Night monkeys, also known as owl monkeys or douroucoulis[2] (), are nocturnal New World monkeys of the genus Aotus, the only member of the family Aotidae ().
The genus comprises eleven species which are found across Panama and
much of South America in primary and secondary forests, tropical
rainforests and cloud forests up to 2,400 metres (7,900 ft). Night
monkeys have large eyes which improve their vision at night, while their
ears are mostly hidden, giving them their name Aotus, meaning "earless".
Night monkeys are the only truly nocturnal monkeys with the exception of some cathemeral populations of Azara's night monkey,
who have irregular bursts of activity during day and night. They have a
varied repertoire of vocalisations and live in small family groups of a
mated pair and their immature offspring. Night monkeys have monochromatic vision which improves their ability to detect visual cues at night.
Night monkeys are threatened by habitat loss, the pet trade, hunting for bushmeat, and by biomedical research. They constitute one of the few monkey species that are affected by the often deadly human malaria protozoan Plasmodium falciparum, making them useful as non-human primate experimental subjects in malaria research. The Peruvian night monkey is classified by the International Union for Conservation of Nature (IUCN) as an Endangered species, while four are Vulnerable species, four are Least-concern species, and two are data deficient.
Taxonomy
Until 1983, all night monkeys were placed into only one (A. lemurimus) or two species (A. lemurinus and A. azarae).
Chromosome variability showed that there was more than one species in
the genus and Hershkovitz (1983) used morphological and karyological
evidence to propose nine species, one of which is now recognised as a junior synonym.[3] He split Aotus into two groups: a northern, gray-necked group (A. lemurinus, A. hershkovitzi, A. trivirgatus and A. vociferans) and a southern, red-necked group (A. miconax, A. nancymaae, A. nigriceps and A. azarae).[1] Arguably, the taxa otherwise considered subspecies of A. lemurinus – brumbacki, griseimembra and zonalis – should be considered separate species,[4][3] whereas A. hershkovitzi arguably is a junior synonym of A. lemurinus.[4] A new species from the gray-necked group was recently described as A. jorgehernandezi.[3] As is the case with some other splits in this genus,[5] an essential part of the argument for recognizing this new species was differences in the chromosomes.[3] Chromosome evidence has also been used as an argument for merging "species", as was the case for considering infulatus a subspecies of A. azarae rather than a separate species.[6] Fossil species have (correctly or incorrectly) been assigned to this genus, but only extant species are listed below.
Classification
Three-striped night monkey
Family Aotidae
- Genus Aotus
- Aotus lemurinus (gray-necked) group:
- Aotus azarae (red-necked) group:
Physical characteristics
Night
monkeys have large brown eyes; the size improves their nocturnal vision
increasing their ability to be active at night. They are sometimes said
to lack a tapetum lucidum, the reflective layer behind the retina possessed by many nocturnal animals.[7] Other sources say they have a tapetum lucidum composed of collagen fibrils.[8] At any rate, night monkeys lack the tapetum lucidum composed of riboflavin crystals possessed by lemurs and other strepsirrhines,[8] which is an indication that their nocturnalitiy is a secondary adaption evolved from ancestral diurnal primates.
Their ears are rather difficult to see; this is why their genus name, Aotus
(meaning "earless") was chosen. There is little data on the weights of
wild night monkeys. From the figures that have been collected, it
appears that males and females are similar in weight; the heaviest
species is Azara's night monkey at around 1,254 grams (2.765 lb), and the lightest is Brumback's night monkey,
which weighs between 455 and 875 grams (1.003 and 1.929 lb). The male
is slightly taller than the female, measuring 346 and 341 millimetres
(13.6 and 13.4 in), respectively.[9]
Ecology
Night monkeys can be found in Panama, Colombia, Ecuador, Peru, Brazil, Paraguay, Argentina, Bolivia, and Venezuela.
The species that live at higher elevations tend to have thicker fur
than the monkeys at sea level. Night monkeys can live in forests
undisturbed by humans (primary forest) as well as in forests that are recovering from human logging efforts (secondary forest).[9]
Distribution
A primary distinction between red-necked and gray-necked night monkeys is spatial distribution. Gray-necked night monkeys (Aotus lemurinus group) are found north of the Amazon River, while the red-necked group (Aotus azare group) are localized south of the Amazon River.[10]
Red-necked night monkeys are found throughout various regions of the
Amazon rainforest of South America, with some variation occurring
between the four species. Nancy Ma's night monkey occurs in both flooded and unflooded tropical rainforest regions of Peru, preferring moist swamp and mountainous areas.[11] This species has been observed nesting in regions of the Andes[12] and has recently been introduced to Colombia, likely as a result of post-research release into the community.[13] The black-headed night monkey is also found mainly in the Peruvian Amazon (central and upper Amazon), however its range extends throughout Brazil and Bolivia[14] to the base of the Andes mountain chain.[15]
Night monkeys such like the black-headed night monkey, generally
inhabit cloud forests; areas with consistent presence of low clouds with
a high mist and moisture content which allows for lush and rich
vegetation to grow year round, providing excellent food and lodging
sources. The Peruvian night monkey,
like Nancy Ma's night monkey, is endemic to the Peruvian Andes however
it is found at a higher elevation, approximately 800–2,400 metres
(2,600–7,900 ft) above sea level and therefore exploits different niches
of this habitat.[15] The distribution of A. azare, extends further towards the Atlantic Ocean, spanning Argentina, Bolivia and the drier, south western regions of Paraguay,[16] however unlike the other red-necked night monkey species, it is not endemic to Brazil.
Sleep sites
During
the daylight hours, night monkeys rest in shaded tree areas. These
species have been observed exploiting four different types of tree
nests, monkeys will rest in; holes formed in the trunks of trees, in
concave sections of branches surrounded by creepers and epiphytes, in
dense areas of epiphyte, climber and vine growth and in areas of dense
foliage.[17]
These sleeping sites provide protection from environmental stressors
such as heavy rain, sunlight and heat. Sleeping sites are therefore
carefully chosen based upon tree age, density of trees, availability of
space for the group, ability of site to provide protection, ease of
access to the site and availability of site with respect to daily
routines.[17]
While night monkeys are an arboreal species, nests have not been
observed in higher strata of the rainforest ecosystem, rather a higher
density of nests were recorded at low-mid vegetation levels.[17]
Night monkeys represent a territorial species, territories are defended
by conspecifics through the use of threatening and agonistic
behaviours.[18]
Ranges between night monkey species often do overlap and result in
interspecific aggressions such as vocalizing and chasing which may last
up to an hour.[10]
Diet
Night monkeys
are primarily frugivorous (fruit eating species) as fruits are easily
distinguished through the use of olfactory cues,[19] but leaf and insect consumption has also been observed in the cathemeral night monkey species A. azare.[10]
A study conducted by Wolovich et al., indicated that juveniles and
females were much better at catching both crawling and flying insects
than adult males.[20]
In general, the technique used by night monkeys in insect capturing is
to use the palm of the hand to flatten a prey insect against a tree
branch and then proceed to consume the carcass.[20] During the winter months or when food sources are reduced, night monkeys have also been observed foraging on flowers such as Tabebuia heptaphylla, however this does not represent a primary food source.[10]
Reproduction
In
night monkeys, mating occurs infrequently, however females are fertile
year-round, with reproductive cycles range from 13 to 25 days.[21]
The gestation period for night monkey is approximately 117– 159 days
but varies from species to species. Birthing season extends from
September to March and is species dependant, with one offspring being
produced per year; however, in studies conducted in captivity, twins
were observed.[21]
Night monkeys reach puberty at a relatively young age, between 7– 11
months and most species attain full sexual maturity by the age of 2
years of age. A. azare represents an exception reaching sexual maturity by the age of 4.[21]
Behavior
The name "night monkey" comes from the fact that all species are active at night and are, in fact, the only truly nocturnal monkeys (an exception is the subspecies of Azara's night monkey, Aotus azarae azarae, which is cathemeral).[9]
Night monkeys make a notably wide variety of vocal sounds, with up to
eight categories of distinct calls (gruff grunts, resonant grunts,
sneeze grunts, screams, low trills, moans, gulps, and hoots), and a
frequency range of 190–1,950 Hz.[22] Unusual among the New World monkeys, they are monochromats,
that is, they have no colour vision, presumably because it is of no
advantage given their nocturnal habits. They have a better spatial
resolution at low light levels than other primates, which contributes to
their ability to capture insects and move at night.[23] Night monkeys live in family groups consisting of a mated pair and their immature offspring. Family groups defend territories by vocal calls and scent marking.
The night monkey is socially monogamous, and all night monkeys form pair bonds.
Only one infant is born each year. The male is the primary caregiver,
and the mother carries the infant for only the first week or so of its
life. This is believed to have developed because it increases the
survival of the infant and reduces the metabolic costs on the female.
Adults will occasionally be evicted from the group by same-sex
individuals, either kin or outsiders.[24]
Nocturnality
The family Aotidae
is the only family of nocturnal species within the suborder
Anthropoidea. While the order primates is divided into prosimians; many
of which are nocturnal, the anthropoids possess very few nocturnal
species and therefore it is highly likely that the ancestors of the
family Aotidae did not exhibit nocturnality and were rather diurnal species.[25] The presence of nocturnal behavior in Aotidae
therefore exemplifies a derived trait; an evolutionary adaptation that
conferred greater fitness advantages onto the night monkey.[25]
Night monkey share some similarities with nocturnal prosimians
including low basal metabolic rate, small body size and good ability to
detect visual cues at low light levels.[26]
Their responses to olfactory stimulus are intermediate between those of
the prosimians and diurnal primate species, however the ability to use
auditory cues remains more similar to diurnal primate species than to
nocturnal primate species.[26] This provides further evidence to support the hypothesis that nocturnality is a derived trait in the family Aotidae.
As the ancestor of Aotidae was likely diurnal, selective
and environmental pressures must have been exerted on the members of
this family which subsequently resulted in the alteration of their
circadian rhythm to adapt to fill empty niches.[25] Being active in the night rather than during the day time, gave Aotus
access to better food sources, provided protection from predators,
reduced interspecific competition and provided an escape from the harsh
environmental conditions of their habitat.[19] To begin, resting during the day allows for decreased interaction with diurnal predators. Members of the family Aotidae, apply the predation avoidance theory, choosing very strategic covered nests sites in trees.[27]
These primates carefully choose areas with sufficient foliage and vines
to provide cover from the sun and camouflage from predators, but which
simultaneously allow for visibility of ground predators and permit
effective routes of escape should a predator approach too quickly.[19][17]
Activity at night also permits night monkeys to avoid aggressive
interactions with other species such as competing for food and
territorial disputes; as they are active when most other species are
inactive and resting.[19]
Night monkeys also benefit from a nocturnal life style as
activity in the night provides a degree of protection from the heat of
the day and the thermoregulation difficulties associated.[27]
Although night monkey, like all primates are endothermic, meaning they
are able to produce their own heat, night monkeys undergo behavioural
thermoregulation in order to minimize energy expenditure.[27]
During the hottest points of the day, night monkeys are resting and
therefore expending less energy in the form of heat. As they carefully
construct their nests, night monkeys also benefit from the shade
provided by the forest canopy which enables them to cool their bodies
through the act of displacing themselves into a shady area.[27]
Additionally, finding food is energetically costly and completing this
process during the day time usually involves the usage of energy in the
form of calories and lipid reserves to cool the body down. Foraging
during the night when it is cooler, and when there is less competition,
supports the optimal foraging theory; maximize energy input while
minimizing energy output.[27]
While protection from predators, interspecific interactions, and
the harsh environment propose ultimate causes for nocturnal behavior as
they increase the species fitness, the proximate causes of nocturnality
are linked to the environmental effects on circadian rhythm.[28]
While diurnal species are stimulated by the appearance of the sun, in
nocturnal species, activity is highly impacted by the degree of moon
light available. The presence of a new moon has correlated with
inhibition of activity in night monkeys who exhibit lower levels of
activity with decreasing levels of moon light.[28] Therefore, the lunar cycle has a significant influence on the foraging and a nocturnal behaviors of night monkey species.[28]
Pair-bonded social animals (social monogamy)
Night
monkeys are socially monogamous—they form a bond and mate with one
partner. They live in small groups consisting of a pair of reproductive
adults, one infant and one to two juveniles.[29]
These species exhibit mate guarding, a practice in which the male
individual will protect the female he is bonded to and prevent other
conspecifics from attempting to mate with her.[30]
Mate guarding likely evolved as a means of reducing energy expenditure
when mating. As night monkey territories generally have some edge
overlap, there can be a large number of individuals coexisting in one
area which may make it difficult for a male to defend many females at
once due to high levels of interspecific competition for mates.[31] Night monkeys form bonded pairs and the energy expenditure of protecting a mate is reduced.[30]
Pair bonding may also be exhibited as a result of food distribution. In
the forest, pockets of food can be dense or very patchy and scarce.
Females, as they need energy stores to support reproduction are
generally distributed to areas with sufficient food sources.[32]
Males will therefore also have to distribute themselves to be within
proximity to females, this form of food distribution lends itself to
social monogamy as finding females may become difficult if males have to
constantly search for females which may be widely distributed depending
on food availability that year.[32]
However, while this does explain social monogamy, it does not
explain the high degree of paternal care which is exhibited by these
primates. After the birth of an infant, males are the primary carrier of
the infant, carrying offspring up to 90% of the time.[29]
In addition to aiding in child care, males will support females during
lactation through sharing their foraged food with lactating females.[33]
Generally, food sharing is not observed in nature as the search for
food requires a great degree of energy expenditure, but in the case of
night monkey males, food sharing confers offspring survival advantages.
As lactating females may be too weak to forage themselves, they may lose
the ability to nurse their child, food sharing therefore ensures that
offspring will be well feed.[33]
The act of food sharing is only observed among species where there is a
high degree of fidelity in paternity. Giving up valuable food sources
would not confer an evolutionary advance unless it increased an
individual's fitness; in this case, paternal care ensures success of
offspring and therefore increases the father's fitness.[33]
Olfactory communication and foraging
Recent
studies have proposed that night monkeys rely on olfaction and
olfactory cues for foraging and communication significantly more than
other diurnal primate species.[20]
This trend is reflected in the species physiology; members of Aotidae
possess larger scent perception organs than their diurnal counterparts.
The olfactory bulb, accessory olfactory bulb and volume of lateral
olfactory tract are all larger in Aotus than in any of the other new world monkey species.[34]
It is therefore likely that increased olfaction capacities improved the
fitness of these nocturnal primate species; they produced more
offspring and passed on these survival enhancing traits.[34]
The benefits of increased olfaction in night monkeys are twofold;
increased ability to use scent cues has facilitated night time foraging
and is also an important factor in mate selection and sexual
attractivity.[20]
As a substantial portion of the night monkey's activities
occurring during the dark hours of the night, there is a much lower
reliance of visual and tactile cues. When foraging at night, members of
the family Aotidae will smell fruits and leaves before ingesting to
determine the quality and safety of the food source. As they are highly
frugivorous and cannot perceive colour well, smell becomes the primary
determinant of the ripeness of fruits and is therefore an important
component in the optimal foraging methods of these primates.[34]
Upon finding a rich food source, night monkeys have been observed scent
marking not only the food source, but the route from their sleeping
site to the food source as well. Scent can therefore be used as an
effective method of navigation and reduce energy expenditure during
subsequent foraging expeditions.[34]
Night monkeys possess several scent glands covered by greasy hair
patches, which secrete pheromones that can be transferred onto
vegetation or other conspecifics. Scent glands are often located
subcaudal, but also occur near the muzzle and the sternum.[20]
The process of scent marking is accomplished through the rubbing of the
hairs covering scent glands onto the desired “marked item”.
Olfactory cues are also of significant importance in the process
of mating and mate guarding. Male night monkeys will rub subcaudal
glands onto their female partner in a process called “partner marking”
in order to relay the signal to coexisting males that the female is not
available for mating.[20]
Night monkeys also send chemical signals through urine to communicate
reproductive receptivity. In many cases, male night monkeys have been
observed drinking the urine of their female mate; it is proposed that
the pheromones in the urine can indicate the reproductive state of a
female and indicate ovulation.[20]
This is especially important in night monkeys as they cannot rely on
visual cues, such as the presence of a tumescence, to determine female
reproductive state.[20]
Therefore, olfactory communication in night monkeys is a result of
sexual selection; sexually dimorphic trait conferring increased
reproductive success. This trait demonstrates sexual dimorphism, as
males have larger subcaudal scent glands compare to female counterparts
and sex differences have been recorded in the glandular secretions of
each gender.[35]
There is a preference for scents of a particular type; those which
indicate reproductive receptivity, which increases species fitness by
facilitating the production of offspring.[35]
Conservation
According to the IUCN (the International Union for Conservation of Nature), the Peruvian night monkey is classified an Endangered species, four species are Vulnerable, four are Least-concern species,
and two are data deficient. Most night monkey species are threatened by
varying levels of habitat loss throughout their range, caused by agricultural expansion,
cattle ranching, logging, armed conflict, and mining operations. To
date, it is estimated that more than 62% of the habitat of the Peruvian night monkey has been destroyed or degraded by human activities.[12]
However, some night monkey species have become capable of adapting
exceptionally well to anthropogenic influences in their environment.
Populations of Peruvian night monkey have been observed thriving in
small forest fragments and plantation or farmland areas, however this is
likely possible given their small body size and may not be an
appropriate alternate habitat option for other larger night monkey
species.[12]
Studies have already been conducted into the feasibility of
agroforestry; plantations which simultaneously support local species
biodiversity.[36] In the case of A. miconax,
coffee plantations with introduced shade trees, provided quality
habitat spaces. While the coffee plantation benefited from the increased
shade—reducing weed growth and desiccation, night monkeys used the
space as a habitat, a connection corridor or stepping stone area between
habitats that provided a rich food source.[36]
However, some researchers question the agroforestry concept,
maintaining that monkeys are more susceptible to hunting, predator and
pathogens in plantation fields, thus indicating the need for further
research into the solution before implementation.[36]
Night monkeys are additionally threatened by both national and
international trade for bushmeat and domestic pets. Since 1975, the pet
trade of night monkeys has been regulated by CITES (the Convention on
International Trade in Endangered Species). In the last forty years,
nearly 6,000 live night monkeys and more than 7,000 specimens have been
traded from the nine countries which they call home. While the
restrictive laws put into place by CITES are aiding in the reduction of
these numbers, 4 out of 9 countries, show deficiencies in maintaining
the standards outlined by CITES[13] Increased attention and enforcement of these laws will be imperative for the sustainability of night monkey populations.
Use in biomedical research poses another threat to night monkey biodiversity. Species such as Nancy Ma's night monkey, like human beings, are susceptible to infection by the Plasmodium falciparum parasite responsible for malaria.[37]
This trait caused them to be recommended by the World Health
Organization as test subjects in the development of malaria vaccines.[38]
Up to 2008, more than 76 night monkeys died as a result of vaccine
testing; some died from malaria, while others perished due to medical
complications from the testing.[39]
Increased research and knowledge of night monkey ecology is an
invaluable tool in determining conservation strategies for these species
and raising awareness for consequences of the anthropogenic threats
facing these primates. Radio-collaring of free ranging primates proposes
a method of obtaining more accurate and complete data surrounding
primate behavior patterns. This in turn can aid in understanding what
measures need to be taken to promote the conservation of these species.[40]
Radio collaring not only allows for the identification of individuals
within a species, increased sample size, more detailed dispersal and
range patterns, but also facilitates educational programs which raise
awareness for the current biodiversity crisis.[40]
The usage of radio-collaring while potentially extremely valuable, has
been shown to interfere with social group interactions, the development
of better collaring techniques and technology will therefore be
imperative in the realisation and successful use of radio collars on
night monkeys.[40]
Common Squirrel Monkey Range Map
