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Habitat use, fruit consumption, and population density of the black-headed night monkey, Aotus nigriceps, in southeastern Peru

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The black-headed night monkey, Aotus nigriceps, has one of the largest distribution ranges of the 11 night monkey species found across Central and South America. Yet, only three studies have focused on their ecology, describing considerable variation in habitat, group composition, and population density. Therefore, we analyzed habitat use, group composition, population density, and diet of 14 groups at two field sites in southeastern Peru. All sampled groups were found in secondary tropical rainforest, often dominated by native bamboo species. Half of the observed sleeping sites were in bamboo stands, though groups also emerged from cane thickets and lianas. This contrasts with other Aotus studies which have found groups living in tree cavities and lianas. Population density estimates for both sites were 19 and 50 individuals per km2, outside the range previously reported for A. nigriceps (31−34 individuals per km2). We recovered seeds of 12 species from fecal samples over the course of two field seasons, belonging mainly to Cecropiaceae, Piperaceae and Moraceae. Our results suggest that the black-headed night monkey in Peru can survive and even thrive in secondary forest, feeding extensively on pioneer species, occupying a range of forest types, all while living near human settlements.
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37 VOL. 501 2020: 37  43
http://dx.doi.org/10.1590/1809-4392201900172
ORIGINAL ARTICLE
ACTA
AMAZONICA
Habitat use, fruit consumption, and population
density of the black-headed night monkey, Aotus
nigriceps, in southeastern Peru
William. D. HELENBROOK1,2 * , Madison L. WILKINSON3, Jessica A. SUAREZ1
1 Tropical Conservation Fund, Marietta, GA 30064, USA
2 State University of New York , College of Environmental Science and Forestry, Syracuse, NY, USA
3 Colorado College, Colorado Springs, CO, USA
* Corresponding author: wdhelenb@syr.edu; https://orcid.org/0000-0002-2706-3525
ABSTRACT
e black-headed night monkey, Aotus nigriceps, has one of the largest distribution ranges of the 11 night monkey species found
across Central and South America. Yet, only three studies have focused on their ecology, describing considerable variation
in habitat, group composition, and population density. erefore, we analyzed habitat use, group composition, population
density, and diet of 14 groups at two eld sites in southeastern Peru. All sampled groups were found in secondary tropical
rainforest, often dominated by native bamboo species. Half of the observed sleeping sites were in bamboo stands, though
groups also emerged from cane thickets and lianas. is contrasts with other Aotus studies which have found groups living
in tree cavities and lianas. Population density estimates for both sites were 19 and 50 individuals per km2, outside the range
previously reported for A. nigriceps (31−34 individuals per km2). We recovered seeds of 12 species from fecal samples over
the course of two eld seasons, belonging mainly to Cecropiaceae, Piperaceae and Moraceae. Our results suggest that the
black-headed night monkey in Peru can survive and even thrive in secondary forest, feeding extensively on pioneer species,
occupying a range of forest types, all while living near human settlements.
KEYWORDS: Amazon, primates, Aotidae, conservation, owl monkey, nocturnal, habitat
Uso de habitat, consumo de frutos, y densidad poblacional del mono
nocturno de cabeza negra, Aotus nigriceps, en el sureste de Perú
RESÚMEN
El mono nocturno de cabeza negra, Aotus nigriceps, tiene uno de los rangos de distribución más grandes de las 11 especies
de monos nocturnos que se encuentran en América Central y del Sur. Sin embargo, solo tres estudios se han centrado en su
ecología, describiendo una variación considerable en el hábitat, la composición del grupo y la densidad poblacional. Por lo
tanto, analisamos el uso de hábitat, la composición del grupo, la densidad poblacional y la dieta de 14 grupos en dos sitios de
campo en el sureste de Perú. Todos los grupos muestreados se encontraron en selva tropical secundaria, a menudo dominada
por especies nativas de bambú. La mitad de los dormideros observados estaban en bambú, aunque también surgieron grupos
de matorrales de caña y lianas. Esto contrasta con otros estudios, que encontraron grupos de Aotus viviendo en cavidades de
árboles y lianas. Las estimaciones de densidad poblacional para los dos sitios fueron de 19 y 50 individuos por km2, fuera del
rango previamente reportado para A. nigriceps (3134 individuos por km2). Recuperamos semillas de 12 especies de muestras
fecales en el transcurso de dos temporadas de campo, pertenecientes principalmente a Cecropiaceae, Piperaceae y Moraceae.
Nuestros resultados sugieren que el mono nocturno de cabeza negra puede sobrevivir, e incluso prosperar, en el bosque
secundario, alimentándose ampliamente de especies pioneras, ocupando una variedad de tipos de bosque, todo mientras vive
a menos de 1 km de asentamientos humanos.
PALABRAS-CLAVE: Amazonía, primatas, Aotidae, conservación, mono nocturno, hábito nocturno
CITE AS: Helenbrook, W.D.; Wilkinson, M.L.; Suarez, J.A. 2020. Habitat use, fruit consumption, and population density of the black-headed night
monkey, Aotus nigriceps, in southeastern Peru. Acta Amazonica 50: 37-43.
HELENBROOK et al. Black-headed night monkeys in southeastern Peru
38 VOL. 501 2020: 37  43
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INTRODUCTION
ere are currently 11 recognized species of night monkey,
Aotus Illiger 1811 (Deer and Bueno 2007; Rylands and
Mittermeier 2009), though taxonomy of the genus is still
disputed (Ruiz-Garcia et al. 2011). These wide-ranging
nocturnal primates are found in various tropical and
subtropical habitat types ranging from Panama to Argentina
(previously outlined in Aquino and Encarnacion 1998). Aotus
habitat varies considerably, encompassing a broad altitudinal
gradient ranging from lowland rainforest to cloud forest,
primary and secondary forest as described by Chokkalingam
and De Jong (2001), and fragmented or selectively logged
habitat. ey also use lower and upper canopy, and are
tolerant of seasonal rainfall and temperature variation, along
with various levels of habitat disturbance, including bamboo
thickets, mangroves, palm trees, and gallery forest (e.g., Wright
1994; Aquino and Encarnación 1994; Fernandez-Duque et
al. 2008). Night monkey groups can also be found living
near human settlements (Wright 1989; Fernandez-Duque
et al. 2007).
Aotus groups may contain up to six individuals, including
a monogamous pair with infant, juveniles, and one subadult.
Consistent evidence of solitary behavior has also been reported
in A. azarae (Huck and Fernandez-Duque 2017). ey are
primarily frugivorous and supplement their diet with leaves,
nectar, owers, and insects (Wright 1989; Wright 1994). Wright
(1985) describes as many as 70 fruit species consumed by Aotus
nigriceps (Dollman, 1909), including Moracae, Annonaceae,
Leguminosae, and Sapindaceae species. Crepuscular and
nocturnal behavior likely provides Aotus an opportune time
for capturing a wide array of insects available at dusk and in
the night (Wolovich 2010; Wright 2011). Evidence of diurnal
behavior does exist in Aotus azarae (Fernandez-Duque 2003),
though activity in Aotus nigriceps Dollman 1909 is reported to
be minimal (Khimji and Donati 2014).
e black-headed night monkey, A. nigriceps, occurs
throughout a large part of the central and upper Amazon, and
yet the majority of relevant information on habitat, population
density, and group size for the species are centered on three
nearby sites. One study in the central-eastern Peruvian
Amazon recorded 26 groups on transect survey walks (Aquino
et al. 2013), another focused on a single group over the course
of 65 days (Khimji and Donati 2014) and another study
extensively followed two groups (Wright 1985; Wright 1994).
Habitat has been described as both primary and secondary
forest, seasonally ooded, terra rme, and lowland rainforest,
as well as forest patches with bamboo and palm species (Wright
1985; Aquino et al. 2013; Khimji and Donati 2014). Group
composition largely consists of a mating pair with an infant, a
juvenile and one subadult (Wright 1994); however, Aquino et
al. (2013) describe an average of 2.8 individuals per group with
a maximum of 4, while Khimji and Donati (2014) followed
a single pair with a subadult. A single study has reported
A. nigriceps density (31.1 individuals per km) based on the
number of sightings per 10 km (Aquino et al. 2013). Density
estimates are more widely available for other Aotus species,
ranging from 3.2 to 64 individuals per km2 (e.g., Aquino
and Encarnacion 1988; Fernandez et al. 2001; Svensson et
al. 2010; Maldanado and Peck 2014). We therefore aimed at
expanding our understanding of the ecology of A. nigriceps,
by studying their habitat use, group size, seasonal dietary
shifts, and population density two sites in Amazonian Peru.
MATERIAL AND METHODS
Field work was carried out at two sites in the Manu Biosphere
Reserve in southeastern Peru: Villa Carmen Biological Station
(12°53’39»S, 71°24›16»W), a conservation area managed by
the Asociación para la Conservación de la Cuenca Amazónica
(ACCA) in the Cuzco region, and the Manú Learning
Centre (MLC) (12°4722S, 71°2332W) in the Madre de
Dios region (Figure 1). Both Amazonian sites occur within
Figure 1. (A) Geographic location of the two study areas in southeastern Peru: Manu Learning Center (B) and Villa Carmen Biological Station (C). Night monkey groups
(black stars) were located while conducting line transect surveys or during routine monitoring of trail systems (gray dots).
HELENBROOK et al. Black-headed night monkeys in southeastern Peru
39 VOL. 501 2020: 37  43
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tropical premontane forest, exhibiting similarly stable average
temperatures throughout the year (22°C; maximum 32°C and
minimum 10°C). Average annual rainfall ranges from 3200-
5000 mm yr-1. e highest rainfall occurs from December to
March and the driest months occur from May to September.
Villa Carmen contains 30.65 km2 of protected primary forest
within the Manu Biosphere Reserve, though our surveys were
conducted almost entirely in secondary forest (16.8 km of
trails). MLC has a mixed history of plantations and cattle
grazing, coupled with selectively logged and undisturbed,
primary forest. We sampled both secondary (11 km of trails)
and primary forest (2.5 km) at MLC. In the secondary
forest, 7 km were in a previous timber harvest zone, 0.75
km in secondary bamboo forest, and 3.25 km in a selectively
logged area.
We collected data from 14 black-headed night monkey
groups during April 2016, November 2016 and April
2017 at Villa Carmen, and during April 2017 at MLC.
Population density was estimated using three dierent
methods previously applied in other Aotus studies: encounter
rates per distance traveled (Pontes et al. 2012), line transects
utilizing perpendicular methods using detection function
models (Marhsall et al. 2008), and direct counts (Fernandez
et al. 2001). In the rst method, we calculated the number
of groups encountered per kilometer walked. Established
trails were walked from 18:00 to 21:00 h at 1−2 km per
hour, scanning vegetation continuously as a group of two
to ve eld assistants spaced out evenly. is method was
used as a baseline for comparison between our sites and
earlier Aotus studies. For encounter rates and line transects,
surveys followed pre-existing trails so as not to disturb
habitat, which as a result sometimes included nonlinear
routes. However, most trails at Villa Carmen run parallel to
one another and those at MLC are largely linear (Figure 1).
e closest distance between trails was 250 m, and detection
of groups was not feasible beyond 25 m. ere was little
evidence of avoidance behavior as the trails are routinely
walked and night monkeys have been observed near trails.
Every 100−200 m, eld assistants would pause and listen for
calls. Once a monkey was spotted, we would observe them
in order to obtain demographic information, group size,
GPS location, record time, and to measure the perpendicular
distance from transect to group (Marshall et al. 2008). In
the second method, we calculated population density from
survey data using the program DISTANCE (version 6.2).
Lastly, we simply calculated the known number of groups
and individuals within a well-studied area at Villa Carmen
over the course of two years. We determined nesting sites
during the day and conrmed general travel patterns for
each group in the area both at dusk and dawn.
We later revisited the area where night monkey groups
were found during transect walks to perform habitat analysis,
classifying forests based on qualitative factors, i.e., secondary
versus primary forest, and presence of bamboo or cane, or
lianas (Ganzhorn 2003). We took canopy cover photos at
each group location and used ImageJ software (1.4.3.67)
to calculate canopy cover percentages. GPS points taken at
each location were paired with satellite imagery to determine
proximity of monkey groups to known human settlements.
A quantitative estimate of forest complexity for each group
was made using 50 m × 2 m plots (Gentry 1982), starting
1 m o the trail and measuring 1m beyond, for both sides
from where the group was located. All woody trees ≥ 10 cm
diameter at breast height (approximately 1.3 m above ground)
were recorded within the plot (Ganzhorn 2003).
We collected 48 fecal samples (33 from Villa Carmen and
15 from MLC; 26 in spring and 22 in the fall) (Table 1) for
a preliminary characterization of diet from identication of
deposited seeds. Fecal collection was conducted by covering
forest oor with plastic mesh or cloth nets below areas where
night monkeys had previously been observed or where there
was evidence of their feeding. e nets were used to catch
any falling fecal samples and monitored daily throughout the
study. e fecal samples were preserved in formalin and were
later analyzed in the laboratory. We then strained samples
using cheese cloth to recover seeds and then examined them
under a BSZ405 stereo microscope (Boeco, Germany). Seeds
were then identied to the lowest possible taxonomic level
using available literature and categorized based on association
with primary or secondary-forest types (e.g., Cornejo and
Janovec 2010).
Table 1. Plant taxa identied from seeds recovered from Aotus nigriceps fecal
samples. Values are the frequency of occurrence of seeds in recovered samples
from each site and sampling occasion. VC = Villa Carmen; MLC = Manu Learning
Center; N = fecal sample size.
Genus (Family)
April
2016
November
2016
April
2017
VC
(N=11)
VC
(N=22)
VC
(N=9)
MLC
(N=6)
Philodendron Schott (Araceae) 0 0 11.1 50
Annonaceae Juss. 0 0 0 33.3
Aniba Aubl. (Lauraceae) 0 13.6 0 0
Physocalymma Pohl (Lythraceae) 54.5 0 0 33.3
Bellucia Neck. (Melastomataceae) 27.3 0 22.2 16.7
Henriettella Naudin (Melastomataceae) 0 0 11.1 33.3
Ficus L. (Moraceae)* 0 27.3 55.5 0
Psidium L. (Myrtaceae) 0 31.8 0 0
Piper L. (Piperaceae) 45.5 4.5 66.7 66.7
Solanum L. (Solanaceae) 0 0 0 16.7
Urera Gaudich. (Urticaceae) 27.3 0 0 0
Cecropia Loe (Urticaceae)* 100 77.3 100 66.7
*Previously described in Aotus nigriceps (Wright 1981 and Wright 1985)
HELENBROOK et al. Black-headed night monkeys in southeastern Peru
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RESULTS
Nine night-monkey groups were found at Villa Carmen and
ve at MLC, ranging in size from two to ve individuals,
though a solitary individual was also encountered (Table
2). ese groups were revisited over the course of the two
years. All groups were in areas with some level of historical
logging and habitat degradation (Table 2). Basal area estimates
were consistent with previously described degraded habitat
(Brown and Lugo 1990). All but one group at Villa Carmen
was found in forest dominated by native bamboo species,
Guadua weberbaueri Pilg. and Guadua sarcocarpa Londoño
and P. M. Peterson. A single group was found in degraded
cane (Gynerium Willd ex P. Beauv) forest with bamboo. Only
two groups at MLC were found in areas with bamboo, while
the others were found in secondary forests devoid of bamboo.
We were unable to locate specic nesting sites for all
groups; however, of the five that were located at Villa
Carmen, three were in bamboo stands, one in a cane thicket,
and another in lianas. ough we could not locate an exact
nesting site for the four remaining groups (44%), we were
often present when they rst started moving in the evenings.
For example, we could often triangulate the general area
where they would begin moving at dusk but could not locate
them during the day to pinpoint their sleeping site. ese
four groups were also found in areas dominated by bamboo.
At MLC, only one nesting site was conrmed, and this was
found in lianas lacking any bamboo. All groups were found
within 1 km of each associated eld station. Two groups at
Villa Carmen and one group at MLC were routinely found
on the perimeter of the station in secondary forest (< 100 m).
Estimated DISTANCE densities were higher at Villa
Carmen (50.0 individuals per km2) than at MLC (19.2
individuals per km2). Both estimates had a large condence
interval, ranging from 17.0−147.0 individuals per km2 at
Villa Carmen, and 4.9−75.3 individuals per km2 at MLC.
e known number of individuals in our sampling area at
Villa Carmen was 17.5 individuals per km2 and the encounter
rate was 5.8 groups per 10 km. We could not calculate these
parameters for MLC since group composition there is not as
well-known as at Villa Carmen, and our sample size was too
small to calculate the encounter rate.
We recovered seeds belonging to 12 genera and ten families
(Table 1). e number of taxa recovered from Villa Carmen
groups in bamboo forest was similar (N = 10) to that from
MLC (N = 8). We recovered as many as seven genera from a
single MLC group, and just four genera from a group living
in disturbed mixed bamboo forest at Villa Carmen. Cecropia
was found in all sampled groups, and three genera were found
in both sampled seasons: Cecropia sp., Piper sp., and Ficus sp.
Groups at MLC consumed all the same fruits identied at
Villa Carmen in Spring 2016 except for Urera sp. However, we
found that groups at MLC consumed two other fruit species,
including an unidentied Annonaceae and Solanum sp.
DISCUSSION
All black-headed night monkey groups in our study were
found in secondary forest, though there is considerable
evidence to suggest that they are also found in primary habitat
based on camera trap data provided by MLC (unpublished
data) and from previous Aotus studies (Wright 1978; Aquino
and Encarnacion 1994; Cornejo et al. 2008; Aquino et al.
2013; Shanee et al. 2013). Limited sampling in primary forest
is presumably the main reason we did not encounter Aotus in
these areas. Dense canopy in primary forest also likely limited
our ability to detect auditory or visual cues of night monkeys.
Table 2. Habitat structure of Aotus nigriceps groups found at Villa Carmen (VC) and Manu Learning Centre (MLC) in southeastern Peru. N = number of individuals in group.
Field site Group N Habitat type Nest type Canopy cover (%) Total basal area (m2 ha-1) Elevation (m a.s.l.)
VC A 4 Secondary forest, bamboo Bamboo 74.7 12.66 530
VC B 3 Secondary forest, bamboo Bamboo 76.9 11.91 530
VC C 3 Secondary forest, bamboo Unknown 65.5 2.11 610
VC D 2 Secondary forest, bamboo Bamboo 69.3 10.34 529
VC E 3 Secondary forest, cane Cane 68.3 22.1 516
VC F 3 Secondary forest, Bamboo Liana 69.8 9.93 529
VC G 3 Secondary forest, Bamboo Unknown 70.2 14.15 530
VC H 3 Secondary forest, Bamboo Unknown 68.2 4.85 529
VC I 2* Secondary forest, Bamboo Unknown 72.3 19.75 529
MLC T2A 5 Secondary forest Unknown 80.8 15.62 516
MLC T2B 4 Secondary forest Liana 71.3 14.11 512
MLC T9A 3 Secondary forest Unknown 84.4 13.11 489
MLC T9B 2* Secondary forest, Bamboo Unknown 77.2 38.12 487
MLC Camp 4 Secondary forest, Bamboo Unknown 76.0 NA 456
*In two cases, groups were observed but exact numbers could not be ascertained. We include the minimum number of individuals observed (N), though the total
group size could be higher. The qualitative assessment was based on visual assessment and unpublished historical records provided by each eld station. In a single
case, basal area was not available (NA).
HELENBROOK et al. Black-headed night monkeys in southeastern Peru
41 VOL. 501 2020: 37  43
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e majority of groups were found in forest dominated by
native bamboo, and all groups were found in proximity to
each eld station (< 1 km). Our results suggest that night
monkeys are likely to be found, and even potentially thrive,
in these types of secondary forest dominated by bamboo and
cane species. Aotus nigriceps were also found to attain relatively
high densities (31.1 individuals per km2) living in mixed
bamboo forests in an area ~150 km northeast from our study
sites, suggesting that this species may be able to survive in an
array of forest types (Aquino et al. 2013).
Estimated population density and encounter rates at Villa
Carmen were both higher than the only other A. nigriceps
report (Aquino et al. 2013); however, the known number of
individuals per square kilometer was actually lower. MLC
density estimates were similar to encounter rates found at Villa
Carmen. A number of factors could contribute to dierences
in density estimates, most notably habitat type. Aquino et
al. (2013) pooled results from three habitat types so we are
unable to ascertain whether there was a signicant dierence
compared to our study. However, they found primary forest
and semi-dense primary forest with some bamboo had a
higher percentage of sightings compared to open primary
forest with bamboo. Considering most of our sampled area
was secondary forest with bamboo, it is therefore dicult to
make a reasonable comparison (Nelson 1994). Svensson et
al. (2010) also surveyed three dierent types of Aotus zonalis
habitat in Panama. To our knowledge, none of these contained
bamboo but still had similar densities compared to our study
(i.e., 0− 19.7 individuals per km2; mean = 13.2).
Our DISTANCE estimate at Villa Carmen was higher
than the known number of individuals; however, the
condence interval was fairly large, likely due to a relatively
small sample size. It is conceivable that we counted some
groups twice on trails that were only 250 m apart, since night
monkeys have been reported to travel as far as 708 m in 24
hours (Wright 1989). However, duplicate sampling is not
likely since we established sleeping sites in most cases, and
monitored travel patterns for each group.
Night monkeys have been reported to use tree holes or
vine tangles as nesting sites, which are normally restrictive as
they limit their ability to travel particularly far since they need
to return to the same site the following morning (Aquino and
Encarnacion 1986; Fernandez-Duque et al. 2008). However,
night monkeys at Villa Carmen routinely returned to the same
bamboo patches despite there being other dense patches all
around and no competing groups vying for sleeping sites.
ere was no evidence that they used tree holes, and we only
observed two nesting sites composed of tangled vines. e
absence of nesting sites in tree holes may be related to the
scarcity of such resource in the secondary forest. Additionally,
the return to the same sleeping sites in consecutive days may
be explained by the familiarity in established routes and
accessibility to food sources.
Diet analysis of defecated seeds showed that Aotus relied
heavily on Cecropia spp. However, no species dominated
sample composition. Consumption of Cecropia spp. might
have little to do with preference, but rather with the availability
of this species in secondary forests. Most groups did not have
access to primary habitat, though they could have traveled to
nearby areas with reduced habitat degradation. Two of our
sampled groups also made use of abandoned guava (Psidium)
orchards as part of their home range, areas frequented by
workers at the eld station during the day. ere was no
evidence that other sympatric diurnal primates used these
guava orchards during the day, which makes them potentially
valuable food sources to the night monkeys. Psidium seeds
were recovered from one of these nearby groups along with
two others which were not in proximity to these orchards.
In total, we recovered twelve seed types from fecal samples,
and only two of these genera were previously described in
Aotus (Table 1: Wright 1981 and Wright 1985). No other
known studies have reported on fruits consumed in other
Aotus species. Given our small sample size, the diversity
of fruits consumed is likely much larger, though Wright
(1978) similarly described the use of just nine fruiting tree
species by a group over the course of one month. Of course,
analysis of fecal samples limits our results to seeds that remain
recognizable after passing the digestive tract and does not
give a full picture of other types of food consumed, such
as leaves, nectar, owers, and insects (Wright 1985; Wright
1989; Wright 1994).
e black-headed night monkey - and likely other Aotus
species – are quite adaptable based on their use of degraded
habitat, an omnivorous diet including the consumption of
several pioneer species, and an ability to persist in areas close
to human settlements. For example, there are nine other
monkey species in nearby primary habitat at Villa Carmen;
however, only A. nigriceps and Sapajus apella (Linnaeus 1758)
were found in the sampled secondary forest with bamboo,
an area which also has evidence of hunting based on camera
trap footage (unpublished data). Likewise, night monkeys
use multiple habitat types and forests with varying levels of
degradation which suggests that they can traverse ecological
matrices that might be difficult for other species. Their
consumption of fruit from a dozen tree species suggests that
they may be able to disperse an array of seeds throughout
the year, though over short distances, as their ability to
move seeds over large distances is presumably limited. We
previously conducted a limited analysis of seed germination
success and time to germination in Aotus nigriceps and found
both measurements were positively associated with digestion
(unpublished data). However, expanded sampling is necessary
HELENBROOK et al. Black-headed night monkeys in southeastern Peru
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to determine to what degree night monkeys contribute to seed
dispersal, predation, and germination success.
CONCLUSIONS
We report that Aotus nigriceps is able to occupy degraded
habitat, inhabiting bamboo forests and relying on a varied
diet of fruits from pioneer species. e presence of this
species in heavily disturbed habitat suggests some level of
behavioral and dietary plasticity. Expanded sampling into
more diverse habitat types and across a larger geographical
range would likely contribute to our understanding of their
ecological niche.
ACKNOWLEDGMENTS
We would like to thank Asociación para la Conservación de
la Cuenca Amazónica, and sta at both the Villa Carmen
Biological Station and Manu Learning Centre (CREES) for
hosting us, clearing trails, and providing valuable insight into
location and behavior of groups. We are indebted to the students
and sta from e School for Field Studies (Peru) who assisted
with data collection and logistics, specically Isabelle Berman,
Noah Linck, Audrey Nelson, Ben Sharaf, Caroline Rzucidlo,
Katlin Gott, Leigh Preston, and Sheridan Plummer. Special
thanks to Brooke Zale and two anonymous reviewers for
their valuable feedback on the manuscript. Logistical support
provided by the Tropical Conservation Fund.
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RECEIVED: 16/01/2019
ACCEPTED: 28/08/2019
ASSOCIATE EDITOR: Paulo D. Bobrowiec
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... Aotus nigriceps is a wide-ranging nocturnal monkey species found across much of the central and upper Amazon, including the moist forests of the Southwest Amazon, Jurua-Purus, Purus-Maderia, and Maderia-Tapajos. They are also typically found in degraded forest, agro-forested landscapes, and areas in proximity to humans (Wright 1994;Helenbrook et al. 2020). While night monkeys are adaptable and found to persist in degraded landscapes, they still require connective forest cover, access to seasonally available fruiting trees, sleeping sites, and are restricted by environmental conditions (Aquino and Encarnación 1994;Helenbrook et al. 2020). ...
... They are also typically found in degraded forest, agro-forested landscapes, and areas in proximity to humans (Wright 1994;Helenbrook et al. 2020). While night monkeys are adaptable and found to persist in degraded landscapes, they still require connective forest cover, access to seasonally available fruiting trees, sleeping sites, and are restricted by environmental conditions (Aquino and Encarnación 1994;Helenbrook et al. 2020). Although thought to be a common species, it is currently listed as Appendix II of CITES [Convention on International Trade in Endangered Species of Wild Fauna and Flora], and the impact of anthropogenic disturbances on the long-term viability of A. nigriceps remains unknown. ...
... However, discrepancies remain regarding the extent of their eastern distribution in the state of Rondonia, and additional taxonomic analysis is needed from the area (e.g., Pieczarka et al. 1993;Plautz et al. 2009;Menezes et al. 2010;Babb et al. 2011;Ruiz-Garcia et al. 2011). The species is not considered under threat due to their presumed extensive range, their large and sustained population size (Shanee et al. 2018), and highdensity estimates ranging from 19 to 50 individuals/km 2 (Helenbrook et al. 2020). However, no known population size estimates or trends have been described despite large portions of the range of A. nigriceps overlapping with areas experiencing some of the highest deforestation rates in the world (Estrada et al. 2018). ...
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... Aotus nigriceps is a wide-ranging nocturnal monkey species which lives in degraded habitats, utilizes agroforested landscapes, and is known to tolerate human populations (Helenbrook et al., 2020). Nevertheless, while night monkeys are adaptable and persist in degraded landscapes, they still require connective forest cover, access to seasonally available 60 fruiting trees, sleeping sites, and are restricted by environmental conditions (Wright 1981;Aquino & Encarnación 1994;Fernandez-Duque et al., 2001;Helenbrook et al., 2020). ...
... Aotus nigriceps is a wide-ranging nocturnal monkey species which lives in degraded habitats, utilizes agroforested landscapes, and is known to tolerate human populations (Helenbrook et al., 2020). Nevertheless, while night monkeys are adaptable and persist in degraded landscapes, they still require connective forest cover, access to seasonally available 60 fruiting trees, sleeping sites, and are restricted by environmental conditions (Wright 1981;Aquino & Encarnación 1994;Fernandez-Duque et al., 2001;Helenbrook et al., 2020). This species is found in Southern Peru, northern Bolivia, and central-western Brazil with density estimates ranging from 19-50 individuals/km 2 (Helenbrook et al., 2020). ...
... Nevertheless, while night monkeys are adaptable and persist in degraded landscapes, they still require connective forest cover, access to seasonally available 60 fruiting trees, sleeping sites, and are restricted by environmental conditions (Wright 1981;Aquino & Encarnación 1994;Fernandez-Duque et al., 2001;Helenbrook et al., 2020). This species is found in Southern Peru, northern Bolivia, and central-western Brazil with density estimates ranging from 19-50 individuals/km 2 (Helenbrook et al., 2020). The International Union for Conservation of Nature (IUCN) currently lists this species as Least Concern because of their 65 extensive range, suspected large and sustained population size, and presumed low risk of extinction. ...
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Deforestation rates in the Brazilian Amazon have been steadily increasing since 2007. Recent government policy, projected growth of agriculture, and expansion of the cattle industry is expected to further pressure primates within the Amazon basin. In this study, we examined the anthropogenic impact on the widely distributed black-headed night monkey, Aotus nigriceps, whose distribution and population status have yet to be assessed. We 1) modeled species distribution in A. nigriceps; 2) estimated impact of habitat loss on population trends; and 3) highlight landscape-based conservation actions which maximize potential for their long-term sustainability. We found the black-headed night monkey to be restricted by several biotic and environmental factors including forest cover, elevation, isothermality, and precipitation. Over the last two decades, over 132,908 km2 of tree cover (18%) has been lost within their documented range. We found this species occupies only 49% of habitat within in their range, a loss of 19% from their estimated 2000 distribution, and just over 34% of occupied areas were in protected areas. Projected deforestation rates of A. nigriceps equates to an additional loss of 23,084 km2 of occupied habitat over the next decade. This study suggests that although classified as a species of Least Concern, A. nigriceps may have a much smaller range and is likely more at risk than previously described. The future impact of continued expansion of mono-cultured crops, cattle ranching, and wildfires is still unknown. However, expanded use of participatory REDD+, sustainable agroforestry in buffer zones, secured land tenor for indigenous communities, wildlife corridors, and the expansion of protected areas can help ensure viability for this nocturnal primate and other sympatric species throughout the Amazon Basin.
... 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;Guzmán et al. 2016;Helenbrook et al. 2019;de Luna et al. 2017). Among the family Urticaceae, night monkeys mainly consume the genus Cecropia (Castaño et al. 2010;Guzmán et al. 2016;Helenbrook et al. 2019), which all four study groups consumed in high percentages. ...
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• Premise of the study: Frugivore selection of fruits and treatment of seeds together with seed deposition site are crucial for the population dynamics of vertebrate-dispersed plants. However, frugivore species may influence dispersal quality differently even when feeding on the same fruit species and, while animals disperse some seeds, others simply fall beneath the parent plant.• Methods: In southern Mexico, we investigated to see if within-species seed traits (i.e., length, width, weight, and volume) and germination success differed according to seed source. For five tropical tree species we obtained ingested seeds from two sources, howler monkey (Alouatta pigra) and spider monkey (Ateles geoffroyi) feces; and noningested seeds from two sources, the ground and tree crowns (with predispersed seeds used as control).• Key results: A principal components' analysis showed that traits of seeds ingested by howler monkeys differed from other sources while seeds ingested by spider monkeys were similar to noningested seeds. Howlers consumed on average the larger seeds in Ampelocera hottlei, Brosimum lactescens, and Dialium guianense. Both primate species consumed the smaller seeds in Spondias mombin, while no seed trait differences among seed sources were found in Spondias radlkoferi. For all five tree species, germination rate was greatest for seeds ingested by howler monkeys.• Conclusions: For the studied plant species, seed ingestion by howler monkeys confers higher dispersal quality than ingestion by spider monkeys or nondispersal. Dispersal services of both primate species, however, are not redundant and may contribute to germination heterogeneity within plant populations in tropical forests.
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Biotic seed dispersal is a key process maintaining biodiversity in tropical forests where most trees produce vertebrate-dispersed seeds. Existing meta-analyses suggest an overall positive effect of vertebrate gut passage on seed germination, but no significant effects for non-flying mammals. However, previous meta-analyses combined rodents (seed predators) and primates (seed dispersers) into the non-flying mammals category, which may confound specific effects of each group on seed germination. However positive effects of monkeys on germination had previously been found in some studies. Here we disentangle the role of Neotropical primates as contributors to seed dispersal in tropical forests by running a meta-analysis to determine the overall magnitude of gut passage effects on seed germination percentage and mean time to germination. We also compare effect sizes as a function of different feeding guilds, gut complexities, and seed size. Our results show a strong, positive effect of primates on seed germination percentage and on the number of days to first germination. Strictly frugivorous monkeys, the group most threatened by extinction, showed the highest dispersal quality, increasing germination percentage by 75% and decreasing average germination time by 15%. Primates that include insects in their diets had no average effect on germination percentage or time. Gut passage had different outcomes on seeds with different sizes; both large and small seeds showed similar increases in germination percentages after gut passage, but only large seeds germinated faster than control seeds after gut passage. Our results show a relevant role for primates in providing high seed dispersal quality and as drivers of forest regeneration. The combined effects of defaunation and forest fragmentation may result in decreased regeneration of trees, which has the potential to affect negatively both forest structure and ecosystem processes. Finally, we provide general guidelines for standardizing research on seed dispersal by primates.