Alouatta seniculus (Linnaeus, 1766)

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 : 14-17

Alouatta seniculus (Linnaeus, 1766)

VOUCHER MATERIAL (TOTAL 5 3): Marupa (AMNH 98321, 98610), Nuevo San Juan (MUSM 11108).

UNVOUCHERED OBSERVATIONS: Actiamë ( Amanzo, 2006), Choncó ( Amanzo, 2006), Reserva Comunal Tamshiyacu-Tahuayo ( Puertas and Bodmer, 1993; Heymann and Aquino, 1994), Río Orosa ( Freese et al., 1982), Río Tapiche ( Bennett et al., 2001), Río Yavarí (left bank below Angamos; Salovaara et al., 2003), Río Yavarí-Mirím ( Salovaara et al., 2003), Tapiche ( Jorge and Velazco, 2006).

IDENTIFICATION: Morphological revisions of howler monkeys have recognized as few as six valid species ( Hill, 1962), but as many as 14 might be recognized on the basis of coatcolor phenotypes ( Groves, 2001; Gregorin, 2006). Cytogenetic and molecular research provides compelling support for some, but not all, of the species recognized in the recent taxonomic literature and underscores our still incomplete understanding of this geographically widespread genus. In the absence of any published synthesis of phenotypic and genetic data, the following remarks summarize the emerging taxonomic consensus, suggest where future research could usefully be focused, and explain our preferred binomen for the red howlers of the Yavarí- Ucayali interfluve.

Phylogenetic analyses of mitochondrial DNA sequence data ( Cortés-Ortiz et al., 2003) support the recognition of just two trans-Andean howler species: Alouatta palliata (Gray, 1849) , the mantled howler of Mesoamerica and northwestern South America, and A. pigra Lawrence, 1933 , the black howler of Guatemala and southeastern Mexico. 4 The distinctness of these species, which was first clearly indicated by conspicuous cranial and pelage differences that are maintained in sympatry ( Smith, 1970), is additionally supported by karyotypic data ( Steinberg et al., 2008) and by patterns of allelic variation at eight microsatellite loci ( Ellsworth and Hoelzer, 2006). By contrast, the nominal taxon coibensis Thomas, 1902 (from the Azuero Peninsula and Coiba Island, Panama), which was recognized as a valid species by Groves (2001, 2005), seems to be genetically indistinguishable from A. palliata (see Cortés- Ortiz et al., 2003).

The reciprocal monophyly of several morphologically distinctive cis-Andean species or species complexes is likewise support- ed by mitochondrial sequence data (Cortés- Ortiz et al., 2003), including: (1) the brownish howlers of the Atlantic Forest, for which the oldest available name is Alouatta fusca (E. Geoffroy, 1812; see Gregorin, 2006); (2) the sexually dichromatic howlers of eastern Bolivia, central Brazil, Paraguay, and northern Argentina, for which the oldest available name is A. caraya (Humboldt, 1812) ; (3) the red-handed howlers of southeastern Amazonia, for which the oldest available name is A. belzebul (Linnaeus, 1766) ; and (4) the reddish howlers of northern Colombia, Venezuela, the Guiana Region, and western Amazonia, for which the oldest available name is A. seniculus . The latter complex is the one represented in the Yavarí-Ucayali interfluve.

In addition to their reddish coloration, members of the Alouatta seniculus complex are uniquely distinguished from other simiiform primates by the presence of microchromosomes in all published karyotypic preparations ( Consigliere et al., 1996; Sampaio et

al., 1996). 5 Eight nominal taxa of red howlers referable to the seniculus complex have been regarded as valid by recent authors ( table 1 ). Although subtle differences in pelage color, sexual dichromatism, and hyoid morphology are said to exist among some of these forms ( Gregorin, 2006), chromosomal comparisons provide the most compelling evidence for species recognition. Unfortunately, published karyotypes have only been reported for arctoidea (see Stanyon et al., 1995), macconnelli (including ‘‘ straminea ’’; Lima et al., 1990; Lima and Seuánez, 1991; Vassart et al., 1996), sara (see Minezawa et al., 1985; Stanyon et al., 1995), and seniculus (see Yunis et al., 1976; Lima and Seuánez, 1991). Among other chromosomal differences described in this literature, a shared Y-auto-

some translocation in arctoidea, macconnelli, and sara has resulted in a X 1 X 2 Y 1 Y 2 /X 1 X 1 X 2 X 2 sex-chromosome system, whereas seniculus has the standard XY/XX system. Chromosome painting ( Consigliere et al., 1996; Oliveira et al., 2002), mtDNA sequence comparisons ( Bonvicino et al., 2001; Cortés- Ortiz et al., 2003), and morphometric analyses ( Bonvicino et al., 1995) provide additional evidence of genetic divergence among these four taxa.

The red howlers of the Yavarí-Ucayali interfluve are referable to Alouatta juara sensu Gregorin (2006) , but the validity of this taxon seems questionable. Gregorin applied the name juara to western Amazonian (Brazilian and Peruvian) specimens collected south of the Amazon and west of the Purus, and he suggested that the name might also apply to unexamined Brazilian material collected north of the Amazon and west of the Negro. However, western Amazonian specimens geographically assignable to juara (sensu Gregorin, 2006) closely resemble typical seniculus in pelage coloration ( Hill, 1962) and cranial morphology ( Bonvicino et al., 1995). Likewise, the single available karyotype attributed to juara — obtained from an animal collected at Tefé

(on the south bank of the Amazon between the Juruá and the Purus)—was found to be ‘‘basically the same’’ ( Lima and Seuánez, 1991: 154) as the karyotype of typical seniculus from Colombia. Morphological material that we examined from the Yavarí- Ucayali interfluve falls within the range of phenotypic variation (coat color and craniodental dimensions) present in large comparative series of typical seniculus from northern Colombia; in the absence of any compelling data to the contrary, we conclude that the populations in question are conspecific, and that juara is a synonym of A. seniculus .

Craniodental measurements of the few available specimens of howler monkeys from the Yavarí-Ucayali interfluve are provided in table 2 . The only specimen accompanied by external dimensions is MUSM 11108, an adult male that measured 528 X 589 X 137 X 34 mm; unfortunately, no weight was obtained from this animal.

ETHNOBIOLOGY: The Matses have only one name for the howler monkey, achu, a word of uncertain etymology and one that is not synchronically segmentable. The pan- Panoan term for howler monkey is du/ru, a word with which the Matses are familiar, but which they do not consider a word in their language and therefore not a true synonym. Two or three varieties are recognized: achudapa ‘‘big howler monkey’’ (or achu piudapa ‘‘big red howler monkey’’), tsusa (a small howler monkey), and achu çhëşhë ‘‘black howler monkey.’’ The first two varieties, achudapa and tsusa, are recognized by all Matses hunters, but the third, achu çhëşhë (which we have never seen) is not known by all. This darker variety is reported to be red, but its underparts and the insides of its arms and legs are said to be black. It is said to live only along the upper Gálvez. Only those Matses that recognize achu çhëşhë use the term achu piudapa to contrast the red and black varieties. The term tsusa, which is not analyzable, is used to refer to the small variety, which is said to live in larger troops and to be lazier. Some speakers say that achudapa and tsusa sometimes travel togeth- er. Achu çhëşhë is said to differ in habitat preference from the other two varieties because it is found in forest where the trees are all short (i.e., the white-sand habitats of the upper Gálvez).

Traditionally, only old people were permitted to eat howler monkeys. If a child or a young person eats howler monkey meat, the Matses believe they will become lazy. The small variety of howler monkey, tsusa, is worse in this respect. For this reason, Matses do not hunt howler monkeys as frequently as they do other monkeys. The lassitude induced by eating howler monkey meat can be cured with frog poison 6 and by following a special diet. In smaller villages, where game is still plentiful, howlers are not hunted at all, while in larger villages, howlers are killed more frequently, for older people to eat. Nowadays, despite disapproval from older and more traditional Matses, some younger people are ignoring this dietary taboo. Their justification is that non-Indians eat howler monkeys without any ill effect. Alternatively, some Matses say that only howlers of the tsusa variety must not be eaten. Howler monkey canines are sometimes used to make men’s tooth necklaces, and young howlers are sometimes raised as pets.

Matses kill howler monkeys by following the sound of their calls from far away. Once they stop howling, they are harder to locate, so a hunter chants ‘‘chimu tawin tsipun

tsipun’’ (this is a phrase from a myth where people turned into howler monkeys by attaching a length of a vine called chimu as tails), as he walks toward the source of the howling, believing this will keep the monkeys from shutting up. When they see people, howlers that have not been exposed to hunting will come closer for a look, in which case they can be shot from the ground. Hunted animals will climb high up into a tree with vine tangles and hide in them. The hunter then climbs up to kill the monkeys with bow and arrow or shotgun. Less frequently, howlers are encountered at a mineral lick and killed there. They are easy to kill because they do not run off. Quite rarely, they are killed as they swim across a river. Matses do not imitate howler monkey calls or use dogs to hunt them.

MATSES NATURAL HISTORY: Howler monkeys are red, the color of a red brocket deer [ Mazama americana ], particularly on their backs. Red howler monkeys have large heads, large upper bodies, and small hindquarters. They have a large larynx in their throat, which makes their heads look elongated. They have a long tail that they use to grab onto branches. Their underparts are sparsely haired. Females are smaller than males. Males have long beards and a white scrotum.

Howler monkeys can be found in any primary forest habitat, but they do not come to abandoned swiddens. They are found mostly in floodplain forests and in swamppalm [ Mauritia flexuosa ] swamps. They are also found in upland forest far from rivers, but not as frequently. They go to mineral licks to eat mud and drink muddy water, and they also descend to drink water from streams. Otherwise, they do not walk around on the ground. They sometimes forage very high up in trees. They can swim well, and troops cross rivers swimming all together, with the babies clinging onto the adults’ backs.

Howler monkeys are found in small troops, always fewer than 10 individuals, counting the young. The troop is led by a large male that has a redder back than the other animals. This male has multiple females as mates. Males carry the young [there is some controversy among informants about this]. Eagles prey on smaller howler monkeys. The large male becomes aggressive when there is an eagle around. Jaguars can kill howler monkeys.

Howler monkeys wake up earlier than other monkeys. Howler monkeys howl saying ‘‘ yooo ’’ very early in the morning [from around 4 a.m.] until dawn [5–6 a.m.], stopping and then starting up again. The Matses can hear them from the village. They howl when it is going to be a nice day, so when Matses hear howler monkeys howl before daybreak, they know it will be a clear day. They also howl in the late afternoon [3–4 pm] and during full moons. During full moons they wake up to howl, but do not travel or feed. The big male howls first, and then the females and any other males join in. The males’ howls are louder and deeper than females’. The troop congregates and may put their arms around each other as they howl. They scream a lot when they are hit with an arrow.

Right from where they slept, howler monkeys howl, defecating at the same place where they howl. At daybreak they start to move through the trees slowly, looking for food. They are lazy, and do not move around much, and when they do, they do so slowly. Because they stay in the same place for a long time, they defecate where they hang out and there are many flies and ants around where they are, and it stinks there. They go to sleep together at dusk in trees that have many vine tangles. They have two or three places to which they always return to sleep. These sleeping sites can be identified by the smell. They always come back to the same mineral licks, where they get all dirty eating mud. They do not go to mineral licks early in the day; they go in the afternoon. One monkey stays in the trees as a lookout, while the others make a hole in the bank of the mineral lick and eat inside the hole. They do not follow a fixed route, but have a fixed territory and always come back to the same sleeping trees and mineral licks.

Their favorite food is swamp-palm [ Mauritia flexuosa ] fruit. They also eat the fruit of other palms, including isan [ Oenocarpus bataua ]. They drink the liquid from some unripe palm fruits, like dapais [ Attalea phalerata ]. Howler monkeys are the only monkeys that eat tsadte [ Apeiba aspera (Tiliaceae) ] fruits. They also eat many types of dicot tree fruits, including këku [ Couma macrocarpa (Apocynaceae) ], diden këku [ Parahancornia peruviana (Apocynaceae) ], machishte [ Rhigospira quadrangularis and? Mucoa duckei (Apocynaceae) ], mamuin [ Rheedia longifolia (Guttiferae) ], okodo mabis [an undetermined species of Guttiferae], moste [ Hymenaea spp. (Leguminosae) ], achu inkuente [ Inga spp. (Leguminosae) ], mannan tsipuis [ Inga spp. and? Pithecellobium (Leguminosae) ], tankada [ Parkia igneiflora , P. multijuga , Pithecellobium auriculatum (Leguminosae) ], bin [ Castilla (Moraceae) ], dadain [ Clarisia racemosa (Moraceae) ], chiwish [ Ficus spp. , Coussapoa spp. (Moraceae) ], piuşh bëchi [ Helicostylis tomentosa and H. elegans (Moraceae) ], şhankuin [ Pourouma spp. (Moraceae) ], bata [ Pseudolmedia and Maquira spp. (Moraceae) ], kose [ Manilkara bidentata (Sapotaceae) ], and taëpa [undetermined]. They also eat vine fruits, including poşhodi [ Passiflora nitida (Passifloraceae) ] and nënë pada [undetermined]. They also eat epiphyte fruits, including nënë pada [undetermined], and many types of young, soft leaves, including leaves of tote [ Eschweilera spp. and Lecythis spp. (Lecythidaceae) ] and iwise [? Capirona (Rubiaceae) ] trees. They eat spiders, crickets [or katydids], beetle grubs, and other invertebrates for which they search in palm crowns, under tree bark, and in rotten wood. They gnaw on rotten wood, especially rotten swamp-palm trunks.

Tables

TABLE 1 Nominal Taxa of Red Howlers in the Alouatta seniculus Complex Recognized as Valid by Recent Authorsa

Name	Type locality
amazonica Lönnberg, 1941b	‘‘Codajáz’’ (5 Codajás on left [north] bank of Amazon; Gregorin, 2006), Amazonas,
	Brazil
arctoidea Cabrera, 1940c	Northern Venezuela
insulanus Elliot, 1910 d	‘‘Island of Trinidad’’
juara Elliot, 1910	‘‘Rio Juara, Peruvian Amazon’’ (5 Rio Juruá, Brazil; Gregorin, 2006)
macconnelli Elliot, 1910e	‘‘Coast of Demerara’’ (5 coastal Guyana)
puruensis Lönnberg, 1941f	Jaburu, Rio Purus, Amazonas, Brazil (fixed by lectotype selection; Gregorin, 2006)
sara Elliot, 1910	‘‘Province of Sara’’ (5 Provincia Gutiérrez; Paynter, 1992), Santa Cruz, Bolivia
seniculus Linnaeus, 1766	Cartagena, Bolívar, Colombia (fixed by lectotype selection; Husson, 1978)

a Rylands et al. (2000), Groves (2001, 2005), Gregorin (2006).

b A synonym of juara according to Groves (2001, 2005) and Gregorin (2006).

c Cabrera’s arctoidea is a replacement name for ursina Humboldt, 1805 (preoccupied by ursina Kerr, 1792, a baboon) and, therefore, has the same type locality. According to Rylands and Brandon-Jones (1998), Humboldt’s ursina was based on observations of red howlers along the Caribbean coast of Venezuela (from Aragua to Sucre), in the llanos of Apure, and along the lower Orinoco.

d A synonym of macconnelli according to Groves (2001,

2005), but on zoogeographic grounds it seems likely that the

Trinidadian population is more closely related to howlers in northern Venezuela than to those in Guyana.

e Includes ‘‘ stramineus ’’ of authors (e.g., Lima and Seuánez, 1991; Bonvicino et al., 1995, 2001) according to Gregorin (2006).

f A synonym of juara according to Groves (2005).

TABLE 2 Craniodental Measurements (mm) of Alouatta seniculus from the Yavarí-Ucayali Interfluve

	AMNH	MUSM	AMNH
	986103	111083	98321♀
CIL	123.7	121.2	84.7
OB	65.6	71.0	52.7
POC	39.5	42.8	38.0
ZB	—	85.7	64.9
BB	52.6	53.0	47.6
PPL	—	—	46.2
LMT	43.1	36.3	38.8
BM1	8.6	8.2	7.9
M1–M1	40.2	—	32.4
I2–I2	—	15.9	13.6