aotus nocturnality

7/25/2019 Aotus Nocturnality

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Nocturnality in the Owl Monkey, Aotussp.

Jonathan Greenberg

3 December 1997


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Introduction

Aotussp., the owl monkey, is the worlds 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), Aotushas markedly different lifestyle strategies. Morphology, geographical and

habitat distribution, social system and diet all factor into the explanations of the development of

nocturnality onAotus. 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 Aotusand 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

Aotussp. 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).Aotuscoats 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


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large and lack cones but contain a fovea, suggesting the ancestor of Aotuswas a diurnal monkey

(Napier & Napier, 1996). Aotusis 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 Aotushave

true nails, two of which are possibly a grooming nail on the toes similar to those found in

prosimians (Wright, 1985). Aotushas 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 ofAotusare large (Hunter et al., 1984) and olfaction is

well-developed when compared to other Neotropical primates (Bolen and Green, 1997).

Taxonomy

Aotussp. (Family Cebidae, Subfamily Aotinae) is most closely related to the titi monkeys

(Callicebussp.). 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

Aotusmay 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 ofAotus 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


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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).

Aotussleeps 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 Coendousp.

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 -5C

(Wright, 1995).

Social System

Aotusis 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


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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).

Aotusis 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 Aotusis relatively sedentary (Charles-Dominique, 1977). This is supported by

Isbells (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).

Aotusis a relatively noisy monkey, uttering loud contact and locomotory notes (Moynihan,1976). Olfaction is an important component of communication and Aotusmarks substrates by

rubbing a gland at the base of its tail and exuding a brown, oily substance (Wright, 1981).

Diet


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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. Aotusfeeds 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 inAotus. The seeds pass unharmed through the gut (Wright, 1985)

which may suggestAotusis 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 Aotuscontained

insect parts, compared to less than one-fifth for Callicebus(Wright, 1985). Aotuspreys 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,Aotuscaptures insects during

methodical movements along branches and catching them on the branches or in the air (Wright,

1985).


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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, andAotus

rarely leaves the trees. Felids do pose a threat, though Wright (1985) has suggested Aotusare

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).

Aotusis 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 whichto 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


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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 saveLemur cattaare predatory (Petter, 1962).

Three Hypotheses for the Development of Nocturnality in Aotus

Aotusshares all of the aforementioned characteristics of nocturnal animals. However, the

question of why nocturnality is beneficial to the owl monkeys 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, Aotusdoes 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. Aotushas 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 whichmay 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 Callicebusif

found feeding. There have been reports of Ateles paniscus, Cebus apellaand Cebus albifrons

displacing smaller primates from feeding sites. Saimiri uses large group size to prevent


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interspecific displacement by larger primates from becoming effective at keeping them out of larger

fruiting trees. Unlike Saimiri, Callicebusdoes 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 Saimiriand Cebus. Aotusprefers 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 ofAotusin this habitat.

Aotusare displaced byDidelphis sp. (opossum), P. flavius, and Bassaricyonsp. 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, Aotusis 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 sympatricspecies (MacArthur, 1958). Aotususes 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). Aotuseats far more insects


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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, Aotuswas able to exploit figs and nectar producing plants,

which Callicebuswas not able to due to interspecific displacement by larger-bodied and larger-

grouped primates. High levels of interspecific competition have also been reported betweenAteles

paniscus , Alouatta seniculus and Cebus apella during periods of high fruit productivity

(Guillotin et al., 1994). Aotusrarely 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 Aotusin

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 Aotusbeing 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

onAotusas 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.


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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 Aotushas

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 ofAotusare 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.

Aotusbenefits 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-qualityfoods 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. Aotusresides in large-crowned trees and rarely face interspecific

competition, except with the occasional marsupial or one of the few other large mammals in which


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little if any aggression occurs (Wright, 1995). The only significant competition occurs

intraspecifically, asAotusterritories 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,Aotushypothetically 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 anypopulation 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 MacArthurs (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). Aotusis 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 usingAotus

as a model. Typically frugivorous and insectivorous, Aotusis able to exploit leaves in scarce

seasons and regions. How Aotusis 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 ofAotuslifestyle

may prove invaluable in utilizing the comparative method to discuss these broader ideas.


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