIOLOGY: The principal name for the two-toed sloth is şhuinte, which is not analyzable or found in other Panoan languages. It has three archaic synonyms: nai, posën, and tabidiate. The first two are not analyzable but, unlike the principal term, they do occur as sloth names in other Panoan languages; the third term is a nominalization meaning “one for tying up its feet” (when the Matses bring a sloth back to the village alive, they tie their claws to their hand so that they cannot harm the person carrying it; this was the standard way of bringing back sloths during the komok ceremony, and is still done sometimes today). In the language used in the komok ceremony, the two-toed sloth is called uşhtud kudu; the first word seems to include the verb uşh ‘sleep’ (the Matses associate two-toed sloths with sleepiness and laziness) and the second term is an archaic adjective meaning “grayish” or “light-colored.” Four subtypes of two-toed sloth are recognized by Matses hunters: şhuinte uşhu (“white/light-colored two-toed sloth”), şhuinte piu (“red/reddishbrown two-toed sloth”), şhuinte poçhëşh (“black-/dark-bellied two-toed sloth”), and chompish. The last name is not analyzable, but it is also the name of a small bird that purportedly reveals the presence of two-toed sloths. Chompish and the other three subtypes seem to occupy different levels in the Matses classification, in the sense that chompish is considered more distinct from the other three types . This could be represented as follows: şhuinte şhuinte chompish şh. uşhu şh. piu şh. pokçhëşh The chompish variety is said to be much rarer than the others and to be the size of a young twotoed sloth, but to have head, claws, and teeth the TABLE 7 Measurements (mm) and Weights (g) of Adult Choloepus hoffmanni from the Yavarí-Ucayali Interfluve

AMNH 73760	MUSM 11079	MUSM 15346	AMNH 268226	MUSM 5072
Sex	female	female	female	male	unknown
Head-and-body length	—	650	647	614	—
Length of tail	—	28	18	27	—
Hind foot	—	148	155	144	—
Ear	—	28	22	27	—
Weight	—	—	7700	8100	—
Condylobasal length	—	118.6	121.2	120.2	126.2
Rostral breadth	40.8	39.3	37.0	43.1	39.1
Least interorbital breadth	34.9	37.6	35.6	39.2	40.1
Least postorbital breadth	40.0	41.1	35.9	41.9	39.9
Posterior zygomatic breadth	71.9	71.4	71.8	78.4	75.4
Maxillary toothrow	42.2	44.4	43.9	43.5	44.7
Mesopterygoid ratio	1.92	—	1.63	1.77	1.76

size of a full-grown adult. It has a short back, rostrum, and limbs. Its body is reddish, while its head is light colored. Informants never fail to mention that its meat is very hard and takes a long time to cook. The other three varieties are generally associated with different sizes and habitat preferences, but there is much inconsistency and even direct contradictions among informants. This is a primary game species that is much appreciated by the Matses. Informants emphasize that every part of the sloth is eaten, including its vulva, bladder, and viscera. This species, along with the greater long-nosed armadillo and the spectacled caiman, were the most important species to be hunted during the Matses komok ceremony. Two-toed sloths are considered very desirable and hardy pets. When a hunter kills a mother that is carrying its young, the hunter brings it home for his children to raise (fig. 11). Two-toed sloths are usually hunted by climbing trees and clubbing or strangling them. 4 A hunter may be tipped off as to the presence of two-toed sloth by hearing its urine drip from the treetops or by hearing the call of a bird called chompish (a type of flycatcher). Otherwise the hunter simply scans the canopy as he walks down a path. The sloth is typically curled up asleep in the crotch of a branch, in the crown of a bottle palm ( Iriartea deltoidea [ Arecaceae ]) or in a vine tangle. When he spots a sleeping sloth, the hunter makes a climbing ring (a loop of epiphyte stems or a palm frond, to loop between his feet as he shinnies up the trunk) and judges whether he can get within arm’s reach of the sloth. If he can get close to it, he cuts a hard stick to use as a club, climbs up next to the sloth, wakes it, and then clubs it on the head until it dies or falls out of the tree. Twotoed sloths are very resistant, and do not succumb quickly when they are clubbed. While the hunter is clubbing a sloth, it will become fierce and try to bite the hunter. If he cannot get close to it (for example, if it is in the crown of a bottle palm), he prepares a noose from epiphyte stems and attaches it to a stick 1.5 to 2 m long. He then climbs an adjacent tree, taps the sloth lightly with the stick (so that it wakes up and sticks out its head), snares it around the neck, and then pulls hard to yank it off its perch. Next, he throws down the sloth with the noose still attached. He may then club it to death on the ground or decide to take it back home alive. The latter option is preferred if the hunter is far from home, to keep the meat from spoiling. 4 Occasionally a hunter may shoot a sloth out of a tree with a shotgun, but this is uncommon since hunters prefer not to waste ammunition on game that can be taken by other means. FIG. 11. Matses girl with pet two-toed sloth on the upper Quebrada Chobayacu, ca. 1975 (photo by Steven Romanoff). There is a particular way to pack up a sloth for carrying it home. First, the hunter presses on its abdomen to make it defecate and urinate. Then, he breaks all of its limb bones with a club, ties the hind feet together, tucks the tied-up legs together, and lashes all in place to make a roughly spherical bundle. If the sloth is still alive, its front and back claws are tied tightly to its arms and feet, so that it cannot grab the carrier. Then a tumpline (a carrying strap worn across the forehead, made from the bark of certain trees) is attached to the sloth and the hunter carries it home on his back. Hunters typically leave hunting signs where they kill certain game, usually next to the path that is closest to the kill site. Sloth kills are marked with a meter-long stick jammed into the ground; a slot is cut in the top of the stick, and a tuft of the sloth’s fur is wedged in the slot. If the sloth was captured by noosing, the noose stick is jammed in the ground next to the stick with fur; if the sloth was captured by clubbing, the club and the climbing ring are placed next to the trophy stick. The Matses used to hang two-toed sloth mandibles on one the horizontal poles of their longhouses, as hunting trophies and to keep track of how many sloths had been killed at that locality. Today this is still done by a few old men. The Matses believe that a certain type of owl hoots at night near a Matses house to announce human visitors or the presence of game species, including two-toed sloths. After killing a sloth, a hunter may remove the sloth’s anal scent gland and rub it across his eyes. This is believed to improve his ability to find two-toed sloths in the future. A similar effect is thought to be achieved by burning a sloth forearm bone and letting the smoke enter one’s eyes. Children do not eat the jaw meat, lest their jaws swell up. Young men do not eat young sloths, lest they not wake up early. Young men do not eat the ball of fat that is found in the twotoed sloth’s abdominal cavity, lest they become unable to spot sloths. The hunter who killed the sloth does not eat the intestines, lest he not find more sloths. Young men and the hunter who killed the sloth do not eat the liver, lest they do not find more sloths. When a sloth is killed, the hunter’s children (or any other child that looks upon the dead sloth) may be made ill by the sloth’s spirit. The symptoms of contagion by sloths include oversleeping and fever. MATSES NATURAL HISTORY: Two-toed sloths are very hairy. They have no tail. They have sharp black teeth, small ears, and hairless noses. They have two long claws on their front feet and three on their hind feet. Their backs are lighter-colored than their undersides. Their meat is hard and takes a long time to cook. They have the most fat during the rainy season (December to April), especially in February. Two-toed sloths are found in any type of primary forest, including upland forest, and flooded or dry floodplain forest. They are also found in very old (>25 years old) abandoned swiddens. They are relatively common, especially in areas that have not been hunted. Two-toed sloths do not make nests. They sleep during the day in vine tangles, under the cover of large-leafed epiphytes, in crotches of trees high in the canopy, or in the crown of bottle palms ( Iriartea deltoidea [ Arecaceae ]). They sleep curled up, with their head tucked in. They usually perch high up to sleep, but they perch lower when they are at the edge of a river or when it is raining. The two-toed sloth is nocturnal. After sleeping all day, it wakes up at dusk and stays in its perch looking around until it is fully dark. It sets out traveling along the undersides of branches and horizontal lianas looking for leaves and fruits to eat. It avoids dead branches. It drinks water from holes in trees in the canopy, where frogs have laid eggs, or water trapped in palm-tree crowns. It also licks rainwater from leaves. It climbs down to the ground to drink water when there is none in the treetops. It also climbs down to the ground to eat clay that has been dug out by an armadillo, to eat rotten meat, and to defecate. It climbs back up quickly after having defecated, drunk water, or eaten clay or rotten meat. After eating a lot it stops to sleep for a while before setting out to forage again. Unlike three-toed sloths, two-toed sloths do not swim. Two-toed sloths are usually solitary but are sometimes found in male-female pairs perched near each other. They give birth to a single young, which clings to its mother’s venter. Two-toed sloths are followed by a small swarm of little black flies and sweat bees (tabanid flies that have black-and-yellow striped abdomens). A bird called chompish (a type of flycatcher) follows sloths (perhaps to feed on its flies?). Large eagles and hawks kill and eat twotoed sloths, even fully grown adults. Jaguars also occasionally kill them. Two-toed sloths do not make any noise while perched or while feeding. They huff when they are being killed or when they are defending themselves. Two-toed sloths eat the young leaves of almost any tree. They are particularly fond of the leaves of tote trees ( Eschweilera spp. , Lecythis spp. , or Cariniana spp. [ Lecythidaceae ]). Other favored foods are the ripe fruits and leaves of trees in the cacao ( Sterculiaceae ) family, particularly tonkodo ( Theobroma sp. ) and senad dëbiate ( Theobroma subincanum ). They eat the ripe fruits of a few other types of dicot trees, including mamuin ( Garcinia longifolia [Guttiferae]), which they eat after splitting open the rind; piuşh bëchi ( Helicostylis tomentosa [ Moraceae ]); tonnad (a general term for trees in the Myristicaceae ); and mannan tsipuis ( Inga spp. [Leguminosae]). They also eat the fruits of some epiphytes and the heart and young leaves of okodonte epiphytes ( Philodendron [ Araceae ]). They feed much more on leaves than on fruits, and they do not eat old/mature leaves. They descend to the ground to eat rotten meat. REMARKS: Matses interviews include many original observations about the behavior and diet of two-toed sloths, notably including their use of water sources in the canopy, geophagy, occasional carrion eating, food plants, and a possibly mutualistic interaction with an unidentified species of bird. To the extent that Matses observations overlap with previously published results of scientific research on Choloepus , there is good agreement (e.g., about nocturnality, reproduction, and predation), but one discrepancy merits comment. Two literature reviews—one about C. didactylus and the other about C. hoffmanni — both claim that two-toed sloths can swim ( Adam, 1999 ; Hayssen, 2011a ), but none of the refer- ences cited in either review explicitly report swimming behavior in these species. 5 Most mammals, of course, can swim when necessary, but the absence of any published observation of swimming by Choloepus spp. tends to support the Matses’ claim that two-toed sloths do not often do so, by contrast with three-toed sloths, which are frequently found swimming across rivers and lakes.