Lemurine Owl Monkey (Aotus lemurinus)


MORPHOLOGY:
The lemurine owl monkey has a grooming claw on the fourth digit of both feet. Members of the genus Aotus are the only nocturnal New World primate. The legs of this species are longer than the arms, which assists in leaping. The lemurine owl monkey has large eyes, but lacks the tapetum typical of the nocturnal prosimians. The average body mass for this species is 1 kilogram, and no difference exists in body mass between males and females (Ford and Davis, 1992). The olfactory bulb, the accessory olfactory bulb, and the volume of the lateral olfactory tract nucleus are larger in relation to body and brain size in members of the genus Aotus to other platyrrhines (Stephan, 1972; Stephan et al., 1981).

RANGE:
This species lives in forests where the trees are evenly dispersed. The lemurine owl monkey is found in Panama, Northern and Western Colombia, and Western Venezuela (Nowak, 1999). This species may have a range that extends northward into Costa Rica, but confirmed, documented sightings are lacking (Timm, 1988).

ECOLOGY:
The lemurine owl monkey is a frugivorous species that also eats leaves and insects. The lemurine owl monkey prefers to eat small ripe fruit (Kinzey, 1997). An advantage of foraging at night is decreased competition from diurnal frugivores and the presence of larger nocturnal insects (Wright, 1989).This species spends all of its life up in the trees (Kinzey, 1997). The lemurine owl monkey becomes more active when the moon is bright (Wright, 1984), and they travel the same route during the night, so they may memorize routes when they travel when the moon is brighter (Wright, 1989)

LOCOMOTION:
The lemurine owl monkey moves through the forest quadrupedally in the trees, but also can leap from tree to tree (Fleagle, 1988).

SOCIAL BEHAVIOR:
The basic group of lemurine owl monkeys is composed of a breeding pair and their offspring. This species has a monogamous mating system (Kinzey, 1997). The monogamous mating system is correlated with having males present to help raise offspring and having food resources in predictable, uniform patches (Wright, 1986). Both males and females disperse in this species (Kinzey, 1997). The young stay with their birth group until between 2.5 and 3.5 years old, then they disperse (Kinzey, 1997). Social grooming is not common for members of this genus (Fleagle, 1988). During the first week of an infant's life they are carried by the female, but after that the male is the sole carrier of the infant, and the infant only returns to the mother to suckle for milk (Dixson and Fleming, 1981). During the 18th week the inafnt moves independently most of the time except when there is a disturbance where it will go back to the father (Dixson and Fleming, 1981). The female will reject the infant after suckling and if it tries to establish contact by biting the tail, hands, or feet of the infant; the infant usually squeals (Dixson and Fleming, 1981). The adults do groom their infants frequently using their mouth, and the most important areas groomed are the face and the ano-genital region (Dixson and Fleming, 1981). At first the infant clings to the parents in a ventro-lateral position, between the thigh and hip of the parent, but as it gets older it moves to the dorsal clinging position, that is on the back of the parent (Dixson and Fleming, 1981).

VOCAL COMMUNICATION:
hoot call: This is a long, low call, of between 200-400 hertz, emitted by an individual, and can be heard for 500 meters (Wright, 1985). Each hoot is made up of 2 long sounds and 2 to 5 short sounds, with brief intervals, making them sound all like one note (Moynihan, 1964). Hoot bouts occur singly or in a series from 2 to 4 (Moynihan, 1964). During each bout the mouth is slightly opened, then closed between bouts (Moynihan, 1964). This call is used to communicate sexual advertisement, and is used by females or subadult males when looking for mates (Kinzey, 1997). This call is also emitted by a separated juvenile, or by an adult if its mate has been separated (Kinzey, 1997).

resonant whoop: This call consists of a series of 10-17 low grunts which build up in intensity to a climax, and is used to communicate defense of a fruit tree used for feeding (Kinzey, 1997). This call starts low and soft, softer than gruff-grunt (Moynihan, 1964). Then the succeeding notes became louder, rapidly, and during the middle of the call the notes are much louder than gruff-grunt and take on a resonating quality that lasts for a few notes (Moynihan, 1964). The last part of the call the notes decrescendo, becoming softer, lower, and slower (Moynihan, 1964). The notes of this call are monosyllabic in nature (Moynihan, 1964). An individual performing this call will go into back-arch, and then stop when the call is completed (Moynihan, 1964). The elbows also move during this call, going in (towards the body) when the note is uttered and going out (away from the body) between the notes (Moynihan, 1964). This pumping action of the elbows may help to increase air flowage moving in and out, which would assist in sound production (Moynihan, 1964). This call may also be emitted during hostile situations, functioning as a threat display (Moynihan, 1964).

gruff-grunt: This call is low-pitched, moderately long, and moderately loud in nature (Moynihan, 1964). The call is uttered singly or in a short series of 2 to 5 notes (Moynihan, 1964). When occurring in series, several series may be emitted which are separated by long pauses (Moynihan, 1964). The mouth is closed or almost completely closed when this call is emitted (Moynihan, 1964). This call is emitted during hostile encounters, during intraspecific disputes, and as a reaction to a predator or a potential predator (Moynihan, 1964). When emitted during intraspecific disputes, the call occurs before or after an attack (Moynihan, 1964). This is essentially a threat call (Moynihan, 1964).

scream: This call is high in pitch but wavering, and can be quite prolonged (Moynihan, 1964). When the call is uttered the mouth is usually wide open (Moynihan, 1964). This call functions to startle a predator or potential predator, giving the individual time to escape (Moynihan, 1964). When this call is emitted by infants or young juveniles this call is softer and more plaintive in tone (Moynihan, 1964).

low trill: This is described as "a 'bubbling' series of short low-pitched notes. uttered very rapidly one right after the other but still distinguishable by the human ear" (Moynihan, 1964). The individual notes of the call are described as being slightly plaintive in tone (Moynihan, 1964). The number of notes varies from 2 to 12 in a series and successive notes tend to rise in pitch (Moynihan, 1964). This call is done with the mouth closed or almost closed (Moynihan, 1964). This call is emitted during initial greeting ceremonies between individuals, and when this occurs between members of the opposite sex, the female will emit this call more frequently than the male (Moynihan, 1964).During the greeting, this call will often occur before or during social sniffing (Moynihan, 1964). The call may serve to function as a threat between novel individuals (Moynihan, 1964). This call may also function as an appeasement display (Moynihan, 1964). This call is heard in association with moan and sneeze-grunt (Moynihan, 1964).

moan: This call is brief, soft, and described as plaintive sounding (Moynihan, 1964). The mouth is closed when this call is emitted (Moynihan, 1964). This call serves the same function as low trills do, and also when two mates are separated and brought back together (Moynihan, 1964). This call is also heard during the first parts of a precopulatory sequence (Moynihan, 1964). This call is heard in association with low trill, gulp, and sneeze-grunt (Moynihan, 1964). This call may occur when hostile and nonhostile stimuli occur simutaneously (Moynihan, 1964). This call also function as an appeasement call (Moynihan, 1964).

gulp: This call is moderately loud and "liquid" in nature, sounding like a human belch (Moynihan, 1964). The mouth remains closed during this call, but the throat swells up (Moynihan, 1964). The call is uttered in a series of 2 to 5 notes, with 2 or 3 being the most common (Moynihan, 1964). This call was heard in captivity during vigorous locomotory activity, and may function as being a contact call (Moynihan, 1964). Contact calls would be important for this species because of the need to maintain contact during the night when moving and/or foraging (Moynihan, 1964).

sneeze-grunt: This call is described as being sounding like a sneeze superimposed upon a gruff- grunt (Moynihan, 1964). The call is sharp and abrupt, and has a slightly nasal tone (Moynihan, 1964). Usually this call is emitted singly, but sometimes two are emitted in a quick succession (Moynihan, 1964). The mouth is closed or nearly closed when this call is uttered (Moynihan, 1964). This call occurs in association with gulp, moan, and low trill (Moynihan, 1964). This call may function as a contact call like gulp (Moynihan, 1964).

squeak: This call is made up of two to three sounds with short intervals in between them and are brief and relatively high in pitch compared to a grunt (Moynihan, 1964). The pitch of this call usually first rises then falls (Moynihan, 1964). This call is emitted by infants and young juveniles (Moynihan, 1964). This call is uttered when an individual is distressed, for example when it separated from its parent (Moynihan, 1964).

high trill: This call sounds like three to four squeaks emitted in rapid succession (Moynihan, 1964). This call rises and falls in pitch with the first two notes rising and the last two notes falling in pitch (Moynihan, 1964). This call may be interpreted as components of squeaks or a discontinuous series of squeaks (Moynihan, 1964). This call is emitted by infants and young juveniles (Moynihan, 1964). This call is produced in response to distress with an alarm or escape component (Moynihan, 1964).

Moynihan (1964) made an interesting comment regarding infant vocal patterns:

"It is interesting that the vocal patterns uttered by infants
who want to attract or join their parents are similar to those
of adults who want to attract or copulate with their mates.
This might suggest that the sexual tendencies
of adults develop from the infantile tendency to keep in
contact with parents."


OLFACTORY COMMUNICATION:
urine-wash: This is when an individual will deposit urine on its hands and then rub the hands on a branch or other substrate. This is used to communicate sexual attraction.

social sniffing: This is when one individual will approach another, stick its neck out, and smells the other individual (Moynihan, 1964). The duration of each sniffing bout lasts for a few seconds, and the individual being sniffed will remain motionless while this occurs (Moynihan, 1964). The individuals start out nose-to-nose before a sniffing bout will occur, then individual who will sniff will bring its head as close to other as possible (Moynihan, 1964). The most common places which are sniffed are the armpit and/or the perineal region (Moynihan, 1964). The individual being sniffed will sometimes respond by sniffing, and two individuals may occasionally sniff each other's perineal region simultaneously (Moynihan, 1964). This behavior is done when two individuals meet each other for the first time, thus this functions as part of a greeting ceremony (Moynihan, 1964). Individuals who have just met each other may repeat social sniffing for the first few hours after first introduction (Moynihan, 1964). This behavior is also seen before copulation amongst mates (Moynihan, 1964).

VISUAL COMMUNICATION:
back-arch: This is when an individual will raise the dorsal part of the body while in a quadrupedal stance, with all four limbs held straight (Moynihan, 1964). Sometimes an individual will have the hands free, in a standing position with the knees slightly bent and the palms facing outward, when performing this behavior (Moynihan, 1964). This display is used to communicate aggression.

swaying: This is when an individual will move its body back and forth, from side to side in a smooth, regular, moderately rapid, wide arch (Moynihan, 1964). The head of the individual is either facing straight forward while moving or turns the head to the right when moving to the right and turning the head to the left when moving to the left (Moynihan, 1964). This behavior may have gruff-grunts or gulps occurring at the beginning or the ending of a bout (Moynihan, 1964). An individual will do this with the hands clasping or free from a branch (Moynihan, 1964). This is done in response to the presence of a predator or a potential predator (Moynihan, 1964). This behavioral pattern is often followed by overt escape (Moynihan, 1964). An individual might do this to let the potential predator know that they have been detected, thus discouraging the predator (Moynihan, 1964). An individual can save energy that would be used for escaping by doing this because the predator would not waste time chasing after the individual because it knows it has been detected (Moynihan, 1964).

rubbing: This is when an individual will flex their legs, press their perineal region against a substrate, and start rubbing the region against the substrate with rapid side-to-side motions (Moynihan, 1964). Individuals tend have favorite sites where to perform this behavior (Moynihan, 1964). This behavior is done between males and females and in the context of hostile or copulatory patterns (Moynihan, 1964). This behavior is done more by females than by males (Moynihan, 1964). Males tend to be slightly dominate over females, and in an instance where a female was dominant over a male, the male performed rubbing during an encounter with her (Moynihan, 1964). This suggests that perhaps this behavior is a submissive display.

TACTILE COMMUNICATION:
rejection bite: This is done by the mother to the infant after suckling or when the infant tries to establish contact after the first week; also done by the male more after the first 8 weeks (Dixson and Fleming, 1981). The mother will bite the tail, hands or feet of the infant, signaling it to move away (Dixson and Fleming, 1981). The infant will often squeal after being bitten (Dixson and Fleming, 1981). The mother does this in higher frequency than the male up to the first 8 weeks of an infants life (Dixson and Fleming, 1981).

social grooming: This behavior is only associated with copulation in this species (Moynihan, 1964). This is where one individual will use the hands and the teeth to remove dead hairs, dead skin, and small arthropods from hair of another (Moynihan, 1964). The hands are used to separate the hair so that the teeth may be used to get at the base of the hair (Moynihan, 1964). The most common places groomed are the sides, back, crown, and back of the head (Moynihan, 1964). Social sniffing usually occurs before a grooming bout will occur (Moynihan, 1964). This behavior occurs before and after both successful and unsuccessful copulation attempts (Moynihan, 1964).

REPRODUCTION:
The lemurine owl monkey most often gives birth to a single offspring, although twins have been recorded. The gestation period for this species is 133 days and the minimum inter-birth interval is 150 days (Hunter et al., 1979). Copulation attempts tend to be brief and rapid, with the male and female first quietly approaching each other (Moynihan, 1964). Then the male performs social sniffing, and the female may social sniff while the male is doing the same to her (Moynihan, 1964). Mating is done dorso- ventrally, with the male inserting his penis under the female's tail, with female moving the tail slightly (Moynihan, 1964). The male usually makes 3 to 4 pelvic thrusts, with ejaculation occurring on the last thrust (Moynihan, 1964).

REFERENCES:
Burton, Frances. 1995. The Multimedia Guide to the Non-human Primates. Prentice-Hall Canada Inc.

Dixson, A.F. and Fleming, D. 1981. Parental Behaviour and Infant Development in Owl Monkeys (Aotus trivirgatus griseimembra). Journal of the Zoological Society of London. Vol. 194, 25-39.

Fleagle, John G. 1988. Primate Adaptation and Evolution. Academic Press.

Ford, S.M. and Davis, L. C. 1992. Systematics and Body Size: Implications for Feeding Adaptations in New World Monkeys. American Journal of Physical Anthropology. Vol.88, 415-468.

Hunter, J., Martin, R.D., Dixson, A.F., and Rudder, B.C.C. 1979. Gestation and Inter-birth Intervals in the Owl Monkey (Aotus trivirgatus griseimembra). Folia Primatologica. Vol. 31, 165-175.

Kinzey, W.G. 1997. Aotus. in New World Primates: Ecology, Evolution, and Behavior. ed. Warren G. Kinzey, Aldine de Gruyter, New York.

Moynihan, M. 1964. Some behavior patterns of platyrrhine monkeys I. The night monkeys (Aotus trivirgatus). Smithsonian Miscellaneous Collections. Vol. 146(5), 1-84.

Nowak, R.M. 1999. Walker's Primates of the World. The Johns Hopkins University Press, Baltimore and London.

Stephan, H. 1972. Evolution of primate brains: A comparative anatomical investigation. in The Functional andd Evolutionary Biology of Primates. ed. R.H. Tuttle. Aldine-Atherton, Chicago.

Stephan, H., Frahm, H., and Baron, G. 1981. New and revised data on volumes of brain structures in insectivores and primates. Folia Primatologica. Vol. 35, 1-29.

Timm, R.M. 1988. A review and reappraisal of the night monkey, Aotus lemurinus (Primates: Cebidae), in Costa Rica. Revista de Biologia Tropicale. Vol. 36 (2B), 537-540.

Wright, P.C. 1984. Biparental Care in Aotus trivirgatus and Callicebus moloch. in Female Primates: Studies by Women Primatologists, ed. M. Small. Alan R. Liss, N.Y.

Wright, P.C. 1985. The Costs and Benefits of Nocturnality for the Night Monkey (Aotus trivirgatus). Unpublished Ph.D dissertation, City University of New York, New York.

Wright, P.C. 1986. Ecological Correlates of Monogamy in Aotus and Callicebus. in Primate Ecology and Conservation. eds. J. Else and P. Lee. Cambridge University Press.

Wright, P.C. 1989. The Nocturnal Primate Niche in the New World. Journal of Human Evolution Vol. 18(7), 635-658.

Last Updated: April 25, 2007.
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