Ateles belzebuth (E. Geoffroy, 1806)

Voss, Robert S. & Fleck, David W., 2011, Mammalian Diversity And Matses Ethnomammalogy In Amazonian Peru Part 1: Primates, Bulletin of the American Museum of Natural History 2011 (351), pp. 1-81 : 18-22

Ateles belzebuth (E. Geoffroy, 1806)

VOUCHER MATERIAL (TOTAL 5 12): Nuevo San Juan (MUSM 11109, 11110), Orosa (AMNH 74027–74031), Boca Río Yaquerana (FMNH 88839–88843).

UNVOUCHERED OBSERVATIONS: Actiamë ( Amanzo, 2006), Choncó ( Amanzo, 2006), Divisor ( Jorge and Velazco, 2006), Itia Tëbu ( Amanzo, 2006), Reserva Comunal Tamshiyacu-Tahuayo ( Puertas and Bodmer, 1993; Heymann and Aquino, 1994), Río Orosa ( Freese et al., 1982), Río Yavarí (left bank below Angamos; Salovaara et al., 2003), Río Yavarí-Mirím ( Salovaara et al., 2003), Tapiche ( Jorge and Velazco, 2006). (Note that previous reports of spider monkeys from the Yavarí- Ucayali interfluve identified the local species as either Ateles chamek or A. paniscus for reasons explained below.)

IDENTIFICATION: Kellogg and Goldman’s (1944) revision of the spider monkeys recognized four polytypic species, of which two ( Ateles fusciceps , A. geoffroyi ) were trans- Andean endemics, one ( A. paniscus ) was restricted to Amazonia, and another ( A. belzebuth ) included both trans-Andean and Amazonian subspecies. Although Kellogg and Goldman’s revision was largely based on pelage traits that some researchers (e.g., Hernández-Camacho and Cooper, 1976) have interpreted as infraspecific geographic variation, recent studies based on other kinds of data (reviewed by Collins, 2008) support the recognition of several valid species. The following paragraphs summarize the empirical basis for recognizing distinct species in Amazonia.

Amazonian spider monkeys consist of four allopatric nominal taxa, variously recognized as valid species or subspecies by modern authors: paniscus Linnaeus, 1758 , which occurs north of the Amazon and east of the Rio Negro/Rio Branco; belzebuth E. Geoffroy, 1806 , which occurs north of the Amazon and west of the Negro/Branco; chamek Humboldt, 1812 , which occurs south of the Amazon and west of the Tapajos; and marginatus E. Geoffroy, 1809, which occurs south of the Amazon and east of the Tapajos. Kellogg and Goldman (1944) recognized chamek as a subspecies of Ateles paniscus , and marginatus as a subspecies of A. belzebuth , but subsequent analyses of allozymic, cytogenetic, morphometric, and sequence datasets provide compelling evidence that paniscus (sensu stricto) is a distinct species, and that chamek is more closely related to belzebuth and marginatus. Although skins of belzebuth (with buffy or whitish underparts) and marginatus (with whitish facial markings) are easily distinguished from those of chamek (which are almost completely black; see below), these three taxa are craniometrically similar ( Froehlich et al., 1991), have the same diploid number of chromosomes ( Medeiros et al., 1997; Nieves et al., 2005), and have been recovered as a clade in phylogenetic analyses of mitochondrial sequence data ( Collins and Dubach, 2000; Collins, 2008). Because molecular analyses that have includ- ed representative samples of belzebuth , chamek , and marginatus suggest that these coat- color phenotypes are not reciprocally monophyletic ( Collins, 2008: fig. 3.3), and in the absence of any other morphological traits known to be correlated with coat-color differences in this complex, we see no justification for recognizing chamek and marginatus as distinct species (contra Groves, 2001, 2005).

b Summary statistics (mean, observed range in parentheses, and sample size) for measurements of AMNH 74029–74031; FMNH 88839–88841; MUSM 11109, 11110.

Although some museum skins of spider monkeys from the Yavarí-Ucayali interfluve are completely black (consistent with most published descriptions of the chamek phenotype; e.g., Kellogg and Goldman, 1944; Emmons, 1997), patches of blond or buffy hairs are present along the inner thighs of other specimens (e.g., AMNH 74029, 74031), and the exposed skin of the nose and the central part of the face of large adults is often unpigmented (reddish in life, according to the Matses; see below). Cranial measurements of our material (table 3) fall within the range of variation in homologous dimensions of western Brazilian, northeastern Bolivian, and eastern Peruvian specimens previously reported by Kellogg and Goldman (1944 [as Ateles paniscus chamek ]) and Lönnberg (1940a [as A. ater peruviensis ]). Most specimens are unaccompanied by weight data, but

an adult female from Nuevo San Juan (MUSM 11109) weighed 7400 g.

ETHNOBIOLOGY: The spider monkey is called çhëşhëid, a term that the Matses analyze as meaning ‘‘black one’’ (probably a valid etymology). The spider monkey is also called by the archaic synonyms mëshe (not analyzable, but apparently containing the prefix më- for ‘‘hand’’) and çhuna wisu (5 ‘‘black çhuna’’; çhuna is one of the archaic names of the woolly monkey). In the language used in the Matses’ komok ceremony, spider and woolly monkeys are called şhëmën kudu (these are the only primates to have a name in the ceremonial language). All Matses hunters recognize two varieties of spider monkey, which are said to never occur in the same troop. One is called chëshëidtapa (‘‘big spider monkey’’), and the other variety is simply called tsidu, a word that is not analyzable and is only used to refer to this variety of spider monkey. The larger spider monkey subtype has a red nose and central part of its face, and is the ‘‘normal’’ or prototypical type of spider monkey. The tsidu spider monkey is much smaller, skinnier, has an all-black face, has less or no yellow hair on its inner thighs, has a higher-pitched call, lives in much smaller troops, is less common, and is found mostly in deep rainforest very far from rivers. Some tsidu spider monkeys are believed to be demons instead of real animals, and can cause hunters to miss them repeatedly, or, if killed, can make hunters get lost on the way back home. If a tsidu spider monkey makes a hunter get lost, he must dump the dead monkey, and only then will he find his way back home.

The principal economic importance of spider monkeys for the Matses is as food. Spider monkeys and woolly monkeys are the preferred primate game of the Matses. As with sloths and other large monkeys, the arm and leg bones of spider monkeys are broken (to tenderize the meat) before the carcass is bound with plaited palm leaves into a basketlike package, to which a tumpline made of a strip of bark is then attached for carrying. The normal way to cook large monkeys ($ ca. 2 kg) is to singe the hair off, remove the viscera, cut off the appendages, and boil them in a big pot. Large monkeys are also smoked when much game is killed, or on long (multiple-day) hunting trips. The canines are sometimes used to make necklaces, although the larger teeth of other atelid species are preferred. Young spider monkeys make good pets, but captive-raised animals can become aggressive when they reach adulthood. The Matses believe that hunters cannot eat or touch the intestines of spider monkeys (and other primate game species), lest they lose their marksmanship.

One way that the Matses hunt monkeys (and ungulates) is by walking quickly along forest paths listening for calls and rustling branches; smelling the air; and looking for eaten food, spoor, and other signs of game. How the Matses hunt spider monkeys depends on how wary the local animals are, which in turn depends on how much previous experience a troop has had with hunters. As he walks, every so often a hunter will alternately imitate the calls of spider monkeys, woolly monkeys, and capuchin monkeys, hoping that one species or another will come or at least respond by calling back. If a spider monkey troop that is not wary hears the imitations, the monkeys will respond and come to the hunter. Troops that have had no experience with people will shake branches above the hunter, bark, defecate, urinate and throw branches down at him (which they also do when they see jaguars and anteaters). Or they may simply all come and stare at the person from above. Spider monkeys that are a bit wary will come, but once the large male that leads the troop sees the hunter, it screams and all the monkeys turn around and flee. Troops that are somewhat more wary will respond vocally to the hunter’s call but without approaching him, in which case the hunter seeks the monkeys in the direction from which they responded. Troops that are a bit more wary will not respond to loud imitations, so the hunter must call softly and cannot detect wary monkeys that are far away. Very wary troops simply do not respond, and the wariest will hide or move quietly and quickly in the opposite direction when they hear the hunter’s call. If no spider monkeys respond, the hunter may try a brown capuchin monkey call, which may make spider (or other) monkeys vocalize, thinking that capuchins have found fruits. The closer to the village a hunter is, the more wary the spider monkeys are likely to be, so as a hunter travels away from the village at first he only listens; then further out he makes lowvolume spider monkey calls and/or capuchin monkey calls; and then further out calls spider monkeys at full volume. The hunter may simply imitate spider monkeys (and woolly monkeys) while walking to check if they might answer. Or he may be motivated to try the imitation upon finding dropped halfeaten fruits. Or if he comes across a sleeping tree early in the morning, he may call. When he is ready to turn back to the village, a hunter will make loud spider-, woolly-, and capuchin-monkey calls and listen for a while. In addition to listening and imitating calls, hunters also go to mineral licks (where there may be other game) to kill spider monkeys.

Ideally, the hunter sees the monkeys before they see him. If the troop comes toward the hunter after hearing his imitation (they can be heard approaching because they scream and make noise as they swing through the treetops), then the hunter hides and shoots them when they arrive. If they answer but do not come, the hunter must stalk them. If the hunter is able to catch them by surprise, he shoots the biggest one he can get a clear shot at, and chases a second one after the rest run off. When spider monkeys flee from a hunter, they split up and go in different directions (rather than fleeing all together, as uakari monkeys do). They move through the trees extremely quickly so that the hunter must run at full speed, and try get ahead of one and shoot it as it passes overhead, or he must keep up with one until it tires out. Because females that are carrying young go the slowest, they are the most easily killed. A hunter hunting alone generally kills only one or two spider monkeys from a troop.

The Matses traditionally hunted spider monkeys with bows and arrows, but now they hunt them almost exclusively with shotguns (in some villages bows and arrows are still used when there is no ammunition). Spider monkeys are hard for archers to kill because a shot monkey will pull out the arrow and keep running, dripping blood along the way. If the monkey dies without falling to the ground, the hunter must climb into the canopy to recover the carcass. If a spider monkey falls injured to the forest floor, it will try to bite any person or dog that approaches it.

MATSES NATURAL HISTORY: Spider monkeys have very long limbs and tails. They hold their tails stretched out, unlike woolly and capuchin monkeys, which coil up their tails as they travel. They use their tails to grab onto things, and when they travel swinging under the branches, they use their tail as an additional limb. They hang by their tails when they eat fruit, sometimes all spread out with limbs and tail grabbing onto separate branches. Their hands have only four fingers—that is why a fork is called ‘‘spider monkey’s hand’’ [a recently coined term]. In contrast to their limbs, their heads are small. Their heads have little meat to eat on them, unlike woolly monkeys’. The spider monkey’s head hair looks like it was combed forward from the back; this along with its red nose makes it look silly as it sits there scratching its small head. Adult males are larger than females and have more yellow hair on their inner thighs.

Spider monkeys are found in all primary forest habitats, but more often in upland forest than in floodplain forest. Spider monkeys mostly use the middle of the canopy, but often climb higher to forage, escape predators, and sleep. When they hear a tinamou fly, they climb up higher. They do not walk around or forage on the ground, unlike white-fronted capuchin monkeys, except when they go to mineral licks [see below].

Spider monkeys are more common than woolly monkeys. Troop size varies from one to very many [some narrators say up to 40], but 10 to 20 is more usual. A large male leads the troop. Females carry their young on their backs, unless the young are very small, in which case they carry them ventrally. Spider monkeys suckle their young in the same way that people do. Harpy eagles take the smaller animals, and jaguars and pumas may attack them at mineral licks. Spider monkeys defend themselves by grabbing and biting.

Spider monkeys have several different vocalizations. They scream very loudly to communicate over long distances saying ‘‘ eeeeEEee, eeeeEEee ’’; they bark like a dog when they are mad saying ‘‘ aik, aik, aik ’’; they communicate among themselves with soft vocalizations, saying ‘‘ oh, oh, oh ’’; and they scream like people when they are shot. They make a lot of noise rustling branches as they move across the treetops.

When there is good weather, spider monkeys wake up early. When it is rainy, they get up later. They wake up calling loudly, calling their companions who are sleeping nearby, usually in the same tree. Once they are all together, they go in search of food. They travel through the trees screaming. They follow a daily route, traveling far in one day, but do not advance very fast [some say they complete their route in one day, others say it takes them 2–3 days, others say they simply use the same general area with no set route]. When in flight, they travel faster than any other monkey. Large males go the fastest, and females carrying young go slower. They travel swinging under the branches using their arms and tails, except when there are no small branches, in which case they run across the tops of large branches. They are most active in the morning, and they rest when the sun is high and hot. They rest lying on branches, while their young play. In the afternoon they are active again, but not as much as in the morning. When it rains, they sit in sheltered places such as under a tangle of vines or under large-leafed epiphytes.

They sleep in the same big tree every night [some speakers say it is only at one locality, others say there are two or three trees on their route where they sleep]. They sleep very high up, splitting into small groups that huddle together. They defecate and urinate where they sleep. Where they sleep, there are a lot of feces and defecated seeds on the ground. Especially common are the seeds of the isan palm [ Oenocarpus bataua ]. These seeds can be found sprouting under their sleeping trees. Sleeping sites stink very badly, and the Matses can smell them from far away. Spider monkeys come out and yell at night when there is a full moon.

Spider monkeys go to muddy mineral licks to eat mud and drink muddy water. They always go to the same mineral lick. Although the troop may split up to forage and eat fruits, they go to the mineral licks together as a group. At the mineral lick, some drink the muddy water while others stay up in the trees nearby watching for jaguars and people. Then they switch places. They make a hole in the walls of the mineral lick, like a cave, where they always collect mud. They drink from the mineral lick with their tails wrapped around trees. They descend and ascend via thin trees next to the mineral lick, and these trees are always covered with mud. After climbing back to the trees after drinking from the mineral lick, they sit there a while scratching their heads and eating their lice.

Spider monkeys eat mostly fruits. Large troops may split up to forage. When one spider monkey finds fruits, it starts eating, and then the others come to join it. The one that comes first finishes eating first and rests while waiting for the others to finish. Unlike other monkeys, they eat fruits without peeling them, swallowing even isan palm seeds and other large seeds [up to about the size of an acorn]. They eat palm fruits, especially isan palm fruits [which ripen during the early rainy season] and swamppalm [ Mauritia flexuosa ] fruits, which ripen during the dry season]. They also drink the liquid or eat the soft endosperm of unripe niste palm [ Iriartea deltoidea ] fruits. They also eat a lot of dicot tree and vine fruits, especially këku [ Couma macrocarpa (Apocynaceae) ], şhankuin [ Pourouma spp. (Moraceae) ], dadain [ Clarisia racemosa (Moraceae) ], tonnad [species of Myristicaceae ], moste [ Hymenaea spp. (Leguminosae) ] and chiwish [ Ficus and Coussapoa spp. (Moraceae) ], which are available during the rainy season. Other dicot tree fruits they eat include: wesnid debiate [ Anacardium giganteum (Anacardiaceae) ], machishte [ Rhigospira quadrangularis and? Mucoa duckei (Apocynaceae) ], diden këku [ Parahancornia peruviana (Apocynaceae) ], ichibin [ Matisia sp. , Eriotheca sp. (Bombacaceae) ], mamuin [ Rheedia longifolia (Guttiferae], okodo mabis [an undetermined species of Guttiferae], mannan tsipuis [ Inga spp. and? Pithecellobium (Leguminosae) ], tankada [ Parkia igneiflora , P. multijuga , and Pithecellobium auriculatum (Leguminosae) ], bin [ Castilla (Moraceae) ], şhanned [? Brosimum (Moraceae) ], piuşh bëchi [ Helicostylis tomentosa and H. elegans (Moraceae) ], kuşhu tëbin [ Naucleopsis mello-barretoi and N. ternstroemiiflora (Moraceae) ], bata [ Pseudolmedia and Maquira spp. (Moraceae) ], mabis mabiskid [ Chrysophyllum prieurii (Sapotaceae) ], and kose [ Manilkara bidentata (Sapotaceae) ].