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 and interspecific competition with other nocturnal frugivores . 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, ) to 930 g. (A. trivirgatus, ). Aotus is a quadruped and lacks a prehensile tail . Their coat is thick, counter-shaded and cryptic, similar to many other nocturnal mammals . Most divergences from the basic primate morphology result from selection for their nocturnal lifestyle. Although they lack a tapetum lucidum, a light-gathering instrument and retain several diurnal eye features including a retinal fovea , Aotus have several visual adaptations to nocturnality. Owl monkeys have strikingly large eyes. 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 . The olfactory bulb of the owl monkey is the largest of any neotropical primate . Owl monkeys use urine and glandular scents for territorial markings and sexual recognition .
Taxonomy
Prior to , Aotus (Family Cebidae) was thought to be a single species, Aotus trivirgatus . 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.
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 . Aotus is usually found in more lowland areas, but in Colombia can be found at altitudes exceeding 3200 meters . Aotus is a habitat generalist, occupying primary and secondary forests, as well as human-created remnant forests . In Paraguay, A. azarae occupies dry forests where temperatures range from 40° C down to - 5° C annually .
Aotus is a habitat generalist but prefers areas with concealed sleeping sites such as dense tangles or holes in large branches or tree trunks . 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 . A. vociferans, in particular, will only use tree cavities to sleep 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 . 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 but will occupy all strata of the forest while moving and defending their territories . 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 . In Peru, A. nigriceps has been found eating in the same tree with P. flavus and marsupials with no observed aggression . Without significant competition, Aotus is able to feed in larger crowned trees . 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 .
Nocturnal predators are unlikely to be a significant threat to owl monkeys. found that nocturnal predators like owls, cats and snakes rarely, if ever, eat primates. In the dry forests of Paraguay, 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 . Humans do not seem to be a significant predator and Aotus' only economic values is to the biomedical industry .
Diet
Nocturnal animals typically have a lower basal metabolic rate (BMR) for their body size than do diurnal animals . 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 . In Perú, 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 . Aotus nicriceps was found to forage on insects 15 to 20% of the time year-round. 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 . 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 . The mother will only be found carrying the infant in the first week following birth and during nursing . 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 . Twinning is uncommon in the wild (1 observed twin in A. vociferans ) but occurs relatively frequently in captivity (2/35 births ) 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
Observations of solitary adults are uncommon so little is known of them. 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 . It is likely that the solitary adults are offspring of the local family groups, putting them at about 2 to 3 years of age .
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) . 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 . Besides vocalization, Aotus will also utilize urine and glandular secretions in territorial defense . 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. Captive studies have found that males attack males, and females attack females . Aggression lasts about 10 minutes, after which both families return to the center of their own territories . Solitary individuals in the territory of a family group will avoid the family group's feeding and sleeping sites , 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 . 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 , owl monkeys infants are born a full month earlier than Callicebus . The only neotropical primate with a faster reported gestation is the golden lion tamarin (Leontopithecus rosalia) at 129 days . Aotus infants are actually a larger percentage of the adult body weight at birth (10 - 13%, ) than are Callicebus (about 8%, ). At birth, Aotus infants weight about 97 g (range 90 to 105 g) and have a developed fur coat . 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 . Infants are transferred to the mother for suckling every 2 to 3 hours . After suckling, the mother bites the infant on the tail, hands or feet until it returns to the male . 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 , often shared by the father . At 18 weeks the infant moves around independently, returning to the father only when frightened . Infants are weaned at about 8 months . 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 . At 211 to 400 days, subadults go through puberty . Subadults are often the individuals who call during territorial defense and it has been suggested that these calls may also function in mate attraction . At 2 1/2 years, Aotus individuals are sexually mature and emigrate from the group by approximately 3 years of age . 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 . 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 .
Adult Females
The adult female's ovarian cycle lasts 13 to 19 days . Females do not appear to menstruate . During periovulation, females have no change in external genitalia and do not solicit matings . 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 suggesting seasonality of birthing may be heavily influenced by seasonality in abundance of resources . Females will give birth to twins on occasion, more often in captivity than in the wild . After birth, the mother carries the infant only for the first week, afterwards rejecting the infant except to nurse . 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 . Interbirth intervals among owl monkeys are only 8 months (271 days) on average .
Adult Males
Adult males show a surprising lack of spermatozoa and have extremely small testes for their body mass (mean volume 514 mm3) . Males mate infrequently and without regard to the period of the female's ovarian cycle . Copulations are brief and it is likely that the male ejaculates after a single pelvic thrust . Males carry the offspring almost continuously for two to three weeks until the infant is able to travel independently . 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 .
Discussion:
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 . 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. 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 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:
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:
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:
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 . 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 , twinning becomes more common. The limitation to the system in Aotus is the father, who carries both of the twins . 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 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 .
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
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| A. azarae |
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| A. lemurinus |
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| A. nancymae |
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| A. nigriceps |
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| A. vociferans |
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Table 2: Group and Population Densities for Aotus using transect methods (from .
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| A. azarae |
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| A. azarae |
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| A. azarae |
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| A. lemurinus |
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| A. lemurinus |
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| A. nancymae |
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| A. nancymae |
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| A. nigriceps |
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| A. nigriceps |
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| A. vociferans |
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| A. vociferans |
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Bibliography