Nocturnality in the Owl Monkey, Aotus sp.
Jonathan Greenberg
3 December 1997
Mirrored from his site
Introduction
Aotus sp., the owl monkey, is the world's only nocturnal monkey and one of the most widespread primates in the neotropics. The odd activity pattern of this primate seems at first anomalous but at a closer glance brings up many proximate and ultimate level questions as to its development and yields insights into wider-ranging ecological principles. For a primate which shares similar morphology, social system and diet to other diurnal primates such as the titi monkey (Callicebus), Aotus has markedly different lifestyle strategies. Morphology, geographical and habitat distribution, social system and diet all factor into the explanations of the development of nocturnality on Aotus. These differences can serve to test the effects of interspecific competition, predation, group size and foraging patterns. A strong case can be made for the effects of interspecific competition being the driving force behind Aotus' activity patterns by examining variation both intraspecifically as well as between Aotus and other sympatric primates. Dietary choices are also suggested to play an important role in determining activity patterns. Predation pressure differences between night and day may also causes an adaptive response leading towards activity patterns matching periods of low predation.
Morphology
Aotus sp. is a relatively small-bodied primate. Head and body measures approximately 350 mm, weight 1 kg. (Napier & Napier, 1996). Sexual dimorphism is almost nonexistent. The coats are thick and counter shaded: grayish brown with pale underparts (Napier & Napier, 1996). Aotus coats are relatively cryptic and resemble many other nocturnal animals including lorises, phalangerids, opossums and owls (Moynihan, 1976). The faces have dark stripes and white patches over the eyes. The white patches may be used in intraspecific encounters or for defense to give the illusion of looking alert even while their eyes are closed (Moynihan, 1976). The eyes are large and lack cones but contain a fovea, suggesting the ancestor of Aotus was a diurnal monkey (Napier & Napier, 1996). Aotus is color blind. The tail is nearly as long as the body and acts as a balancing organ for quadrupedal locomotion (Wright, 1985). Aotus' intermembranal index is 74 (Napier & Napier, 1996). The ears are small and round (Wright, 1985). The digits of Aotus have true nails, two of which are possibly a grooming nail on the toes similar to those found in prosimians (Wright, 1985). Aotus has conspicuous tactile pads (Wright, 1985), the terminus of which is free to bring into contact with branches and other objects in its environment (Napier, 1976). Teeth are adapted to frugivory: canines are small and ineffective as nut-crackers and molars have a relatively unpronounced cristid obliqua (Wright, 1985). The mandible is more shallow than Alouatta and Callicebus, suggesting little specialization to folivory (Wright, 1985). The vomeronasal organ and nasopalatine ducts of Aotus are large (Hunter et al., 1984) and olfaction is well-developed when compared to other Neotropical primates (Bolen and Green, 1997).
Taxonomy
Aotus sp. (Family Cebidae, Subfamily Aotinae) is most closely related to the titi monkeys (Callicebus sp.). Originally thought to be a single species with different subspecies, more recent analysis has split the genus into at least nine distinct species (Hershkovitz, 1983). The genus Aotus may be over 12 million years old (Setoguchi and Rosenberger, 1987) and probably evolved from a diurnal ancestor into nocturnality which was, at the time, practiced solely by marsupials and rodents (Wright, 1995), most of which are quite a bit smaller than Aotus. Setoguchi and Rosenberger (1987) suggest Aotus' nocturnal lifestyle dates back at least as far as the 12 million year old fossil of Aotus didensis.
Geographical Distribution and Habitat
Aotus is found in most of northern South America from Panama to northern Argentina and from the Pacific in Ecuador and Colombia to the Atlantic in Brazil (Robinson et al., 1987). They are found from lowland forest to high altitude cloud forests at 3000 m (Napier, 1976). They can occupy virtually every wooded habitat found in these regions. Aotus are found in every strata of a forest, from 7 to 35 m (Wright, 1981).
Aotus sleeps in holes in hollow trees or in dense vine tangles (Wright, 1981). There is some variance in nesting preference geographically and Rathbun and Gache (1980) have reported Argentinean owl monkeys sleeping almost exclusively in vine tangles. There are reported cases of interspecific competition over sleeping sites with Potos flavus (kinkajou) (Aquino and Encarnacion, 1986). Cohabitation with other species has also been reported with bats, P. flavus, Bassaricyon gabbi (olingo), Coendu bicolor (Aquino and Encarnacion, 1986), and Isothrix bistriatus (Puertas et al., 1995). Coocupation of the same tree has been seen with Coendou sp. and Caluromys lanatus (Puertas et al., 1995). Choice of concealed nesting sites is probably influenced by predation (Heymann, 1995 and Isbell, 1994) and proximity to feeding sites (Heymann, 1995).
Aotus is found in regions with extremes in temperatures, particularly in the subtropical dry forests of the Chaco of Paraguay where daily temperatures can range from 40° C down to -5°C (Wright, 1995).
Social System
Aotus is usually reported as a highly monogamous primate. Groups are often composed of an adult male and female and up to three infants and juveniles. However, reliable observations of up to five multi-adult groups moving through the canopy together have been reported (L. T. Rosengreen, pers. comm.) and multiple-adult groups nesting together (Hernandez-Camacho and Cooper, 1976). Other reports of larger groups of up to 30 individuals found in fruiting trees are probably aggregations of smaller groups, a point supported by a high degree of agonistic behavior between individuals in the larger groupings (Wright, 1981).
Owl monkeys have a relatively short interbirth interval of about one year which is possible due to high levels of paternal care which alleviates much of the energetic costs to the mother (Garber and Leigh, 1997). Male owl monkeys carry the young, defend them from predators, play and instruct them (Wright, 1985). The social system benefits the male, usually limited by access to females, by providing high parental certainty (Garber and Leigh, 1997), low infanticide rates and short interbirth intervals. Owl monkeys are unique in that females will actively refuse to carry the young if the male is unavailable, going so far as to violently pull the infant off of its back (Eduardo ???, pers. comm.) Two birth peaks occur, one at the end of the dry season and the other in the middle of the wet season (Wright, 1985). Gestation is about 133 days (Hunter et al., 1979). Young disperse at two to three years (Wright, 1985) and probably pass into a nomadic, "vagabond" stage before pair-bonding with a female (Charles-Dominique, 1977).
Male-male aggression is common and is a factor in keeping groups apart (Moynihan, 1964). Agonistic encounters involve back arching, stiff-legged jumping, pilo-erection, urination and defecation, as well as giving clicking/grunting alarm calls. Identical agonistic displays occur between conspecifics and other species (Wright, 1978).
Aotus is highly territorial. Territories are extremely small for a primate of its size, usually no greater than 10 ha (Wright, 1985). Although little work has been done on the dynamics of territory size and location over time, it has been suggested, based on the behaviors of nocturnal prosimians, that Aotus is relatively sedentary (Charles-Dominique, 1977). This is supported by Isbell’s (1994) conclusion that use of unfamiliar areas by primates may increase the rates of predation. Relatively mobile, daily path lengths are reported to be approximately three-quarters of a kilometer. Territories between neighboring groups overlap extensively (Wright, 1978). Aotus has been reported to come out of trees and cross open savanna to move between forest patches (Rathbun and Gache, 1977). Population densities in Peru are reported to be around 25 to 50 individuals per km2 (Moynihan, 1976).
Aotus is a relatively noisy monkey, uttering loud contact and locomotory notes (Moynihan, 1976). Olfaction is an important component of communication and Aotus marks substrates by rubbing a gland at the base of its tail and exuding a brown, oily substance (Wright, 1981).
Diet
Aotus' diet consists of fruits, insects and leaves. Spending approximately 50% of its waking hours foraging (Wright, 1985), the owl monkey has a wide range of diet compositions both geographically as well as seasonally. In Peru, Aotus spends three-quarters of its time foraging for fruits, and the remaining time searching for leaves and insects. In Paraguay, conversely, only 16% of its time is spent foraging for fruits, 40% on leaves, 11% on insects and the remaining 33% on other food sources (Wright, 1985). Aotus spend much of their time foraging in medium- to large-crowned trees.
Fruits are usually sweet or bland, though about 15% are bitter-tasting . There is probably an increased ability to digest secondary compounds found in the fruits and other foods consumed. Due to the color-blindness, color choices are presumed to be irrelevant. Aotus feeds on over 70 different species of fruits in Peru. Figs become extremely important food sources in time of scarcity (Wright, 1985).
Due to the small body size, folivory is uncommon in wetter habitats. Leaves eaten are either young leaves or taken from lianas of any age. Flowers and nectar are eaten when available, and nectar becomes the sole source of nourishment in July and August when food is extremely scarce (Wright, 1985). In areas with little fruits or nectar in scarce seasons, folivory increases significantly (Wright, 1995).
Seed predation is rare in Aotus. The seeds pass unharmed through the gut (Wright, 1985) which may suggest Aotus is an important dispersal agent.
Insects are an important source of protein for the owl monkey and occupies, on the average, one-fifth of their foraging time. Over half of the feces collected for Aotus contained insect parts, compared to less than one-fifth for Callicebus (Wright, 1985). Aotus preys primarily on large orthopterans, lepidopterans, coleopterans and spiders which it forages for at dusk and dawn and on clear, moonlit nights (Wright, 1995). Rarely missing, Aotus captures insects during methodical movements along branches and catching them on the branches or in the air (Wright, 1985).
There have been reports of consumption of vertebrates such as bats, small birds, eggs and lizards (Bates, 1863; Sanderson, 1957) but this is probably rare (Wright, 1985).
Predation
Predation pressures are suggested to be low for Aotus. Nocturnal activity patterns preclude many of the diurnal predators, such as raptors, from creating any serious threat. Nocturnal prey, also, are harder to detect than are diurnal (Isbell, 1994). Although occasionally nocturnal, many of the potentially threatening snakes are terrestrial with few exceptions, and Aotus rarely leaves the trees. Felids do pose a threat, though Wright (1985) has suggested Aotus are quite capable of evading them. Larger owls such as the Great-horned owl may pose a threat to the infants and juveniles (Wright, 1985).
Activity Patterns
Activity patterns are more diverse than was originally thought in Aotus. In Colombia, Ecuador and most other habitats, the monkeys are entirely nocturnal (Salano, 1995 and Rosengreen, pers. comm.). In the palm savannas of Paraguay, Argentina and Bolivia, however, owl monkeys are partly or entirely diurnal (Mann, 1957; Rathbun & Gache, 1977; Wright, 1983). Aotus is usually more active during the full moon than the new moon (Erkert and Grober, 1986).
Why Be Nocturnal?
Characteristics of Nocturnal Animals
Nocturnal animals, particularly mammals, tend to have small, non-gregarious social systems. Low light levels require an increase in reliance on auditory and olfactory means by which to communicate (Charles-Dominique, 1974). Olfaction is probably more effective at night due to higher olfactory transmissions rates (Wright, 1995). Color vision tends to be lacking. Nocturnal species tend to be small, as studies in Gabon and Barro Colorado Island in Panama have shown: both birds and mammals have much lower body weights than do diurnal. No nocturnal primate exceeds 1 kg (Charles-Dominique, 1974) and no nocturnal Neotropical mammal exceeds 6 kg (Wright, 1995).
Olfaction is the primary sense in locating plant foods (Charles-Dominique, 1977). Insectivory tends to be a more important component of the diet in nocturnal animals than in diurnal. Capturing insect prey requires good hearing and dexterity (Charles-Dominique, 1974). It is worthy to note no diurnal strepsirhines save Lemur catta are predatory (Petter, 1962).
Three Hypotheses for the Development of Nocturnality in Aotus
Aotus shares all of the aforementioned characteristics of nocturnal animals. However, the question of why nocturnality is beneficial to the owl monkey's reproductive success remains unclear. Nocturnality was not the "default" character state in Aotus, rather a derived trait developed from a diurnal ancestor. Lacking a tapetum lucidum, Aotus does not have the overly specialized eyes for night living. Still, the success of the owl monkey at colonizing much of the neotropics is undeniable. Three explanations present themselves to the reasons in which this unique shift in activity pattern evolved: response to interspecific competition for resources, exploitation of an un- or under-utilized food niche, and avoidance of predators.
Avoidance of Direct Interspecific Competition
The most convincing explanation as to the benefits of nocturnality is due to the avoidance of interspecific competition. Aotus has little direct contact with diurnal animals who might displace them from their feeding sites. One of the most important pieces of evidence to support this hypothesis comes in the differences in feeding tree size between Aotus and Callicebus, a similar diurnal species. Callicebus, a small monogamous frugivore, exploits smaller-crowned trees which may not provide enough food or be found quickly enough by larger-bodied and larger-grouped primates. Larger-crowned trees are dominated by larger primates who will displace Callicebus if found feeding. There have been reports of Ateles paniscus, Cebus apella and Cebus albifrons displacing smaller primates from feeding sites. Saimiri uses large group size to prevent interspecific displacement by larger primates from becoming effective at keeping them out of larger fruiting trees. Unlike Saimiri, Callicebus does not have the advantages in numbers (Wright, 1995). Aotus, on the other hand, has little interspecific interaction with larger animals at feeding sites as most nocturnal animals are both small and solitary (Wright, 1985). During a full moon, however, Wright (1985) did report displacement by Saimiri and Cebus. Aotus prefers larger-crowned trees which can be defended against conspecifics and provide more than adequate nourishment while allowing for smaller territories. In Paraguay there is a reduced number of diurnal primates (Wright, 1985) which, by using the hypothesis of interspecific competition avoidance may explain the diurnal activity patterns of Aotus in this habitat.
Aotus are displaced by Didelphis sp. (opossum), P. flavius, and Bassaricyon sp. but are never aggressively chased from their feeding site (Wright, 1985). Little direct or indirect competition is found with the chiropterans (Estrada et al., 1984), which are not large enough to pose a threat (Wright, 1985). Lack of intense folivory precludes any intense interactions with other folivores such as the bamboo rat (Wright, 1985).
By avoiding most sympatric species, Aotus is able to exploit a wider range of habitats while minimizing dangers of injurious encounters with larger primates and the need to defend large territories. Being one of the largest nocturnal frugivores (Wright, 1995), the owl monkey is able to out-compete most sympatric species active at night.
Exploitation of Underutilized Food Niches
Due to high levels of sympatry between many primates, different strategies have evolved to decrease the niche overlap: species who can exploit underutilized resources with little interspecific competition will have a selective advantage over those who try to directly compete with sympatric species (MacArthur, 1958). Aotus uses its nocturnal activity patterns as well as a generalist diet to minimize the overlap. A greater reliance on insectivory in Lagothrix than Ateles has been suggested to be due to microsympatry in fruit diets (Di Fiore, 1997). Aotus eats far more insects than does Callicebus. Many of the larger insects call and are active at night, making them easier to locate and confer an advantage to nocturnal insect foraging.
During periods of scarcity, Aotus was able to exploit figs and nectar producing plants, which Callicebus was not able to due to interspecific displacement by larger-bodied and larger-grouped primates. High levels of interspecific competition have also been reported between Ateles paniscus, Alouatta seniculus and Cebus apella during periods of high fruit productivity (Guillotin et al., 1994). Aotus rarely ate leaves when other higher-quality foods were available. However, in the dry forests of Paraguay where seasonally figs and other foods were scarce, Aotus did become folivorous (Wright, 1995) as well as diurnal (Wright, 1985). Diurnal increases in leaf proteins and sugars (Ganzhorn & Wright, 1994) and may explain the diurnal activity of Aotus in Paraguay as an adaptation to maximize the quality of the leaves ingested.
Avoidance of Predators
Predation has historically been a difficult subject to study due to low predator density and low chances of witnessing a predatory attack. Predation certainly does have an effect on populations but the degree to which they can cause major evolutionary responses is, in the opinion of the author, unlikely to be a major factor in determining the course of evolutionary change.
However, a case can be made for the reinforcement of nocturnality in Aotus being in part due to the benefits of avoiding predation. The assumption being made is that predation pressures are less at night in the neotropics than during the day. Wright (1995) has suggested predation by diurnal raptors is more significant than are nocturnal species. One of the significant problems with this hypothesis is the fact that while the raptors are diurnal, many other predators are nocturnal including the snakes and carnivores (Heymann, 1995). It is true that raptors rarely, if ever, prey on Aotus as the nesting sites are often inaccessible to avian predators. Threats from harpy eagles, Crested eagles, Ornate hawk-eagles and others (Robinson, 1994) are significant, but the effects on diurnal monkeys has been as yet unquantified.
Evidence to support the predation hypothesis includes the cryptic coloration of the fur and the relatively loud vocalizations used in communication which would attract predators if they were in proximity (Moynihan, 1976). Male parental care may be a defense against predation (Wright, 1984) as males tend to be more vigilant than females (van Schaik and Horstermann, 1994) but is more likely due to intraspecific defense against infanticide by solitary males and alleviation of the energetic costs of child-rearing on the mother. Cathemerality in certain populations of Aotus has been suggested to be due to the lack of diurnal predators (Wright, 1989; van Schaik and Kappeler, 1996) and the existence of large owls (Wright, 1995). This is further supported by lack of predictable sleeping sites or regular travel routes in these areas (Wright, 1995). Sleeping sites often are well-hidden, contain "escape routes" and offer a high degree of visibility (Aquino and Encarnacion, 1986).
Conclusions
Reductionist, Apollonian viewpoints as to the reasons behind nocturnality in Aotus are self-defeating. Rather, a more holistic, multi-causal explanation must be proposed if the system is to be fully understood. Many features of Aotus are adaptations to a nocturnal lifestyle but are not necessarily the reasons behind the development of the behavior. Other explanations may be important in differing degrees and not mutually exclusive of one another.
Aotus benefits from a nocturnal lifestyle through avoidance of interspecific competition and predation. Food resources are probably the most limiting factor in Aotus' reproductive success. The social system is unique in that males have a much more equal parental investment. Without a male, the female is probably completely unable to take care of the infant. Small-bodied primates require higher quality foods in their diet, being unable to effectively digest enough low-quality foods to sustain life. The important factor in competition, therefore, is over food resources. The ability to utilize and defend large concentrations of high-quality foods requires large body size, large groups or nocturnality. Aotus resides in large-crowned trees and rarely face interspecific competition, except with the occasional marsupial or one of the few other large mammals in which little if any aggression occurs (Wright, 1995). The only significant competition occurs intraspecifically, as Aotus territories often have a high degree of overlap (Wright, 1978). Very large fruiting trees often contain multiple groups of owl monkeys displaying intense agonism towards conspecifics (Wright, 1981).
Predation are probably less important than foraging pressures in determining degrees of influence as causal mechanisms by which nocturnality evolved in Aotus. Unfortunately, little quantitative work has been done to examine the intensity of predation on either the owl monkeys or their diurnal counterparts. Predation is probably rare in either nocturnal or diurnal primates. However, Aotus' hypothetically lower predation rates may be viewed as an added benefit of being nocturnal rather than an adaptive response to high diurnal predation leading to a shift in activity patterns. The evidence to either support or deny the degree by which predation influences the evolution of any population is scarce and often anecdotal. The author does not deny the potential influence of predation on primate populations, but further research needs to be done before any concrete conclusions can be inferred.
Broader-ranging implications of Aotus' lifestyle lend support to MacArthur's (1958) competitive exclusion hypothesis. Primates tend to be broadly sympatric but various life history patterns show a more specific divergence in strategies (e.g., Di Fiore, 1997). Aotus is an excellent species to examine this concept due to a high degree of diet-sharing with other primates and its highly unique activity pattern. Geographical variations on life history patterns can also be examined. Aotus, ranging across vastly different ecosystems, can yield insights into intraspecific variation in behaviors. Food choice is another important topic which can be examined using Aotus as a model. Typically frugivorous and insectivorous, Aotus is able to exploit leaves in scarce seasons and regions. How Aotus is able to subsist on low-quality foods while being a small-bodied primate suggests some interesting issues of foraging strategies as well as possible circadian cycles in leaf nutritional content (Ganzhorn and Wright, 1994). The uniqueness of Aotus' lifestyle may prove invaluable in utilizing the comparative method to discuss these broader ideas.
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