Activity Patterns, Diet and Home Range of Night Monkeys (Aotus griseimembra and Aotus lemurinus) in Tropical Lowland and Mountain Forests of Central Colombia

Abstract

Most primates live in lowland ecosystems; however, some species have been particularly successful at colonizing higher altitudes, such as night monkeys (genus Aotus). Studies of the ecology of night monkeys in tropical forests are numerous, but behavioral data are limited due to the challenges associated with their nocturnal habits. Although Andean night monkeys (A. lemurinus) live in mountain forests >1000 m.a.s.l. and Caribbean night monkeys (A. griseimembra) live in rainforests <1000 m.a.s.l., they are found at similar tropical latitudes. Between 2018 and 2019, we followed three groups of A. lemurinus and one group of A. griseimembra at three sites in Colombia and recorded data on their ecology and behavior. Although they live at different altitudes, the two species had similar activity patterns and diet, investing approximately half of the night in resting (48%), and feeding primarily on fruits. We found differences among groups in the time invested in feeding on flowers, their home range, and distance traveled per night. These differences may be related to the unique characteristics of each study site and differences in resource availability and floristic composition of forests at different altitudes. Although the most important families in their diet were Moraceae and Urticaceae, highland groups also fed frequently on a large number of Melastomataceae and Rubiaceae trees. This research suggests these two nocturnal primates, living in contrasting environments, use similar strategies to cope with the challenges of being active at night in tropical forests.

Full text

Activity Patterns, Diet and Home Range of Night
Monkeys (Aotus griseimembra and Aotus lemurinus)
in Tropical Lowland and Mountain Forests of Central
Colombia
Sebastián O. Montilla, et al. [full author details at the end of the article]
Received: 4 July 2020 /Accepted: 30 November 2020/
#The Author(s), under exclusive licence to Springer Science+Business Media, LLC part of Springer Nature 2021
Abstract
Most primates live in lowland ecosystems; however, some species have been particu-
larly successful at colonizing higher altitudes, such as night monkeys (genus Aotus).
Studies of the ecology of night monkeys in tropical forests are numerous, but behav-
ioral data are limited due to the challenges associated with their nocturnal habits.
Although Andean night monkeys (A. lemurinus) live in mountain forests >1000
m.a.s.l. and Caribbean night monkeys (A. griseimembra) live in rainforests <1000
m.a.s.l., they are found at similar tropical latitudes. Between 2018 and 2019, we
followed three groups of A. lemurinus and one group of A. griseimembra at three sites
in Colombia and recorded data on their ecology and behavior. Although they live at
different altitudes, the two species had similar activity patterns and diet, investing
approximately half of the night in resting (48%), and feeding primarily on fruits. We
found differences among groups in the time invested in feeding on flowers, their home
range, and distance traveled per night. These differences may be related to the unique
characteristics of each study site and differences in resource availability and floristic
composition of forests at different altitudes. Although the most important families in
their diet were Moraceae and Urticaceae, highland groups also fed frequently on a large
number of Melastomataceae and Rubiaceae trees. This research suggests these two
nocturnal primates, living in contrasting environments, use similar strategies to cope
with the challenges of being active at night in tropical forests.
Keywords Altitudinalgradient.Behavior.Feeding.Nocturnality.Tropicalforests.Use of
space
Introduction
Although most extant primates live in lowland ecosystems, a few taxa—in all four
major primate clades—have been particularly successful at colonizing higher altitudes
International Journal of Primatology
https://doi.org/10.1007/s10764-020-00192-1
Handling Editor: Joanna Setchell

(Grow et al.2014). As elevation increases from sea level to high-altitude ecosystems
(e.g., cloud forests in America), other environmental variables including temperature
and sunlight intensity, also vary (Körner 1989). This variation in mean temperature,
coupled with high fluctuation in daily temperatures and other climatic factors, is
associated with lower tree diversity, forest structure, and resource availability
(endozoochorous fruits) in mountain forests (Buitrón-Jurado and Ramírez 2014;
Schmitt et al.2010). Thus, primates that have been able to colonize and adapt to
high-altitude ecosystems have presumably evolved higher dietary flexibility (Hanya
et al.2003;Rothmanet al.2014;Xianget al.2007,2012) to cope with these harsh
environments. Most primates at higher altitudes tend to be dietary generalists,and some
have adapted behaviorally to regulate their activity—and even hibernate—under low
temperatures (Blanco and Rahalinarivo 2010).
In the Americas, only a few primate species are found at high altitudes including red
howler monkeys (Alouatta seniculus), woolly monkeys (Lagothrix lagothricha), large-
headed capuchins (Sapajus macrocephalus), and several species of night monkeys
(Aotus spp.) (Defler 2010;Growet al.2014). Of these, night monkeys are the only
haplorhine primate that is active primarily at night. They are a diverse genus with at
least 11 species and have one of the broadest geographic ranges among extant
American primates, being currently distributed from Panama to the north of Argentina
and from the Pacific coast of Ecuador and Colombia to the Atlantic forests of Brazil
(Defler 2010;DeflerandBueno2007; Fernandez-Duque et al.2013;Rylandset al.
2012). Furthermore, night monkeys are found in a broad altitudinal range that includes
tropical dry forests and rainforests in the lowlands (from sea level) to Andean forests
above 3000 m.a.s.l. (Defler 2010; Fernandez-Duque et al.2013; Shanee et al.2015).
Finally, night monkeys are a very adaptable genus that lives in relatively undisturbed
ecosystems but can also cope with significant levels of habitat fragmentation and
degradation (Castaño and Cardona 2005;Castañoet al.2010; Defler 2010;Montilla
et al.2018). Night monkeys are relatively poorly studied when compared to some other
American primates (García-R et al.2018; Stevenson et al.2010). Most of our under-
standing of night monkeys in the wild comes from a long-term study of Aotus azarae in
the subtropical forests of northern Argentina (Fernandez-Duque 2003; Fernandez-
Duque and van der Heide 2013; Fernandez-Duque et al.2010; Rotundo et al.2005;
Wartmann et al.2014). Numerous studies describe tropical night monkey ecology, but
data on their behavior are limited given the practical difficulties of following and
recording data on nocturnal primates (Aquino and Encarnación 1986;Bicca-Marques
and Garber 2004; Castaño et al.2010;Fernandez-Duqueet al.2008;GarcíaandBraza
1987; Guzmán et al.2016; Khimji and Donati 2014; Puertas et al.1992; Shanee et al.
2013;Wright1978).
Northern South America contains the highest diversity of species of night monkeys,
among which are the Andean night monkey (Aotus lemurinus) and the Caribbean night
monkey (A. griseimembra). Both species are categorized as Vulnerable (VU) by the
International Union for Conservation of Nature (IUCN) due to habitat destruction as a
result of deforestation and landscape transformation into agricultural fields (Link et al.
2019; Morales-Jiménez and de la Torre 2008). These two species are considered cryptic
taxa because they are almost indistinguishable through morphological characteristics
and have adjacent trans-Andean geographic distributions. However, they appear to
inhabit tropical ecosystems with different environmental conditions (Defler 2010).
Montilla S. et al.

A. lemurinus inhabits Andean forests in Colombia, Ecuador, and Venezuela between
1000 and 3200 m.a.s.l, while A. griseimembra inhabits tropical rainforests in Colombia
and Venezuela between sea level and 1000 m.a.s.l. (Defler 2010; Link et al.2019;
Morales-Jiménez and de la Torre 2008). Both species (previously considered subspe-
cies of A. lemurinus) were first studied in captive conditions, and such studies provided
valuable information on their chronobiology (Erkert 1991; Erkert and Grober 1986)
and reproductive behavior (Dixson and Fleming 1981). However, studies on the
ecology in wild A. lemurinus are scant (Castaño et al.2010; Guzmán et al.2016)—
and nonexistent to our knowledge—for A. griseimembra.
We describe basic aspects of the behavioral ecology (activity patterns, diet, home
range and traveled distance per night) of three groups of Aotus lemurinus in two
highland forests in the Central and Eastern Andes Cordilleras, and one group of
A. griseimembra, in the lowland rainforests of the middle Magdalena River basin, in
Colombia. We aimed to provide novel data on their ecology and behavior to underpin
future studies of more complex questions associated with the evolution of nocturnality.
Methods
Study Areas and Groups
This study took place at three sites in two different tropical ecosystems in Colombia:
the Andean mountain forests and the lowland rainforests between the Andes Cordilleras
(Fig. 1;TableI). In the Andean forests, we followed three groups of Aotus lemurinus at
two different sites: 1) El Colegio (groups CO1): A forest in a departmental protected
area called Distrito de Manejo Integrado Cuchilla de Peñas Blancas y el Subia in El
Colegio municipality, Cundinamarca (4°33′18″N, 74°22′26″O).Thissiteisconsidered
a secondary forest with a regeneration process that dates from 1993, when it was
declared as a protected area. Since then, the reduction of anthropogenic pressures has
allowed the natural recovery of degraded areas that are surrounded by mature Andean
forests. 2) Pijao (groups PI1, PI2): a small forest fragment in an Andean forest located
on El Billar farm in Pijao municipality, Quindío (4°19′58″N, 75°42′39″O). This forest
fragment is part of a mosaic of small fragments of forests and agricultural fields and
limits with plantations of plantain, coffee and avocado.
In the lowland rainforest in central Colombia, we studied one group of Aotus
griseimembra (group SJ1). The forest fragment comprises a seasonally flooded forest
on the northwestern bank of the San Juan River, on the private cattle farm of San Juan
del Carare, Cimitarra municipality, Santander (6°42′59″N, 74°08′22″O). This fragment
is part of a mosaic of small forest fragments and grasslands used for livestock and
naturally flooded savannahs.
The three sites have a bimodal annual pattern of precipitation with two seasons of
peak rains (March–May and September–November) and two drier seasons (December–
February and June–August).
At El Colegio, our single study group (CO1) was composed of an adult male (with a
telemetry collar), an adult female, a subadult male that left the group in July 2019, and
another subadult of unidentified sex. At Pijao, group PI1 was composed of an adult
male, an adult female, a subadult male, a subadult female, and an unidentified infant
Activity Patterns, Diet and Home Range of Night Monkeys (Aotus...

born in July 2019. Group PI2 was composed of an adult male (with a telemetry collar),
an adult female, a subadult female, and an unidentified infant born in March 2019.
Finally, group SJ1 at San Juan del Carare was composed of an adult male, an adult
female (with a telemetry collar), a subadult female that left the group in September
2018, and an infant of unidentified sex born in the same month (Table I). We were able
to sex the adult pair in all groups because we placed a collar on at least one of them,
observed copulations and sexual behavior between them, and because offspring were
born in all groups during the study. The age of the individuals was determined based on
their size and by the development of a subcaudal spot at the ventral base of the tail,
which is larger and more defined in adult individuals (Castaño et al.2010). All four of
our study groups were habituated to our presence, given that we had started following
them (several nights per week) at least 6 mo before the start of data collection, and
Fig. 1 Sites where we studied night monkeys in central Colombia. We studied A. lemurinus in Andean
mountain forests at El Colegio (yellow circle) and Pijao (red circle). We studied A. griseimembra in the
lowland rainforest at San Juan del Carare (blue circle).
Montilla S. et al.

Table I Characteristics of the study sites and study groups of two species of night monkey in central Colombia between 2018 and 2019
Site Ecosystem Species Altitude
(m.a.s.l)
Size of
forest (ha)
Annual
precipitation (mm)
Annual mean
temperature (°C)
Annual mean
relative
humidity (%)
Group No. of
individuals
Group composition
El Colegio Andean
mountain
forests
Aotus
lemurinus
2350–2550 60 1400 12–18 87 CO1 4 1AM,1AF,1SAM,
1SXX
Pijao Andean
mountain
forests
Aotus
lemurinus
1750–1800 6 1400 18–25 84 PI1 5 1AM,1AF,1SAM,
1SAF,1IX
PI2 4 1AM,1AF,1SAF,
1IX
San Juan del Carare lowland
rainforests
Aotus
griseimembra
90–150 30 3458 24–34 82 SJ1 5 1AM,1AF,1SAF,
1JF,1IX
Activity Patterns, Diet and Home Range of Night Monkeys (Aotus...

throughoutthe study we could followthem during the entire night and often they would
come close (<5 m) to us while foraging or moving.
Age and sex categories: AF = adult female; AM = adult male; JF = juvenile female;
SAF = subadult female; SAM = subadult male; SAX = subadult sex undetermined; XX
= sex and age undetermined.
Data Collection
We used direct behavioral follows during the entire night when weather conditions
allowed. We attempted to follow the groups 2–5 nights per week, from 18:00 to 06:00
h. We recorded behavioral data on CO1, PI1, and PI2 from July 2018 to July 2019, and
from January 2018 to May 2019 for SJ1 (Table II). For SJ1, sampling was not
continuous because the forest remained flooded for several months of the year, which
prevented us from following the study group continuously throughout the year.
To overcome some of the inherent challenges of following monkeys during the night
and collect behavioral data effectively, we used telemetry signals emitted by VHF radio
collars (MOD-80 radiocollars-Telonics) fitted to an adult individual in groups CO1,
Table II Sampling effort during a study of the behavioral ecology of tropical night monkeys at three sites in
Colombia between 2018 and 2019
Month–
year
CO1 PI1 PI2 SJ1
Contact
hours
No. of focal
samples
Contact
hours
No. of focal
samples
Contact
hours
No. of focal
samples
Contact
hours
No. of focal
samples
Jan–18 —— —— —— 21.5 —
Feb–18 —— —— —— 51.9 20
Mar–18 —— —— —— 94.2 61
Apr–18 —— —— —— 13.2 6
May–18 —— —— —— ——
June–18 —— —— —— 20.0 3
July–18 39.5 2 4.1 1 1.1 —16.0 3
Aug–18 101.9 96 33.0 14 1.6 1 32.0 37
Sept–18 113.4 86 51.2 37 35.1 20 47.1 82
Oct–18 61.8 50 40.5 50 50.9 53 13.6 24
Nov–18 68.2 56 44.3 39 68.0 39 25.8 44
Dec–18 19.5 15 23.4 17 25.5 17 54.3 82
Jan–19 52.1 48 76.1 52 23.4 23 16.4 26
Feb–19 137.1 108 52.7 33 66.8 71 4.1 10
Mar–19 168.8 115 59.8 60 71.6 83 13.2 22
Apr–19 79.5 52 76.0 50 58.9 64 20.7 40
May–19 128.4 77 43.2 30 58.9 51 2.2 2
June–19 79.0 42 74.4 74 87.7 128 ——
July–19 11.6 2 4.9 6 12.0 21 ——
Total 1060 749 583 463 561 571 446 462
Montilla S. et al.

PI2, and SJ (but not in group PI1 because we did not capture this group). To capture the
animals, we administered 0.5-ml darts loaded with controlled doses of Zoletil (50
mg/ml) (Zolazepam and Tiletamine) using a veterinary rifle following methods in
Fernandez-Duque and Rotundo (2003). We conducted all captures during daytime near
the sleeping sites of our study groups, released monkeys in the same location, and
monitored them until they rejoined their group. All captured individuals recovered well
and returned to their corresponding groups a few hours after immobilization.
While observing night monkeys during the night (18:00–06:00 h), we used flash-
lights wrapped with red cellophane paper that minimizes interference with the mon-
key’s activity due to artificial light, and binoculars (Nikon Monarch 7-10x42). We
began observations when the study group came out from their sleeping site and
continued throughout the night until they returned to their sleeping site. To record
comparable data on activity patterns, diet, home range size, and traveled distance per
night of each group, we collected data using a standardized behavioral sampling
protocol complemented with ad libitum observations. We recognized individuals by
the presence or absence of the collar, their size, and the development of the subcaudal
spot. Behavioral observations were made simultaneously by teams of two researchers.
One researcher recorded data and both observed the study animals to avoid losing them
and to obtain reliable data on their diet, behavior, and activity. All field assistants were
trained by other more experienced team members in one of our study areas to reduce
observational bias between study sites during the study and overlapped with other
assistants to identify group members during data collection.
Activity Patterns
We conducted 20-min focal samples on all adults or subadults and recorded the focal
animal’s behavior every 2 min through instantaneous records (Altmann 1974). We
attempted to conduct as many 20-min focal samples per night as possible, rotating
sampling among the group members and attempting to balance sampling effort across
them. For each 2-min instantaneous record we recorded the following exclusive
activities: 1) feeding, 2) moving, 3) resting, 4) social interactions, 5) other activities,
and 6) out of view (Table III). We determined the percentage of time devoted to each
activity (excluding “out of view”records) for each individual and estimated the mean
for all adult and subadult individuals in each study group. We pooled activity records
into biweekly periods to compare patterns of activity among the groups of night
monkeys studied.
Diet
To describe the diet and feeding behavior of each group of night monkeys, we extracted
data (instantaneous records) from the focal samples that included “feeding”and
classified them into the following feeding items: 1) fruits, 2) arthropods, 3) leaves, 4)
flowers, 5) other, and 6) unidentified items. We determined the percentage of con-
sumption of each item for each individual then calculated the mean for the group using
these data. Given the high variability in resource availability throughout the year in
tropical ecosystems, we divided all feeding records into biweekly periods to compare
the diet among the groups of night monkeys studied. We also estimated the proportion
Activity Patterns, Diet and Home Range of Night Monkeys (Aotus...

of feeding items in the monthly diet of night monkeys and analyzed temporal variations
in the diet excluding months with fewer than five feeding records per group.
To determine the relative contribution of plant species to night monkeys’diet, we
recorded the initial and final time when night monkeys fed from a tree or a liana and
calculated the bout duration in minutes. During all feeding records on trees and lianas,
we marked the feeding source with flagging tape and a metal plate with a unique code
and collected specimens for botanical identification (Rivera-Díaz et al.2012;Vargas
2002). We compared these specimens with botanical material deposited in collections
at Herbario de la Universidad del Quindío (HUQ), Museo de Historia Natural Jaime
Quijano Caballero de la Universidad INCCA de Colombia (Museo JQC), Herbario de
la Universidad El Bosque (HUEB), and Herbario de la Universidad de Caldas (FAUC).
Finally, based on all feeding events recorded in the study we calculated the percent of
each dietary item in the diet of each species as follows:
Percentage of diet ¼ni
N

100
where ni corresponds to the time (in seconds) each plant species or morpho-species was
consumed, and Ncorresponds to the sum of feeding times for all plant species that each
group consumed during the study.
Home Range and Core Area
We recorded spatial data every 15 min using a hand-held GPS (Garmin e-trex 10),
starting from 18:00 h and throughout the night. We took these data just under the tree
where the night monkeys were observed. From these records, we estimated the home
range (90% kernel) and core area (50% kernel), using kernel density estimations in the
adeHabitatHR package in R (Calenge 2006; R Core Team 2018). We used the
bandwidth href as the smoothing parameter, which takes into account variation in the
xand ycoordinates and is not sensitive to large data sets with multiple observations,
unlike other smoothing methods (Hemson et al.2005;Kieet al.2010). To reduce
Table III Ethogram of activities we recorded for two species of tropical night monkeys in Colombia between
2018 and 2019
Activities Description
Feeding An animal is searching for, manipulatingor ingesting part of a plant (fruits, leaves, flowers, or
others) or when it is actively looking for arthropods.
Moving When an evident change of position occurred, either within the same tree or among
neighboring trees in the forest canopy.
Resting The animal remained still, resting with eyes open or closed.
Social
interaction
The animal engaged in social behavior with a conspecific or visitor. Includes grooming,
playing, aggression, and copulation.
Others Activities other than the above, including defecation, scratching, displaying to the observer.
Out of view When the animal is not observed or the activity is not clear.
Montilla S. et al.

biases due to differences in sampling intensity across study groups and to compare their
home ranges and core areas, we chose subsets of 1000 random locations for groups
CO1, PI1, and PI2 and compared these with the 958 locations recorded for SJ1: the
group with the lowest number of location records. In addition, we estimated the home
range for each of the groups from these same subsets of locations, using the minimum
convex polygon (MCP) method.
Distance Traveled per Night
To estimate the horizontal distance traveled per night by night monkeys, we
estimated the distance covered by the group each hour of the night by summing
the distances between subsequent 15-min location records. Thus, we grouped all
location records into 12 intervals corresponding to the hours of the night: from
18:00–19:00 h to 05:00–06:00 h. For incomplete night follows (those <12 h)
we estimated traveled distances for hours with complete sampling. Subsequent-
ly, we estimated the distance traveled during each 1-h interval using the X-
Tools Pro extension in ArcGIS 9.3 (ESRI 2018). This method underestimates
total distance traveled and ignores the monkey´s movement between sampling
records. Finally, we estimated a mean distance for each hourly interval using all
the nights of monitoring. We determined the distance traveled per night for
each group as the sum of the mean values of the 12 time intervals.
Statistical Analysis
We used biweekly data to compare activity patterns and diet between groups.
We first evaluated the normality of variables using Shapiro–Wilks tests and
homogeneity of variance by inspecting residual plots. Based on the results, we
used a one-way ANOVA test to evaluate differences between groups in the
biweekly percentage of time invested in resting, moving, and feeding activities.
We used a post hoc Tukey’s Honestly Significant Difference (HSD) test for
differences between group dyads when the one-way ANOVA test was signifi-
cant. We did not include “social interaction”in analysis, as it accounted for
only a small percentage of biweekly activity patterns in all four study groups.
To evaluate diet and feeding patterns in night monkeys we used a nonparamet-
ric Kruskal–Wallis test, because these variables were not normally distributed,
and a post hoc Bonferroni test correction to test differences between group
dyads when the Kruskal–Wallis test was significant. We excluded all biweekly
periods with fewer than 10 focal samples. We performed all analyses in R 3.6.1
(R Core Team 2018).
Ethical Note
This research complies with principles of animal use of the Institutional Committee for
Care and Use of Laboratory Animals of the Universidad de los Andes (CICUAL) and
adhered to the American Society of Primatologists' Principles for the Ethical Treatment
of Primates. The authors declare that they have no conflict of interest.
Activity Patterns, Diet and Home Range of Night Monkeys (Aotus...

Data Availability The data sets during and/or analyzed during the current study avail-
able from the corresponding author on reasonable request.
Results
Overall, we obtained 2650 h of observation across the four groups of night monkeys
(Table II).
Activity Patterns
Based on 2245 activity records (Table II), we found that all four study groups
spent most of their time resting (48.3% ± SD 6.7%, N=4) (Fig. 2) (Electronic
Supplementary Material [ESM] Table SI). For groups CO1, PI2, and SJ1, the
second most frequent activity was moving (27.7% ± SD 1.6%, N=3) and the
thirdwasfeeding(20.5±SD4.4%,N=3), while for the group PI1, the
second most frequent activity was feeding (33.5%) and the third was moving
(25.6%). Social interaction and other activities accounted for less than 1% of
sampling time in all groups.
We found no significant differences in the proportion of time groups spent moving,
based on biweekly percentages of time spent, but we found significant differences in
the proportion of time spent resting and feeding (Table IV). Particularly for time spent
resting, differences were driven by the lower percentage of time spent resting by PI1
group—the only group without a VHF radiocollar—compared to the other groups
(Table IV). PI1 also spent more time feeding than other groups and CO1 fed more than
SJ1 (Table IV).
Diet
Overall, we recorded 1118 feeding records: 395 from CO1, 287 from PI1, 223
from PI2, and 213 from SJ1 (ESM Table SII). All groups of night monkeys
spent two-thirds of their time feeding on fruits (63.5% ± SD 2.4%, N=4)
(Fig. 3). Arthropods were the second most consumed feeding item in the four
groups (15.6% ± SD 2.2%, N=4). Flowers were the third most consumed item
by the two groups at Pijao (PI1 11.6% and PI2 11.0%), and flowers represented
8.1% of total consumption in SJ1, while accounting only for 0.7% in CO1.
“Other”feeding items, including those that we could not classify, represented
less than 4% of their overall diet in the four study groups. Fruit consumption
was consistently high throughout the study (Fig. 4) and fruits represented more
than 80% of the items consumed in monthly sampling periods (81% in CO1,
81% in PI1, 90% in PI2, and 90% in SJ1).
We found no significant differences between groups in the percentage of time
invested in the consumption of fruits (Kruskal–Wallis: χ2=2.07,df=3,P=0.55),
leaves (χ2= 6.54, df = 3, P=0.08), or arthropods (χ2=3.95,df=3,P=0.26). There
were differences in the proportion of flowers eaten by the study groups (χ2=11.48,df
=3,P=0.009), driven by lower percentage of flowers in CO1 than in PI1 (P=0.01)
and SJ1 (P = 0.03), all other post hoc tests were non-significant (P=1.00).
Montilla S. et al.

Fig. 2 Activity pattern of two species of tropical night monkeys in Colombia between 2018 and 2019. Bars
indicate the mean for individuals and whiskers the standard deviation (CO1: N=4; PI1: N=5; PI2: N=4;
SJ1: N=5).
Table IV Results of ANOVA and post hoc tests comparing biweekly activity patterns between four groups of
tropical night monkeys in Colombia between 2018 and 2019
Activity ANOVA Tukey’stest(P)
PI1–CO1 PI2–CO1 SJ1–CO1 PI2–PI1 SJ1–PI1 SJ1–PI2
Resting F=6.32
df =3
P<0.001
a
0.02a0.91 0.51 0.008a<0.001a0.89
Movement F=0.51
df =3
P=0.67
NA NA NA NA NA NA
Feeding F=9.14
df =3
P<0.001
a
0.03a0.92 0.04a0.01a<0.001a0.21
aCorresponds to significant differences (P< 0.05).
Activity Patterns, Diet and Home Range of Night Monkeys (Aotus...

Group CO1 relied on at least 31 species of plants from 20 different plant families,
while PI1 used 27 species from 18 families, PI2 used 20 plant species from 13 families,
and SJ1 used 16 species from 13 families. The most important plant families for night
monkeys were Urticaceae and Moraceae, that were among the three main plant families
in the diet of all four study groups. The most important plant families for CO1 included
Melastomataceae (50.0% of feeding time), Urticaceae (17.0%), and Moraceae (15.1%),
that together represent more than 80% of their diet. For PI, the main families of plants
eatenwereMoraceae(29.1%),Urticaceae(23.6%),andEuphorbiaceae(7.2%),ac-
counting for more than 55% of their diet. Plants from Ulmaceae (28.0%), Moraceae
(26.6%), and Urticaceae (13.0%) accounted for >65% of PI2’s diet. Finally, SJ1 based
their diet on plants form the Moraceae (42.3%), Rubiaceae (12.5%), and Urticaceae
(12.3%) families, accounting for more than 65% of consumption time (ESM
Table SIII). For all the groups, each of the rest of the families represented less than
8% of consumption time. The plant families with the greatest number of species
consumed were Melastomataceae with seven and Rubiaceae with three species for
CO1, and Moraceae with seven species for PI1, five for PI2, and three for SJ1. The
remaining plant families were represented by three or less species in the diet of all
Fig. 3 Percentage of items in the diets of two species of tropical night monkeys in Colombia between 2018
and 2019. Bars indicate the mean forindividuals per group and the whiskers the standard deviation (CO1: N=
4; PI1: N=5; PI2: N=4; SJ1: N=5).
Montilla S. et al.

groups. Finally, the most intensively consumed plant genera were Ficus,Cecropia,and
Miconia (ESM Table SIV).
Home Range and Core Area
The home range of CO1 was 8.0 ha (90% kernel) or 11.3 ha (MCP), four times larger
than that of PI1, which was 1.8 ha (90% kernel) or 2.5 ha (MCP), and PI2, which was
1.9 ha (90% kernel) or 2.4 ha (MCP), and three times larger than that of SJ1, which was
2.7 ha (90% kernel) or 3.6 ha (MCP) (Fig. 5;TableV). Groups PI1, PI2, and SJ1 had
core areas of <1 ha (PI1: 0.6 ha; PI2: 0.5 ha; and SJ1: 0.8 ha), while group CO1 had a
core area of 2.2 ha (Fig. 5; Table V).
Distance Traveled per Night
The sums of the mean distances traveled during hourly intervals revealed a total
distance traveled per night of 901 m for CO1, 874 m for PI1, 640 m for PI2, and
Fig. 4 Monthly variation in the proportion of fruits, leaves, arthropods, and flowers eaten by four study groups
of tropical night monkeys in Colombia between 2018 and 2019.
Activity Patterns, Diet and Home Range of Night Monkeys (Aotus...

793 m for SJ1. For all four study groups, peaks in distance traveled were evident in the
first quarter of the night, during the 18:00–19:00 h (PI1, PI2, and SJ1) or 19:00–20:00 h
interval (CO1). Three of the four groups (CO1, PI1, and PI2) showed a second peak in
distance traveled in the last quarter of the night, specifically at 04:00–05:00 h and
05:00–06:00 h. The four groups traveled least in the middle of the night, specifically at
00:00–01:00 and 01:00–02:00 (Fig. 6).
Discussion
Activity Patterns
From the systematic monitoring of four groups of night monkeys over a period of
approximately 1 yr, in two different tropical ecosystems, we found that these
nocturnal primates spend a large proportion of the night resting. Night monkeys in
lowland and highland forests had very similar use of time. These results suggest
that night monkeys in tropical forests invest similar proportion of time in their
main activities, which may be more strongly influenced by factors such as
Fig. 5 Home range (90% kernel and 100% MPC) and core area (50% kernel) of four groups of night monkeys
in tropical forest in Colombia between 2018 and 2019.
Montilla S. et al.

moonlight (Erkert 1976; Muñoz-Delgado et al. unpubl. data.) or other ecological
factors (e.g., forest quality, population density) than by environmental differences
(e.g., mean temperature) between lowland and highland forests. Night monkeys
also spent a high proportion of time moving and feeding, and only a small
proportion of their time in social activities.
These results resemble those for Aotus lemurinus in an investigation that included
sampling with the aid of telemetry in a tropical Andean coffee-shade plantation in
Santander, Colombia (Guzmán et al.2016). Studies that use technological aids such as
telemetry collars have consistently shown similar activity patterns for night monkeys,
that are notably different from earlier studies without such aids which reported that
Table V Results of home range estimation for four groups of tropical night monkeys in Colombia between
2018 and 2019
Species Group Home range estimate (ha)
50% Kernel 90% Kernel 100% MCP
Aotus lemurinus CO1 2.2 8.0 11.3
PI1 0.6 1.8 2.5
PI2 0.5 1.9 2.4
Aotus griseimembra SJ1 0.8 2.7 3.6
Fig. 6 Distance traveled per hour interval for each group of two species of tropical night monkeys in
Colombia between 2018 and 2019. The bars indicate the mean distance traveled per hour interval and the
whiskers the standard deviation. The sample size per hour interval is specified inside the bars.
Activity Patterns, Diet and Home Range of Night Monkeys (Aotus...

A. miconax,A. nigriceps,andA. lemurinus spent a much larger proportion of time
foraging or traveling (Castaño et al.2010;Shaneeet al.2013;Wright1978). Some of
the earlier investigations were conducted over short periods of time (Wright 1978), and
the practical difficulties of losing the monkeys during observations may have biased the
results toward conspicuous behaviors, and undersampled extended resting periods
(Castaño et al.2010). Some studies might also have had a sampling bias by focusing
on specific times of the night (first and last hours of the night when the monkeys are
more active) (Shanee et al.2013)oronnightswithfullmoonwhentheyalsohave
higher activity levels (Erkert 1976). Finally, it is possible that in some of these
investigations, the study groups were not completely habituated to the presence of
researchers and they may have moved more than usual to avoid the researcher, which
could result in an overestimate of the time night monkeys spent moving (Castaño et al.
2010;Wright1978)(TableVI).
Methodological differences may also have affected our findings. PI1—the only
group not fitted with a radiocollar and thus lost more often during follows—spent a
higher biweekly percentage of time feeding and less time resting. From the telemetry
signals, it is possible to identify when the night monkeys are resting in a tree, giving
more reliable results on activity patterns, by not omitting activity data when the study
groups are resting inconspicuously.
We found significant differences in the time our study groups spent looking for food.
PI1 (A. lemurinus) spent the highest percentage of time feeding (33%), followed by
CO1 (A. lemurinus)with24%.Incontrast,SJ1(A. griseimembra) spent only 15% of
time feeding. Group CO1 also showed significant differences in biweekly feeding time
compared to SJ1. CO1 group (A. lemurinus) lives in a mountain forest at 2400 m.a.s.l.
andspentmoretimefeedingthanSJ1group(A. grisemembra)inthelowland
rainforests of San Juan del Carare at 100 m.a.s.l. These differences may reflect the
fact that night monkeys may need to incorporate more energy (food) to maintain
constant body temperatures when exposed to lower temperatures at higher elevations
(Kleiber 1961). If so, this adds to the proposed adaptations related to thermoregulation
in night monkeys, such as a low metabolic rate and high body insulation (Le Maho
et al.1981). Other studies on primates, including titi monkeys (Callicebus sp.), have
shown similar patterns, where populations living in seasonal areas increase feeding
time to face thermoregulatory costs in the winter season (Caselli and Setz 2011). The
higher feeding time in highland night monkeys may also act as a compensatory
measure driven by lower quality, or abundance, of feeding resources (Rothman et al.
2014). As altitude increases, the quantity of endozoochoric fruits (the main source of
food for night monkeys) decreases (Buitrón-Jurado and Ramírez 2014;Schmittet al.
2010;Zhuanget al.2012). This means that night monkeys have to feed on other less
nutritious sources of food and invest more time in food consumption to fulfill their
energetic and nutritional requirements (Ganzhorn and Wright 1994;Ménard2002).
Diet
We found that night monkeys rely heavily on ripe fruits, and all study groups spent
>60% of the feeding time eating fruits. Similar results have been reported for other
groups of Aotus lemurinus (Castaño et al.2010; Guzmán et al.2016) and for other
species of night monkeys such as A. azarae (Arditi 1992; Fernandez-Duque and van
Montilla S. et al.

der Heide 2013)andA. brumbacki (Solano 1995). Arthropods (the second important
dietary element in PI1, P12, and SJ1) and leaves (the second important dietary element
in CO1), are also important in the diet of night monkeys, and we found similar
proportions to those reported in species such as A. azarae and A. brumbacki
(Castaño et al.2010;Guzmánet al.2016; Solano 1995). Although fruits, arthropods
and leaves were consumed in similar percentages between study groups, flower
consumption was small (<1%) in the CO1 group compared to the other groups. We
observed the same pattern in the biweekly consumption, with no differences between
groups in fruit, arthropod, and leaf consumption, but differences in the consumption of
flowers, with lower amounts in CO1 than in the other groups. This low consumption of
flowers in the CO1 group may be related to the lower abundance of this resource in the
high-altitude and low-canopy forests of the Andean highlands. In mountain forests,
trees are usually smaller in diameter and lower in height than in lowland forests, which
probably results in lower abundance of fruits and flowers and could affect the behav-
ioral ecology of primates (Lehman 2014).
The number of plant species consumed by the four groups of night monkeys in this
study is greater than in earlier studies on tropical night monkeys with shorter sampling
periods (Castaño et al.2010;Puertaset al.1992;Wright1978) but is similar to that of
other studies involving more extended monitoring (Guzmán et al.2016;Solano1995).
Differences between groups may reflect the different types of forest they inhabit.
Forests in protected areas, such as those inhabited by CO1, are likely to have a greater
diversity of plants than forests in crop or livestock mosaics, such as those inhabited by
the other groups, affecting the species they consume (Stevenson et al.2012; Zuidema
et al.1996). The seasonally flooded forests of San Juan del Carare, where SJ1 lives,
have a lower diversity of plants due to stringent environmental filters that prevent many
Table VI Activity patterns of Aotus spp.in the wild
Species Activity percentage Time of
following
Notes Source
Feeding Resting Movement
Aotus
lemurinus
50 4 41 18 nights Not habituated Castaño et al.(2010)
28 0 71 5 nights
53 1 41 6 nights
69 5 20 4 nights
33 15 37 9 nights
27 34 26 16 mo Used telemetry Guzmán et al.(2016)
16 43 30 7 mo
Aotus
miconax
33 11 54 12 mo Follows between
18:30–22:00
and 03:00–06:30,
only on full moon
Shanee et al.(2013)
Aotus
nigriceps
53 22 21 2 mo Not habituated Wright (1978)
Aotus azarae 31 49 19 10 nights Sampling during
full moon
García and Braza
(1987)
Activity Patterns, Diet and Home Range of Night Monkeys (Aotus...

trees from surviving extended periods of inundation (Stevenson et al.2012). Brown
spider monkeys (Ateles hybridus) living in these seasonally flooded forests have a less
diverse diet compared to other adjacent populations living in terra firme forests (de
Luna et al.2017).Other factors may also drive the dietary differences of night monkeys
across study sites. For example, the high consumption of leaves by CO1 could be
driven by the large number of species with available leaves for night monkeys
including nonnative plants (Alnus acuminata and Quercus humboltii) (Bare and
Ashton 2016). As altitude increases, leaf protein content increases, and tannins and
lignification of the leaves reduce increasing nutritional content and palatability
(Kitayama and Aiba 2002;Körner1989).
Plants from the Moraceae, Urticaceae, Melastomataceae, and Rubiaceae families are
clearly important in the diet of tropical night monkeys. Other studies has highlighted
the importance of Moraceae in the diet of night monkeys such Aotus nigriceps,
A. vociferans, and A.lemurinus (Castaño et al.2010; Puertas et al.1992; Wright
1978) and many other species of American primates (de Luna et al.2017; Peres
1994; Serio-Silva et al.2002) as they generally possess fleshy fruits, attracting potential
seed dispersers (Gentry 1982). The most consumed genus of Moraceae was Ficus spp.,
which was important in the diet of all four study groups. Ficus provides abundant
resources to frugivores, because they are usually large trees with asynchronous pheno-
logical cycles and few secondary metabolites in their fruits (Parr et al.2011). Rubiaceae
and Melastomataceae are also very abundant species, generally of small size, which are
easily exploited by primates (Terborgh 1983). At El Colegio, where the canopy was
lower, night monkeys ate seven species of the genus Miconia (Melastomataceae) and
three species of Rubiaceae, both for their fruits and leaves. The Urticaceae family also
has been recorded in the diet of both mountain (A. lemurinus) and lowland (A. nigriceps)
night monkeys, even if it is not as diverse as other families and is less consumed by other
American primates (Castaño et al.2010;Guzmánet al.2016;Helenbrooket al.2019;de
Luna et al.2017). Among the family Urticaceae, night monkeys mainly consume the
genus Cecropia (Castaño et al.2010;Guzmánet al.2016;Helenbrooket al.2019),
which all four study groups consumed in high percentages.
Home Range and Core Area
The night monkeys have high behavioral plasticity and can be found in many types of
forests, from highlands to lowlands, and from relatively undisturbed to heavily dis-
turbed forest (Castaño et al.2010; Defler 2010;Montillaet al.2018). Home ranges
range from 17.5 ha for Aotus brumbacki in Tinigua National Park in Colombia
(estimated using minimum convex polygon) (Solano 1995)to0.18haforA. azarae
in a small island forest in Bolivia (unspecified estimation method) (García and Braza
1987). The home ranges and core areas of the four study groups are within the sizes
previously reported for the genus but CO1 group had a larger home range and core area
than all other study groups. The differences between groups may be related to three
nonexclusive factors: 1) the conservation status of the forest, 2) the altitude and
ecosystems where they live (Stevens 1992) as a proxy of resource abundance, and 3)
intra- and interspecific competition at each of the study sites. Conserved forests may
favor larger home ranges for American primate species (Campos et al.2014). CO1
lives in a forest ofca. 60 ha, in a protected area where its movement might be less
Montilla S. et al.

restricted, while PI1 and PI2 groups live in a small forest fragment of 6 ha, which was
used completely by at least two groups of night monkeys. Nonetheless, the forests used
by SJ1 are also protected in a private area and have not been subject to anthropogenic
disruptions in the last decade. Thus, home range size may be limited in the smaller
fragment of Pijao, but other ecological or demographic variable may influence the use
of space by night monkeys in bigger fragments and continuous forests.
As altitude increases, feeding resources become more dispersed for frugivorous
animals, which implies increases in home range and travel distances to obtain the
nutritional requirements (Grow 2014; Stevens 1992). This is evident in several
Afroeuropean primates, including nocturnal species such as pygmy tarsiers (Tarsius
pumilus)(Grow2014;Southwicket al.1996;Wenyuanet al.1993;Whitenet al.
1987). Finally, night monkeys are very territorial and usually exhibit agonistic encoun-
ters with other groups or with other nocturnal mammals such as kinkajou (Potos flavus)
(Puertas et al.1992;Wright1978), which may affect their use of space (Pearce et al.
2013). At Pijao, we recorded three agonistic encounters between PI2 and P. flavus and
11 encounters between PI1 and PI2 groups. The groups home ranges overlapped by ca.
10% and all the agonistic encounters occurred where the home ranges met and included
alarm vocalizations and physical aggression. In the other locations, agonistic encoun-
ters between groups of night monkeys were less frequent, but always at the edges of the
home range (unpubl. data).
Distance Traveled per Night
The distances traveled per night by the four study groups are partially consistent with
the results of other studies of night monkeys. Nightly distances reported so far range
from 252 m in Aotus nigriceps to 854 m in A. lemurinus (Castaño et al.2010;
Fernandez-Duque et al.2008;Solano1995). The distances we recorded for
A. lemurinus groups CO1 (902 m) and PI1 (874 m) are slightly greater than the
maximum distance traveled per night previously reported for the genus (854 m), which
also corresponded to a group of the specie A. lemurinus located in the highlands (1793
m.a.s.l.) (Castaño et al.2010). Aspects of forests such as food availability have been
proposed as regulating factors for distances traveled by primates (Grow 2014;Gursky
2000; Stevenson 2006). The decrease in resource availability as altitude increases
(Lehman 2014) may lead to a longer distance traveled per night in night monkeys,
given that the highest values are in A. lemurinus in Andean forests above 1700 m.
However, PI2 inhabits the same Andean forest as PI1 and traveled the shortest distance
among the four study groups (641 m), suggesting that other factors influence this
behavior. Three of the groups (CO1, PI1, and SJ1) had circular trajectories through
areas of forest that are oval in shape, while PI2 moved in narrow vegetation that
extended over a small stream, which may lead to shorter travel distances.
Our study showed that groups of Aotus lemurinus and A. griseimembra at different
altitudes spend most of their time resting rather than moving, contrasting with earlier
studies of tropical night monkeys. Time spent feeding, home ranges, and distances
traveled per night differ between groups. These basic data on the differences between
groups of tropical night monkeys at different altitudes allow us to hypothesize about the
effects of biotic and abiotic factors on their behavior. Understanding the natural
behavior of night monkeys in tropical forests will complement our knowledge of their
Activity Patterns, Diet and Home Range of Night Monkeys (Aotus...

behavior in subtropical ecosystems and promote comparative research to better under-
stand the evolution of the nocturnal behavior of night monkeys.
Supplementary Information The online version contains supplementary material available at https://doi.org/
10.1007/s10764-020-00192-1.
Acknowledgments The authors thank the National Geographic Society (Grant EC-323R-18), the Global
Wildlife Conservation Primates Action Fund, and the Margot Marsh Biodiversity Foundation (Grant No.
5236.005-0255) for funding the field phase and facilitating the long-term establishment of the night monkey
project in Colombia. Fundación Proyecto Primates also provided valuable logistical and financial support for
the study. We thank the Lalinde and De Greiff families, who have allowed primate research at San Juan de
Carare over the past 13 years; theMontilla family and Rubén Orozco for allowing us to carry out this research
on their property and facilitating our accommodation in Pijao; and Shella Ovalle and Raúl Ladino for
accommodating us in their home in the Cuchilla de Peña Blanca reserve and for all the logistical support
provided during the project. We sincerely thank Sandra Gomez (Fundacion Ingenial Colombia) and biologist
Danilo Santos for the support and logistical facilities given with the Tequendama group.
Author Contributions SOM and AL conceived and designed the study. SOM, AMMC, LNSM, JDMT,
OMCR, JMC, DAGB, JAHV, CJA, LPG, MCM, NJCD, EACD, AHCC, EFP, and AMRO conducted the
fieldwork. SOM and AL performed data analysis and wrote the manuscript.
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Affiliations
Sebastián O. Montilla1,2 &Alex Mauricio Mopán-Chilito3&
Laura Natalia Sierra Murcia1,2 &Jonathan David Mahecha Triana4&
Otto Mauricio Caro Ruiz4&Juanita Montoya-Cepeda5&
Daniela Alejandra Gutierrez-Barreto6&Julie Alejandra Holguín-Vivas4&
Carlos J. Agámez7&Luis Javier Pérez-Grisales8&Mariana Cruz-Moncada8&
Nicole Juliana Corredor-Durango9&Erika Alejandra Chaves Díaz5,6 &
Andrés Humberto Cardona-Cardona3&Estefanía Franco-Pérez10 &
Ana María Rivera-Ospina9&Andrés Link1,2
*Sebastián O. Montilla
juansomontilla94@gmail.com
1
Departamento de Ciencias Biológicas, Laboratorio de Ecología de Bosques Tropicales y Primatología
(LEBTYP), Universidad de los Andes, Bogotá D.C., Colombia
2
Fundación Proyecto Primates, Bogotá D.C., Colombia
3
Programa de Biología, Centro de Estudios de Alta Montaña (CEAM), Universidad del Quindío, Armenia,
Colombia
4
Programa de Biología, Universidad El Bosque, Bogotá D.C., Colombia
5
Programa de Biología, Pontificia Universidad Javeriana, Bogotá D.C., Colombia
6
Programa de Ecología, Pontificia Universidad Javeriana, Bogotá D.C., Colombia
7
Programa de Biología, Grupo de Investigación en Biodiversidad, Universidad de Córdoba, Montería,
Colombia
8
Departamento de Ciencias Biológicas, Escuela de Ciencias, Grupo de investigación en Biodiversidad
Evolución y Conservación (BEC), Universidad EAFIT, Medellín, Colombia
9
Programa de Biología, Universidad INCCA de Colombia, Bogotá D.C., Colombia
10
Programa de Biología, Semillero de Investigación en Primatología y Conservación de sus Ecosistemas
(SIPCE), Universidad de Caldas, Manizales, Colombia
Montilla S. et al.