MFOUs and Night Monkeys:

Paternal care in Aotus sp.

Jonathan Greenberg

Ecology Graduate Group

10 June 1999
Introduction

Owl monkeys (genus Aotus) are the world's only nocturnal anthropoids. They are

more widely distributed than any other genus of new world primate, occupying a range

from southern Panama far south into Paraguay. More remarkable is Aotus' mating

system: a rare form of monogamy in which paternal care has become obligatory. Many

aspects of Aotus' life history can be elucidated in the context of paternal care.

Unfortunately, most of the field research on Aotus has focused on the evolution of

nocturnality (Wright 1985) and interspecific competition with other nocturnal frugivores

(Aquino and Encarnacion 1986a). Little research has been performed looking at the

social system of wild owl monkeys. Here, I will describe the spatial and temporal

patterns of the owl monkey and suggest possible conditions under which paternal care

could evolve and persist across a great range of environmental conditions.

Morphology

Aotus is a small, sexually monomorphic neotropical primate. Mean body mass for

different species ranges from 455 g. (A. brumbacki, Hernandez Camacho and Defler

1985) to 930 g. (A. trivirgatus, Ayres 1986). Aotus is a quadruped and lacks a prehensile

tail (Stern 1971). Their coat is thick, counter-shaded and cryptic, similar to many other

nocturnal mammals (Moynihan 1976). Most divergences from the basic primate

morphology result from selection for their nocturnal lifestyle. Although they lack a

tapetum lucidum, a light-gathering instrument (Wright 1994) and retain several diurnal

eye features including a retinal fovea (Ogden 1975), Aotus have several visual

adaptations to nocturnality. Owl monkeys have strikingly large eyes. Hassler (1967)
found that nerve impulses from the rods of Aotus are accelerated which may function in

catching insects at night or visualizing the environment while moving rapidly (Wright

1994). The olfactory bulb of the owl monkey is the largest of any neotropical primate

(Stephan and Andy 1970). Owl monkeys use urine and glandular scents for territorial

markings and sexual recognition (Dixson 1983).

Taxonomy

Prior to (Hershkovitz 1983), Aotus (Family Cebidae) was thought to be a single

species, Aotus trivirgatus (Ford 1994). Through differences in karyotypes, neck

coloration and other pelage characteristics, and malaria susceptibility, he differentiated

the genus into nine species of two groups. The ancestral group contains the gray-necked

species A. lemurinus (subspecies lemurinus and griseimembra) of Venezuela and

northern Colombia, A. brumbacki of the eastern slope of the Andes in Colombia, A.

trivirgatus of southern Venezuela and northern Brazil, and A. vociferans west of A.

trivirgatus into Perú and Ecuador. The red-necked group contains the remaining five

species: A. infulatus of central Brazil, A. nigriceps of western Brazil and Perú, A.

micronax of the eastern Andean slope in Perú, A. nancymae of northern Perú and western

Brazil, and A. azarae (northern subspecies boliviensis and southern azarae) of Bolivia

and Paraguay. Distributions are shown in Figure 1 (*** INSERT MAP ***) (Ford 1994).

Geographic Distribution and Habitat

Aotus is the most widespread primate genus in the neotropics, found from Panama

to Argentina, from the mouth of the Amazon west into Peru and Ecuador (Ford 1994).
Aotus is usually found in more lowland areas, but in Colombia can be found at altitudes

exceeding 3200 meters (Eisenberg and Redford 1989). Aotus is a habitat generalist,

occupying primary and secondary forests, as well as human-created remnant forests

(Aquino and Encarnacion 1994). In Paraguay, A. azarae occupies dry forests where

temperatures range from 40˚ C down to - 5˚ C annually (Wright 1996).

Aotus is a habitat generalist but prefers areas with concealed sleeping sites such as

dense tangles or holes in large branches or tree trunks (Aquino and Encarnacion 1994).

Aquino and Encarnacion (1988) found that in Perú A. nancymai and A. vociferans have

the highest population densities in seasonally flooded lowland forests where there are

more available sleeping sites. Upland terra firmé forests tend to have harder-wooded

trees and fewer hollows in which Aotus can sleep (Aquino and Encarnacion 1988). A.

vociferans, in particular, will only use tree cavities to sleep (Hershkovitz 1983) and have

significantly lower population densities in the upland habitats than in lowland forests. It

is not uncommon to find Aotus sharing sleeping sites with other diurnal and nocturnal

mammals including Potos flavus (kinkajous), Bassaricyon gabbi (olingos), Coendu

bicolor (bicolor-spined porcupine), Tamandua tridactyla (three-toed anteaters), Isothrix

bistriatus (yellow-crowned brush-tail rats) and several species of chiropterans (Aquino

and Encarnacion 1994). P. flavus and C. bicolor have been known to keep Aotus groups

from entering the sleeping sites.

Aotus is usually found in the upper canopy while foraging (Aquino and

Encarnacion 1994) but will occupy all strata of the forest while moving and defending

their territories (Moynihan 1964; Wright 1978; Wright 1985). Aotus competes for food

with many diurnal and nocturnal frugivores. Although Aotus is small-bodied and lives in
small groups, direct interference competition is negligible since most nocturnal

frugivores are similarly small and solitary (Wright 1994). In Peru, A. nigriceps has been

found eating in the same tree with P. flavus and marsupials with no observed aggression

(Wright 1994). Without significant competition, Aotus is able to feed in larger crowned

trees (Wright 1989). Callicebus, a similarly sized diurnal primate with small group size,

is often seen being chased from large-crowned trees by larger competitors including

Cebus apella, C. albifrons, and Ateles paniscus (Wright 1994).

Nocturnal predators are unlikely to be a significant threat to owl monkeys.

Emmons (1987) found that nocturnal predators like owls, cats and snakes rarely, if ever,

eat primates. In the dry forests of Paraguay, Wright (1994) suggests that great horned

owls may be a threat to the owl monkeys which may explain the largely cathemeral

activity patterns and the frequency with which individuals changed sleeping sites (1 A.

azarae pair used 43 different sites over a period of 4 months). The most significant

predator threat is probably diurnal predators, which Aotus avoids by careful selection of

concealed sleeping sites (Wright 1994). Humans do not seem to be a significant predator

and Aotus' only economic values is to the biomedical industry (Emmons and Feer 1997).

Diet

Nocturnal animals typically have a lower basal metabolic rate (BMR) for their

body size than do diurnal animals (Crompton and others 1978). Le Maho and others

(1981) found that Aotus has a BMR 18 to 24% below Kleiber's standard curve for

BMR/body mass. Like most neotropical monkeys, Aotus feed on fruits, young leaves,

flowers and insects (Wright 1994). In Perú, Wright (1985) found that fruit composed
about 80% of the feeding minutes during most of the year, but Aotus relied heavily on

nectar (about 30% of foraging minutes) to offset the lack of fruit during the dry season.

During these periods of scarcity, figs become an important source of food for Aotus

(Wright 1985). Aotus nicriceps was found to forage on insects 15 to 20% of the time

year-round. Wright (1985) suggests the high amount of animal protein in its diet relative

to Callicebus is due to Orthopterans and Lepidopterans being more active and vocal at

night, facilitating capture.

Spatial Patterns

Aotus populations are comprised of two types of subunits: family groups and

solitary individuals. Family groups are most commonly comprised of a single male and a

single female and from 0 to 4 offspring of varying ages. Table 1 summarizes family

group sizes across different species. Typically, parents will have a single infant, juvenile

and occasionally a subadult within their group (Wright 1994). The most striking

characteristic of a family group is that the primary caregiver is the adult male who does

most of the carrying, playing, guarding and even food sharing with the offspring (Wright

1984). The mother will only be found carrying the infant in the first week following birth

and during nursing (Dixson 1994). Exceptions to the basic pattern of the family group

reported in A. nancymae have been two males and a single female or two females and a

single male. Adult females in multi-female groups are assumed to be adult offspring of

the family group and are thought to be nulliparous (Aquino and Encarnacion 1994).

Twinning is uncommon in the wild (1 observed twin in A. vociferans (Aquino and

Encarnacion 1994)) but occurs relatively frequently in captivity (2/35 births (Cicmanec
and Campbell 1977)) suggesting that during seasons of abundant food, female Aotus may

be able to double their reproductive outputs. When twinning occurs, fathers will carry

both offspring (Aquino and Encarnacion 1994).

Observations of solitary adults are uncommon so little is known of them. Aquino

and Encarcion (1990) have seen A. nancymae solitary adults ranging shortly after group

sizes decrease. Solitary adults may be male or female. They avoid the family groups

whose range they occupy (Wright 1985). It is likely that the solitary adults are offspring

of the local family groups, putting them at about 2 to 3 years of age (Wright 1985).

Aotus family groups are territorial towards neighboring groups. Territories are

small (mean area 9.2 ha) compared to other primates and have low daily path lengths

(mean length 708 s.d. 243) (Wright 1994). Territories have little overlap except at

fruiting trees at the borders between two territories (*** REFERENCE ***). Owl

monkeys defend their territories through vocalizations, scent marking and, on occasion,

agonistic behavior. During moonlit nights, an individual male or female adult or subadult

of a family group will move away from the family group to within 25 m. of the territory

boundary giving low-frequency calls which carry little more than 500 m. and are repeated

for 1 to 2 hours. Neighboring callers respond in kind, but callers rarely come closer than

50 m. from one another and retreat to the centers of their territories after a few hours

(Wright 1994). Besides vocalization, Aotus will also utilize urine and glandular

secretions in territorial defense (Moynihan 1964). Aggression, when it occurs, is always

over fruiting trees located at the borders between territories and involves loud calling,

piloerection, urination and defecation, chasing and wrestling(Moynihan 1964; Wright

1978; Wright 1994). Captive studies have found that males attack males, and females
attack females (Wright 1985). Aggression lasts about 10 minutes, after which both

families return to the center of their own territories (Wright 1994). Solitary individuals in

the territory of a family group will avoid the family group's feeding and sleeping sites

(Wright 1985), and no reported contact between solitary individuals and family groups

has been reported.

At a regional scale, Aotus lives at relatively high population densities. In most

areas, Aotus is at twice the density of the similarly sized Callicebus (Wright 1985). Table

2 summarizes owl monkey population densities across different species and habitats.

Temporal Patterns

Conception and infancy

Aotus is characterized by one of the fastest gestation periods of any neotropical

primate. At 133 days (Hunter and others 1979), owl monkeys infants are born a full

month earlier than Callicebus (Garber and Leigh 1997). The only neotropical primate

with a faster reported gestation is the golden lion tamarin (Leontopithecus rosalia) at 129

days (Dietz and others 1994). Aotus infants are actually a larger percentage of the adult

body weight at birth (10 - 13%, Ross 1991) than are Callicebus (about 8%, Garber and

Leigh 1997). At birth, Aotus infants weight about 97 g (range 90 to 105 g) and have a

developed fur coat (Dixson 1994). An infants will cling in a ventrolateral position on the

mother as she nurses and carries it for the first week.

The father begins to carry the offspring as early as the first day following birth,

and by the end of the first week is the primary caretaker (Dixson 1994). Infants are

transferred to the mother for suckling every 2 to 3 hours (Wright 1994). After suckling,
the mother bites the infant on the tail, hands or feet until it returns to the male (Dixson

1994). At three to six weeks, the infant begins to spend time off of the father and at

about four to six weeks it begins to eat solid food (Dixson 1994), often shared by the

father (Wright 1994). At 18 weeks the infant moves around independently, returning to

the father only when frightened (Dixson 1994). Infants are weaned at about 8 months

(Garber and Leigh 1997). There have been no reports of infanticide in Aotus in the wild

or in captivity.

Subadults and Solitary Adults

Weaned subadults remain with the family group until they are between 2 and 2.5

years of age (Wright 1994). At 211 to 400 days, subadults go through puberty (Dixson

1994). Subadults are often the individuals who call during territorial defense and it has

been suggested that these calls may also function in mate attraction (Wright 1985). At 2

1/2 years, Aotus individuals are sexually mature and emigrate from the group by

approximately 3 years of age (Wright 1994). Charles-Dominique (1980) has suggested

that the emigrating adult will likely pass through a vagabond stage during which it

searches for a mate. This is supported by observation of the solitary adults and by an

observation of a male subadult who traveled over 3 km, calling for 8 hours, presumably

for a mate (Wright 1985). The long distance traveled may suggest that males emigrate

father than the females but as yet there have been no studies to show this. The solitary

adults will avoid feeding and sleeping sites of the family groups in whose territory it

shares (Wright 1985).

Adult Females
 The adult female's ovarian cycle lasts 13 to 19 days (Dixson 1994). Females do

not appear to menstruate (Dixson 1994). During periovulation, females have no change

in external genitalia and do not solicit matings (Dixson 1994). Wright (1985) found in

Perú, Aotus has seasonal birthings during the end of the dry season and during the middle

of the wet season. Captive studies do not support this data (Dixson 1994)suggesting

seasonality of birthing may be heavily influenced by seasonality in abundance of

resources (Wright 1994). Females will give birth to twins on occasion, more often in

captivity (Cicmanec and Campbell 1977) than in the wild (Aquino and Encarnacion

1994). After birth, the mother carries the infant only for the first week, afterwards

rejecting the infant except to nurse (Dixson 1994). Mothers rarely, if ever, show any

affiliative behavior towards the offspring and, while foraging, will avoid the adult male

carrying an infant, often leaving him behind (Wright 1985). Interbirth intervals among

owl monkeys are only 8 months (271 days) on average (Dixson 1994).

Adult Males

Adult males show a surprising lack of spermatozoa (Dixson 1994) and have

extremely small testes for their body mass (mean volume 514 mm3) (Dixson and others

1980). Males mate infrequently (Kleiman 1977) and without regard to the period of the

female's ovarian cycle (Dixson 1994). Copulations are brief and it is likely that the male

ejaculates after a single pelvic thrust (Dixson 1983). Males carry the offspring almost

continuously for two to three weeks until the infant is able to travel independently

(Dixson 1994). There is significant energetic cost incurred by carrying the infant: a

carrying male will often arrive at a feeding site 10 to 15 minutes after the rest of his

family group (Wright 1994).

Discussion:

Maynard Smith (1977) and the Evolution of Obligate Paternal Care

Paternal care is a rare occurrence in mammals: over 90% of all mammals have

females caring for the offspring alone (Woodroffe and Vincent 1994). Since males will

often increase their reproductive success by mating with as many females as possible,

only in rare circumstances will males invest heavily in an individual offspring.

(Woodroffe and Vincent 1994) reviews factors which will increase the likelihood of

males caring for their offspring: increased offspring survival, high paternal certainty, low

additional mating chances, and care improving chances of future matings with the female.

Once paternal care is "introduced" as a viable strategy by males, females may evolve

strategies to maximize the benefits they get from male care.

The (Maynard Smith 1977) model for parental investment allows for an

examination of possible origins of Aotus' relatively unique mating strategy, female and

male evolutionary responses to "ancestral" paternal care, and potential evolutionary

trajectories given differing environmental influences. Let Px(g) be the probability of

offspring survival where x is the number of parents caring and g indicates the gender of

parent caring for the offspring in the case of x = 1 (M is male parent and F is female

parent: note that the model was originally applied to birds, and the inclusion of the

gender, g, of the single parent is my own modification on the model).

We can assume that offspring receiving care from both parents will have a higher

probability of survival than offspring which care from only one parent or no parental

care. Similarly, we can assume that some parental care is better than none, so:
 P2 > P1(g) > P0

Since all mammals are reliant on lactation early in life, infants can not survive

with only paternal care. As such, P1F > P1M = P0 = 0 and the relationship can be rewritten

as:

P2 > P1F > P1M = P0 = 0.

If a male does not care for his offspring, he will have p future matings. If a

female cares for her offspring, she will be able to birth additional w number of offspring

in a mating season and if she deserts she will be able to birth W number of additional

offspring. W must be greater than w. For biparental care to be an evolutionarily stable

strategy, these two conditions must be met:

1. wP2 > WP1M

2. P2 > P1F (1 + p)

Since, for all mammals the chances of an infant surviving without maternal care is

nil, condition (1) is met. For condition (2) to be met, males must either not be able to

acquire many extra-pair copulations, or infant survival from biparental care must be

much greater than if the females cared for the infant alone.

A number of ancestral environmental conditions could have strongly favored

biparental care in Aotus. These theories assume that paternal care is present to some

degree in the ancestral population. For the sake of simplicity, we will assume "standard"

monogamy is the rule where males can not defend ranges larger than a single female but

extra-pair copulations are performed when possible. If owl monkey populations were

experiencing extreme food shortages, P1F may approach or equal zero. In situations

where P1F = 0, if P2 is greater than zero, the few groups with caring males would be the
only ones with any reproductive success. If P1F was not substantially lower than P2,

biparental care could still be favored if the male's future chances of mating decreased

significantly. This may have occurred in periods of low population densities (widely

scattered food resources), high predation or the evolution of strong female choice

favoring caring fathers. If p becomes zero (no future matings beyond the female under

examination), since P2 > P1F, the male should care for the offspring to maximize his

reproductive success.

Current conditions in which Aotus currently lives suggest the environment in

which paternal care originated was much different than the present environment. Aotus

lives at high population densities, experiences a high turnover of new males and females

into the breeding pool and has shown little evidence that food is a significant selective

pressure. The more proximate question remains: if environmental conditions have

relaxed, why doesn't Aotus return to an ancestral state of monogamy? In the ancestral

condition, male care may have provided enough extra energy to the mother that females

with very low energetic input into the offspring were favored. Females with shortened

interbirth intervals or accelerated infant development, accompanied by a shortened

nursing period, had more surviving offspring per breeding season. In other words, the

advantage of biparental care over maternal care alone (P2 - P1F) has increased since the

ancestral condition. In this situation, males can be viewed as an energy resource for

females. Aotus females do show these characteristics of shortened interbirth intervals

through rapid infant development and shortened lactation. By females evolving

shortened interbirth intervals, even in the face of increased regional abundance of food,
P1F can continue to remain low and selection on males to continue to care will remain in

place.

Presently, the probability of extra pair copulations increasing the reproductive

success of the "cheating" male is likely to be low. This is apparent in the lack of any

morphological or physiological evidence of male-male competition. Aotus is sexually

monomorphic and males have extremely low spermatozoa and testes volume. The only

real evidence of male-male competition is over territorial disputes when males will fight

off males, and females will fight off females (Wright 1985). This, of course, could be

due to the females initiating competition with other females and the males fighting off the

remaining adult. Through behavior (infant biting) and, potentially, confusion of estrus,

females enforce male paternal care, decreasing p further.

Aotus mating system may be a "prototype" of a system that eventually led to the

twinning, polyandrous mating system of many Callitrichids. Gestation length is

extremely short, and to increase reproductive success further a possible response would

be for the production of twins. There is some evidence that by increasing food resources,

as seen in captive Aotus (Cicmanec and Campbell 1977), twinning becomes more

common. The limitation to the system in Aotus is the father, who carries both of the

twins (Aquino and Encarnacion 1994). Polyandrous systems like those found in tamarins

and marmosets are an answer to this possibility. There have been some reports of

polyandrous groups in Aotus (Aquino and Encarnacion 1994) but no work has been done

on relatedness of group members and the frequency of these systems appearing in the

wild.
Conclusions and Suggestions for Future Research

Research with a strong sociobiological backing has been relatively absent from

Aotus literature. An examination into the variation in social systems across Aotus taxa

with an emphasis on the polygynous and polyandrous "outliers" is needed. An analysis

of the energetic costs of raising an offspring coupled with the energy input from both

parents can show whether a mother is even capable of raising an offspring by herself

(Woodroffe and Vincent 1994).

Owl monkeys can provide strong insights into the evolution of paternal care in

mammals. Many aspects of their anatomy, physiology and behavior provide evidence of

strong selective pressures working on mating strategies of male and female Aotus.

Historical evidence is, of course, sorely lacking but the persistence of the same social

system across species, across habitats and regardless of resource availability suggests that

the obligation of males to care for their offspring has long since passed a threshold where

male owl monkeys can no longer benefit from acting like standard mammalian males,

increasing their reproductive success through multiple matings.

Table 1: Mean Group Sizes for Aotus
Species Mean Range Reference
Group
Size
A. azarae 4.1 1-4 (Ford and Davis 1992; Rathbun and Gache
1980; Wright 1985; Zunino and others
1986)
A. lemurinus Max = 4 (Green 1978; Heltne 1977)
A. nancymae 3.9 - 4.0 2-6 (Aquino and Encarnacion 1986b; Aquino
and Encarnacion 1994)
A. nigriceps 3.3 2-5 (Wright 1978)
A. vociferans 3.3 2-5 (Aquino and others 1990)

Table 2: Group and Population Densities for Aotus using transect methods (from Aquino
and Encarnacion 1994).
Species Forest Country Groups/ Indiv./ References
2 2
Type km km
A. azarae Gallery Argentin 6 18 (Rathbun and Gache
a 1980)
A. azarae Gallery Argentin 5.4 12.7 (Zunino and others
a 1986)
A. azarae Gallery Paraguay 3.3 - 4.6 8.8 - 14.4 (Stallings 1989)
A. lemurinus Gallery Colombia 18 - 150 (Heltne 1977)
A. lemurinus Gallery Colombia 2.5 - 9.5 15 - 33 (Green 1978)
A. nancymae Lowland Perú 13.5 46.3 (Aquino and
Encarnacion 1986b)
A. nancymae Highland Perú 5.9 24.2 (Aquino and
Encarnacion 1988)
A. nigriceps Hillside Perú 40 (Wright 1978)
A. nigriceps Lowland Perú 36 - 40 (Wright 1985)
A. vociferans Lowland Perú 10 33 (Aquino and
Encarnacion 1988)
A. vociferans Highland Perú 2.4 7.9 (Aquino and
Encarnacion 1988)
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