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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e56851, enero-diciembre 2024 (Publicado May. 14, 2024)
Spatial and temporal dynamics of the primate community
in a regenerating forest of the Manu Biosphere Reserve, Peru
Jackeline Aida Mendoza-Soto1, 2; https://orcid.org/0009-0000-7445-6682
Renato Walter Colan-Rodriguez1, 3*; https://orcid.org/0000-0003-2740-3240
Gladys Milagros Reyes-Lizarraga1, 4; https://orcid.org/0009-0002-3320-4598
Javier Amaru-Castelo1, 5; https://orcid.org/0000-0001-7843-3146
Edgar Luis Marquina-Montesinos1, 5; https://orcid.org/0000-0001-9778-3360
Joseph Oakley1; https://orcid.org/0000-0001-7035-4451
1 Crees Foundation For Manu, Fundo Mascoitania S/N, Cp. 17800, Madre de Dios, Perú; josephoakley94@gmail.com
2 Facultad de Ciencias, Universidad Nacional Agraria La Molina, Av. La Molina S/N, Lima, Perú;
20121018@lamolina.edu.pe
3 Universidad Nacional de San Agustín de Arequipa, Santa Catalina N° 117, Arequipa, Perú; rcolan@unsa.edu.pe
(*Correspondence)
4 Universidad Nacional Mayor de San Marcos, Calle Germán Amezaga N° 375, Lima, Perú; gmilagrosreyes@gmail.com
5 Facultad de Biología, Universidad Nacional de San Antonio Abad del Cusco, Av. de La Cultura 773, Cusco, Perú;
jamarucastelo@gmail.com, emarquina@crees-manu.org
Received 26-IX-2023. Corrected 13-II-2024. Accepted 10-IV-2024.
ABSTRACT
Introduction: Amazonian forests with varying degrees of anthropogenic disturbance in the process of natural
regeneration harbour many sympatric primate species. However, studies on their usage by primates are still
lacking.
Objective: To comprehensively study the spatial and temporal dynamics within the primate community in a
regenerating forest within the Manu Biosphere Reserve.
Methods: Two sets of historical data from Crees Foundation for Manu were analyzed, comprising records from
January 2011 to February 2023 and corresponding to data obtained through incidental data and Terrestrial
In-line Transects in three types of forest with different degrees of historical disturbance.
Results: Lagothrix lagothricha and Ateles chamek showed a preference for less disturbed forests; Plecturocebus
toppini, for more disturbed forests; and the other species did not show a clear preference. Regarding vertical
stratification, A. chamek, L. lagothricha and Alouatta sara showed a preference for the upper stratum, P. top-
pini, Saimiri boliviensis and Sapajus macrocephalus showed a preference for the middle and upper strata and
Leontocebus weddelli and Aotus nigriceps, for the middle stratum. According to the temporal activity of each spe-
cies, seven species (A. chamek, S. macrocephalus, S. boliviensis, P. toppini, L. lagothricha, L. weddelli, and A. sara)
were observed during the day, four were similar.
Conclusions: The primate community varies according to disturbance gradient due to the preferences of some
species. The recorded primates make a differentiated use of the vertical strata and most of them show diurnal
activity.
Key words: secondary forest; conservation; neotropical primates; disturbances, habitat use; Amazon.
https://doi.org/10.15517/rev.biol.trop..v72i1.56851
CONSERVATION
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INTRODUCTION
The Amazon Rainforest stands out as one
of the most important, extensive, and biodi-
verse biomes in the world (Foley et al., 2007;
Mittermeier et al., 2003). This biome encom-
passes 62 % of Peruvian territory, making it
the second largest country in terms of Amazon
coverage after Brazil (Charity et al., 2016).
Currently, the Amazon Rainforest faces vari-
ous anthropogenic threats, such as agriculture,
hunting, livestock, oil and gas extraction, min-
ing, and infrastructure construction (Charity
et al., 2016; Estrada et al., 2017; Francesconi et
al., 2018; Gutiérrez-Vélez et al., 2011). These
activities threaten the diversity and subsistence
of many taxa, such as primates, causing their
species to be considered in various categories of
threat (Estrada et al., 2017; IUCN, 2023; Shanee
et al., 2023). Therefore, the creation of areas
dedicated to the conservation of Amazonian
forests and the improvement of connectivity
between them is essential (Bardales et al., 2023;
Shanee et al., 2014; Shanee et al., 2017; Vuohe-
lainen et al., 2012).
One of the prioritised areas for conserva-
tion in Peru is the Manu Biosphere Reserve
(MBR), containing 19 different ecosystems
across 1 881 200 ha, making it the largest
reserve of Amazonian forest (UNESCO, 2020).
It is considered one of the most biodiverse
places in the world, harbouring 222 species of
mammals (Patterson et al., 2006), 1 003 birds
(Patterson et al., 2006), 132 reptiles (Catenazzi
et al., 2013) and 155 amphibians (Catenazzi et
al., 2013). Among these taxa, primates have
proven to be important for the maintenance
of many ecosystems such as those of the MBR
(Andresen et al., 2018a; Estrada et al., 2017;
Larcher et al., 2019).
The Order Primates is the third largest
group of mammals in terms of species richness,
surpassed only by the orders Chiroptera and
Rodentia (Groves, 2005; IUCN, 2023). Peru is
home to 42 of the 178 primate species docu-
mented in Central and South America (NPC,
2023; Pacheco, 2021). Half of Peruvian species
are critically endangered without an effective
framework to ensure their protection (Sha-
nee et al., 2015; Shanee & Shanee, 2021). The
RESUMEN
Dinámica espacial y temporal de la comunidad de primates en un bosque
en regeneración de la Reserva de Biosfera del Manu, Perú
Introducción: Los bosques amazónicos con diferentes grados de perturbación antrópica en proceso de regenera-
ción natural albergan gran cantidad de especies de primates en simpatría. Sin embargo, aún es carente el estudio
de su uso por primates.
Objetivos: Estudiar la dinámica espacial y temporal dentro de la comunidad de primates en un bosque en rege-
neración en la Reserva de Biosfera del Manu.
Métodos: Se analizaron dos sets de datos históricos de Crees Foundation for Manu que comprenden registros
desde enero 2011 hasta febrero 2023 y corresponden a datos incidentales y transectos lineales terrestres en tres
tipos de bosque con diferente grado de perturbación histórica.
Resultados: Lagothrix lagothricha y Ateles chamek mostraron preferencia por bosques menos perturbados;
Plecturocebus toppini, por bosques más perturbados; y las demás especies no mostraron una preferencia clara. En
cuanto a la estratificación vertical, A. chamek, L. lagothricha y Alouatta sara mostraron preferencia por el estrato
alto; P. toppini, Saimiri boliviensis y Sapajus macrocephalus mostraron preferencia por los estratos medio y alto, y
Leontocebus weddelli y Aotus nigriceps, por el estrato medio. De acuerdo con la frecuencia horaria de cada especie
se observó que siete especies (A. chamek, S. macrocephalus, S. boliviensis, P. toppini, L. lagothricha, Leontocebus
weddelli y A. sara) fueron observadas durante el día, cuatro fueron similares.
Conclusiones: En el estudio, la comunidad de primates cambió en el gradiente de perturbación debido a las
preferencias de algunas especies. Los primates registrados hacen un uso diferenciado de los estratos verticales y
la mayoría de ellos mostraron períodos de actividad diurnos.
Palabras clave: bosque secundario; conservación; primates neotropicales; perturbaciones; uso de hábitat;
Amazonía.
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decline in primate diversity compromises the
ecosystem functions that they perform (Larcher
et al., 2019).
The extent of the ecosystem functions,
such as forest regeneration through seed dis-
persal, that a primate community can perform
in a certain area depends on its complexity.
This complexity is influenced by various factors
such as inter and intraspecific competition; the
vertical layer of the forests, availability of food
resources, presence of suitable resting sites,
hunting pressure, degree of disturbance and
soil fertility, among others (Arcos et al., 2013;
Balbuena de los Ríos, 2023; Chapman, 1995; De
La Ossa et al., 2013; Del Águila-Cachique et al.,
2020; Gómez & Verdú, 2012; Luna, 2013; Villo-
ta-Mogollón, 2023). Understanding the impact
of these factors is crucial for devising effective
primate conservation strategies in regions of
high biodiversity. Therefore, the objectives of
the present research were: (i) characterise the
community of primates present in three types
of forest with different degrees of historical
disturbance, (ii) determine their preference in
vertical stratification and (iii) estimate their
pattern of hourly activity. Additionally, (iv) we
discuss their implications as seed dispersers for
the maintenance and regeneration of secondary
forests in the MBR.
MATERIALS AND METHODS
Study area (Fig. 1): The Manu Learning
Centre (MLC) Biological Field Station is located
Fig. 1. Types of forest according to the degree of historical disturbance found at Manu Learning Centre Biological Field
Station (CCR, PCR and SLR), located within the Manu Biosphere Reserve in the Madre de Dios Region, Perú.
4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e56851, enero-diciembre 2024 (Publicado May. 14, 2024)
within the MBR (12°47’21” S & 71°23’28” W;
470 m.a.s.l.), in the department of Madre de
Dios, Peru. The MBR is made up of three parts:
the core area, which has the highest level of
protection; the buffer zone, with the objectives
to protect indigenous groups, conduct scientific
research, and develop tourist activities; and the
transition zone, which does not have strictly
defined limits and allows various anthropic
activities such as hunting (Yallico & Suarez de
Freitas, 1995). The MLC is in the buffer zone
within a regenerating forest that covers 643 ha
and has been strictly conserved for 20 years. It
has previously been affected by various anthro-
pogenic activities at different scales and is
consequently divided into three types of forests
based on the degree of historical disturbance.
The most disturbed forest, Complete-
ly Cleared and now in Regeneration (CCR),
was previously used for intensive agricultural
activities (coffee, cocoa, and cotton), livestock
grazing, and logging. Currently, this forest
is characterised by having dense vegetation,
mainly bushy. The maximum height of the trees
is up to approximately 20 m, which results in a
canopy that allows the passage of sunlight and
favours the growth of pioneer species of Urtica-
ceae, Melastomataceae and Rubiaceae.
The medium disturbance forest, Partially
Cleared and now in Regeneration (PCR) was his-
torically used for small-scale agricultural activi-
ties and selective extraction of timber trees.
The trees in this area reach an average height
of 30 m, with few open areas that allow limited
access to light. The understory is characterised
by being dense, with a moderate herbaceous
cover. Among the most representative families
are Lauraceae, Urticaceae and Arecaceae.
The least disturbed forest, Selectively
Logged and now in Regeneration (SLR), previ-
ously was subjected to selective logging, and
now features trees with an average height of 50
m and a broader canopy that limits the entry of
sunlight. Most of the trees have robust trunks.
The dominant families in this forest are Faba-
ceae, Meliaceae and Moraceae.
Data collection and statistical analysis:
Two sets of historical data from Crees Founda-
tion for Manu were used in the study, which
correspond to incidental data and Terrestrial
In-line Transect (TILT) surveys. For the inci-
dental data, all the chance observations of
primate species in the different routes made
by the research team at different times of the
day are recorded. We reduced the bias of a
non-systematic methodology by having a vary-
ing schedule of fieldwork, between 03:00 and
00:00 h. On the other hand, TILT sampling is
a systematic methodology of 1 500 m linear
transects carried out in the three types of forest
(CCR, PCR, SLR). In each forest, we set up two
linear transects that were explored in the morn-
ing at 05:00 h and in the afternoon at 16:00 h.
The data set is composed of records from
January 2011 to February 2023. Variables
recorded in the database include the type of
forest, the vertical stratum in which the species
was first observed, and the time of recording.
For incidental data, the complete database was
used. For the analysis of TILT sampling data,
due to the difference in the survey numbers,
we randomly selected the minimum number
(49 for each) to equalise the efforts and com-
pare the three types of forest. To find prefer-
ences for a type of disturbed forest, the count of
individuals by species was carried out in each
forest type. Using this count, rank abundance
curves, correspondence analyses, and Williams’
G goodness-of-fit tests were performed follow-
ing the recommendations of Legendre & Leg-
endre (1983) and McDonald (2014).
The rank abundance curves order the spe-
cies by their abundance and allow us to see
how the structure of the primate community
varies between each of the forest types. In order
to graphically observe if there is a marked
preference towards a certain forest type, a
correspondence analysis with type I scaling
was carried out (Legendre & Legendre, 1983).
Additionally, a Williams’ G goodness-of-fit test
was performed, which allows us to compare
whether the expected proportions are like the
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observed proportions (abundance by forest
type) (McDonald, 2014). The expected propor-
tions were calculated by equating the records
in the three forest types, under the assumption
that they would be the same if they did not
show a preference for forest type.
For the hourly difference analysis, only the
incidental data set was used. The periodic mean
(mean angle, mean direction), periodic median
(mean direction), fit to the von Mises distribu-
tion, Kuiper test, common median test (cm test)
and Dunn’s post hoc test were determined fol-
lowing the recommendations of Dunn (1964),
Fisher (1993), Zar (2010), Glantz (2012) and
Pérez-Bote (2020). The periodic median and
periodic mean were calculated to describe the
data and were made based on the conversion of
hours to radians, since these are the appropri-
ate descriptors for circular data (Fisher, 1993;
Pérez-Bote, 2020). The hourly frequencies were
plotted in a rose diagram, accompanied by
the periodic mean (intermittent line), periodic
median (solid line) and von Mises distribution
(circumference).
The von Mises distribution is equivalent
to the normal distribution in linear statistics
(Pérez-Bote, 2020). To see if the data con-
formed to the von Mises distribution, a Kuiper
test was performed, which allows us to check
if the data conforms to a theoretical distribu-
tion (Pérez-Bote, 2020). The common median
analysis (cm test) is useful to see if the periodic
medians of two datasets are different in a series
of distributions, so it was used to test if there
are differences between the activity period of
the studied primates (Fisher, 1993). The cm
test was carried out with all the species, except
for those that had less than ten total records,
because the test assumes sample sizes of greater
than ten (Fisher, 1993). With the same data,
Dunn’s post hoc test was performed with the
“holm” adjustment, which allows multiple com-
parisons of non-parametric data with differ-
ent sample sizes, and the “holm” adjustment
reduces type I error (Dunn, 1964; Glantz, 2012;
Zar, 2010). Then, the cm test was repeated with
those data that did not present statistical differ-
ences in the post hoc test.
To study vertical stratification, four dif-
ferent strata were considered: high (> 12 m),
medium (> 3-12 m), low (> 0-3 m) and terres-
trial (0 m). A correspondence analysis and Wil-
liams’ G goodness-of-fit tests were performed,
following the recommendations of McDonald
(2014) and Legendre & Legendre (1983). Due
to a limited number of records and the biol-
ogy of the primates studied, we opted not to
include the terrestrial stratum in any of our
analyses. For data manipulation and statistical
analysis, Python 3.11.3 was used with the pack-
ages Scipy 1.10.1, pandas 2.0.2, Matplotlib 3.7.1,
EcoPy 0.1.2.2, Sklearn, collections, pycircstat
(https://github.com/circstat/pycircstat/tree/
master) and pycircular (https://github.com/
albahnsen/pycircular).
RESULTS
For incidental data: Nine primate species
were documented in 5 333 records (Ateles cha-
mek, Sapajus macrocephalus, Saimiri boliviensis,
Plecturocebus toppini, Aotus nigriceps, Lagothrix
lagothricha, Leontocebus weddelli, Alouatta sara,
and Cebus albifrons) (Fig. 2, Table 1). The most
frequently recorded species was P. toppini with
1 337 records, followed by S. macrocephalus
with 1 136 records. There were more inciden-
tal records in CCR (2 904), followed by PCR
(1 444) and finally SLR (985).
According to the abundance range curves
(Fig. 3A) and correspondence analysis (CA1
= 93.61 %, CA2 = 6.38 %) (Fig. 3B), P. toppini
has a marked preference for the most disturbed
forest, presenting 87 % (1 160) of its records in
CCR. S. boliviensis, S. macrocephalus, L. weddelli
and A. sara are representative in the three types
of forest. A. chamek and L. lagothricha present
a high preference for SLR, the least disturbed
forest type. These preferences towards a type of
forest can be verified with the goodness-of-fit
(Table 1), where a statistically significant dif-
ference was obtained between what is expected
and what is observed (P < 0.01) for all species
except C. albifrons, which presents too few
records (seven) to make conclusions from the
goodness-of-fit.
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Regarding the hourly frequencies of inci-
dental data (Fig. 4), most species were recorded
in the morning from 06:00 to 12:00 h, except for
A. nigriceps, which had more records at night
between 18:00 and 05:00 h. None of the records
present a von Mises distribution (P < 0.05) (Fig.
4), so when comparing their medians, it can
be noted that in most species they are between
11:00 and 12:00 h, except for P. toppini, A. sara
and A. nigriceps (Fig. 4). To check if there are
differences between the medians, we applied
the common median test where a CM = 44.33
and P < 0.05 was obtained, indicating that there
are differences in the medians of their hourly
frequencies. The species that are responsible
for these differences are A. chamek, P. toppini,
Fig. 2. Species of primates studied at Manu Learning Centre Biological Field Station. A. Ateles chamek, B. Sapajus
macrocephalus, C. Saimiri boliviensis, D. Plecturocebus toppini, E. Aotus nigriceps, F. Lagothrix lagothricha, G. Leontocebus
weddelli, H. Alouatta sara.
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A. sara and A. nigriceps, showing differences
in post hoc tests with the rest (Fig. 3B). When
performing the common medians test again
without these species, a CM = 0.9099 and P =
0.54 > 0.05 was obtained, finding that the rest of
the species present equal medians.
When comparing the vertical stratifica-
tion of species, we found that the stratum most
Fig. 3. Incidental data analysis of species of primates found in Manu Learning Centre Biological Field Station. A. Rank
abundance curves of primate species records by forest type. B. Correspondence analysis of the preference of each species for
a forest type (CCR, PCR and SLR) C. Correspondence analysis of the preference of each species for a stratum, sumlow (low
stratum), summid (middle stratum) and sumhigh (high stratum). D. Dunn’s post hoc test comparing sample sizes of primate
species, 1. Ateles chamek, 2. Sapajus macrocephalus, 3. Saimiri boliviensis, 4. Plecturocebus toppini, 5. Leontocebus weddelli, 6.
Aotus nigriceps, 7. Lagothrix lagothricha, 8. Alouatta sara.
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frequently used by primates is the middle stra-
tum with 2 484 records, followed by the high
stratum with 1 683 encounters and finally the
low stratum with 1 134 (Table 1). The most
recorded species in all strata was P. toppini
(Table 1). When observing the correspondence
analysis (Fig. 3C), A. sara, L. lagothricha and A.
chamek show a marked preference towards the
high stratum, and the rest of the species towards
the middle stratum. This can be verified by the
goodness-of-fit test, where significant statistical
differences were obtained (P < 0.01) (Table 1).
For TILT data: Eight primate species were
documented in 295 records (Fig. 2, Table 2). The
most frequently recorded species was P. toppini
with 116 records, followed by S. macrocephalus
with 76 records. The least commonly recorded
species was A. nigriceps with four records. More
records were obtained in PCR (142), followed
by CCR (103) and finally SLR (50).
According to the rank abundance curves
(Fig. 5A) and correspondence analysis (CA1 =
62.43 %, CA2 = 37.56 %) (Fig. 5B), three spe-
cies showed a marked preference for CCR: P.
toppini, presenting 59 % (62) of its records in
this forest type; A. sara with 58 % (11) and L.
weddelli with 50 % (six). S. boliviensis, S. mac-
rocephalus and A. nigriceps showed a preference
for PCR. Finally, A. chamek and L. lagothricha
showed a high preference for SLR. These pref-
erences towards a type of forest can be verified
with the goodness-of-fit test (Table 2), which
shows that the observed frequencies are differ-
ent from those expected (P < 0.01) in P. toppini,
A. sara, A. chamek, S. boliviensis, S. macrocepha-
lus and L. lagothricha.
When comparing the vertical distribution,
we found that the stratum most frequently used
by primates was the high stratum with 208
records, followed by the middle with 82 and
finally the low with five (Table 2). The most
frequently recorded species in the high stratum
was P. toppini (96); in the middle stratum, S.
macrocephalus (30); and the low stratum, S.
boliviensis (three). In the correspondence anal-
ysis (Fig. 5C), P. toppini, A. sara, S. boliviensis,
S. macrocephalus and L. lagothricha prefer the
Table 1
Records of primates through incidental sampling at the Manu Learning Centre Biological Field Station in Manu Biosphere Reserve, Peru.
Especie CCR PCR SLR TOT. G_A P_A SH SM SL ST G_B P_B
H M L T S H M L T S H M L T S
A. chamek 6 6 3 0 15 30 7 11 1 49 158 44 29 1 232 296 271.61 0.0000 194 57 43 2 132.34 0.0000
S. macrocephalus 125 359 115 5 604 126 188 65 1 380 60 67 25 0 152 1 136 289.22 0.0000 311 614 205 6 231.46 0.0000
S. boliviensis 103 393 183 3 682 58 176 85 1 320 22 34 17 2 75 1 077 566.81 0.0000 183 603 285 6 259.19 0.0000
P. toppini 295 545 314 6 1 160 53 64 34 1 152 10 9 5 1 25 1 337 1 748.28 0.0000 358 618 353 8 98.62 0.0000
L. weddelli 16 90 41 3 150 42 115 41 1 199 14 56 11 0 81 430 51.78 0.0000 72 261 93 4 141.22 0.0000
A. nigriceps 34 72 27 1 134 13 14 11 0 38 9 8 5 0 22 194 107.42 0.0000 56 94 43 1 21.11 0.0000
L. lagothricha 24 17 6 1 48 106 65 26 2 199 192 111 34 1 338 585 245.34 0.0000 322 193 66 4 183.99 0.0000
A. sara 73 16 17 0 106 67 17 22 1 107 47 5 6 0 58 271 18.75 0.0001 187 38 45 1 145.59 0.0000
C. albifrons 0 5 0 0 5 0 0 0 0 0 0 1 1 0 2 7 7.00 0.0301 0 6 1 0 9.64 0.0081
Abbreviations: CCR: Completely Cleared in Regeneration, PCR: Partially Cleared in Regeneration, SLR: Selectively Logged and now in Regeneration, H: high stratum, M: middle
stratum, L: low stratum, T: terrestrial stratum, S: sum by type of forest, TOT: overall, G_A: goodness-of-fit test statistic for differences in preferences for the degree of disturbance,
P_A: level of significance of the goodness-of-fit test in preferences for a degree of disturbance, SH: high stratum sum, SM: middle stratum sum, SL: low stratum sum, ST: terrestrial
stratum sum, G_B: goodness-of-fit test statistic for differences between strata, P_B: level of significance for the goodness-of-fit test for stratum preferences.
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high stratum; L. weddelli for the medium, and
A. chamek and A. nigriceps for medium and
high. This can also be verified by a goodness-
of-fit test, where statistical differences were
found between the observed and expected fre-
quencies (P < 0.01) for all species except A.
nigriceps (Table 2).
DISCUSSION
Preferences for forest type: In the study,
the primate community exhibited changes along
the disturbance gradient, driven by the prefer-
ences of certain species. Specifically, L. lagoth-
richa and A. chamek displayed a preference for
Fig. 4. Rose plots of the hourly frequencies of incidental data by species of primates in the 24-time categories (0 to 23 h),
showing the periodic median (radians) in intermittent line, the periodic mean (radians) in solid line and the von Mises
distribution in circumference.
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SLR, the least disturbed forest type, while P. top-
pini exhibited a preference for CCR, the most
disturbed forest type. The species L. lagothricha
and those of the genus Ateles have previously
been documented to favour tall primary forests.
This preference is attributed to the presence
of suitable tree cover for their movement, the
abundance of food resources supporting their
populations, and the high potential for protec-
tion from predators afforded by these forests
(Campbell et al., 2005; Di Fiore, 2002; Emmons
& Gentry, 1983; Luna, 2013; Marsh et al., 2016;
Parry et al., 2007; Ramos-Fernández & Ayala-
Orozco, 2003; Rivas-Rojas et al., 2019; Roncan-
cio et al., 2010; Wallace et al., 1998). For this
reason, the structure and vegetal composition
of SLR allows the subsistence of these species;
while the other two forest types, PCR and CCR,
only constitute displacement areas.
The preference for more disturbed forests
in Plecturocebus, as we observed in P. toppini,
has also been reported for other members of
the genus, being present in secondary and
anthropogenised forests with different levels of
disturbance (Defler & Carretero-Pinzón, 2018;
DeLuycker, 2006; García et al., 2010; Shanee et
al., 2013; van Kuijk et al., 2016). This is because
they could modify their behaviour and foraging
strategies according to the availability of food
(Hodges, 2020; Nagy-Reis & Setz, 2017).
A. sara, S. boliviensis, L. weddelli and S.
macrocephalus did not show a clear preference
towards a forest type. These species have been
reported to present relative tolerance to distur-
bance, being found in secondary forests and in
more conserved forests (Aquino et al., 2013;
Buchanan-Smith et al., 2000; Garber et al.,
2006; Garber et al., 2015; Göbel & Heymann,
2018; Peres, 1993; Stevenson et al., 2015; Van
Belle & Estrada, 2006; Wolfheim, 1983). This
relative tolerance may be due to their diet. The
diet of species of the genus Alouatta includes
mature leaves, flowers, leaf and flower buds,
and mature and immature fruits of families
such as Apocynaceae, Arecaceae, Moraceae
and Melastomataceae, allowing them to find
food in any type of forest (Chapman, 1987).
The diet of S. boliviensis and L. weddelli consists
Table 2
Records of primates through TILT sampling at the Manu Learning Centre Biological Field Station in Manu Biosphere Reserve, Peru.
Especie CCR PCR SLR TOT. G_A P_A SH SM SL ST G_B P_B
H M L T S H M L T S H M L T S
P. toppini 54 17 2 0 73 34 1 0 0 35 8 0 0 0 8 116 60.60 0.0000 96 18 2 0 135.226 0.0000
A. sara 11 0 0 0 11 8 0 0 0 8 0 0 0 0 0 19 15.88 0.0004 19 0 0 0 41.747 0.0000
L. weddelli 0 6 0 0 6 1 2 0 0 3 0 3 0 0 3 12 1.41 0.4933 1 11 0 0 19.483 0.0001
S. boliviensis 1 6 0 0 7 26 6 3 0 35 0 3 0 0 3 45 38.98 0.0000 27 15 3 0 22.084 0.0000
S. macrocephalus 4 2 0 0 6 30 27 0 0 57 12 1 0 0 13 76 57.82 0.0000 46 30 0 0 65.024 0.0000
A. nigriceps 0 0 0 0 0 2 1 0 0 3 0 1 0 0 1 4 4.29 0.1171 2 2 0 0 3.244 0.1975
L. lagothricha 0 0 0 0 0 1 0 0 0 1 9 0 0 0 9 10 15.47 0.0004 10 0 0 0 21.972 0.0000
A. chamek 0 0 0 0 0 0 0 0 0 0 0 6 0 0 13 13 28.56 0.0000 7 6 0 0 10.619 0.0050
Abbreviations: CCR: Completely Cleared in Regeneration, PCR: Partially Cleared in Regeneration, SLR: Selectively Logged and now in Regeneration, H: high stratum, M: middle
stratum, L: low stratum, T: terrestrial stratum, S: sum by type of forest, TOT: overall, G_A: goodness-of-fit test statistic for differences in preferences for the degree of disturbance,
P_A: level of significance of the goodness-of-fit test in preferences for a degree of disturbance, SH: high stratum sum, SM: middle stratum sum, SL: low stratum sum, ST: terrestrial
stratum sum, G_B: goodness-of-fit test statistic for differences between strata, P_B: level of significance for the goodness-of-fit test for stratum preferences.
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predominantly of insects, which are also very
abundant and varied in any type of forest
(Fowler et al., 1993; Soini, 1987). Although spe-
cies in the genus Sapajus are considered highly
adaptable and without a clear preference, it has
been reported that some capuchins prefer to
roost in areas of mature forest with larger trees,
showing a slight preference for more conserved
forests (Smith et al., 2018). In contrast, in the
MLC they have refuges in the three types of
forest, which may be related to the strict protec-
tion of the area.
The MLC demonstrates that a forest that
has passed through varying degrees of human
disturbance, today could constitute a habitat for
bioindicator species of healthy ecosystems such
as Lagothrix spp. and Ateles spp., and play a
pivotal role in providing resources and protec-
tion for the primate community (Rivas-Rojas et
al., 2019). Its significance in conserving these
valuable habitats underscores the pressing need
for increased government support and funding
to ensure the continued preservation of this
vital ecosystem.
Vertical stratification: The use of vertical
stratification in primates is closely linked to
various factors, including intraspecific com-
petition, foraging strategies, and the potential
presence of terrestrial predators (Arcos et al.,
2013; De La Ossa et al., 2013). This last aspect
influences the occurrence in the lower and
terrestrial strata, supporting our results, as the
Fig. 5. TILT data analysis of species of primates found in Manu Learning Centre Biological Field Station. A. Rank abundance
curves of primate species records by forest type. B. Correspondence analysis of the preference of each species for a forest
type (CCR, PCR and SLR) C. Correspondence analysis of the preference of each species for a stratum, sumlow (low stratum),
summid (middle stratum) and sumhigh (high stratum).
12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e56851, enero-diciembre 2024 (Publicado May. 14, 2024)
number of recorded instances is significantly
lower in these strata.
A relationship between primate size and
stratum use has been demonstrated (Arcos et
al., 2013; Pozo, 2004). Our findings indicate
that larger primates, such as A. chamek, L.
lagothricha, and A. sara, exhibit a preference
for the upper stratum. This preference is attrib-
uted to the opportunities it provides for engag-
ing in locomotor activities, the abundance of
phytomass, and the high net production of
leaves and fruits, vital resources in the diet of
these species. These patterns align with previ-
ous research (Pozo & Youlatos, 2005). On the
other hand, P. toppini, S. boliviensis and S.
macrocephalus were observed in mid to upper
strata, which may be associated with adopting
a broader field of vision within the forest. This
potentially constitutes a strategy to avoid semi-
arboreal predators such as ocelots (Leopardus
spp.), pumas (Puma concolor), and tayras (Eira
barbara) present in the study area or to identify
potential competitor groups (Arcos et al., 2013;
De La Ossa et al., 2013). The flexibility in forag-
ing strategies could be another reason for their
distribution in these strata, as they disperse and
use various fruit-bearing trees, consuming in
all strata simultaneously or sequentially, adapt-
ing to the forest’s production cycles (De La
Ossa et al., 2013). These same factors are con-
sidered for L. weddelli and A. nigriceps, demon-
strating a pronounced inclination towards the
middle stratum.
Activity period: Primates exhibit a wide
range of temporal activity patterns (Santini
et al, 2015; Tattersall, 1987). According to the
hourly frequency of each species, seven (L.
lagothricha, A. chamek, A. sara, S. macrocepha-
lus, L. weddelli, S. boliviensis and P. toppini) of
the eight species studied were recorded dur-
ing the day, agreeing with the activity pat-
terns described in their ecology (Santini et al,
2015). A. nigriceps was recorded mostly during
the night, agreeing with previous reports of
the species (Santini et al, 2015; Wright, 1978;
Wright, 1989; Wright, 1996). The few records
during the day of A. nigriceps may be since they
show cathemerality, during certain times of the
year (Khimji & Donati, 2014).
Sympatry in primates is possible due to a
differentiated use of habitat, food resources,
vertical stratification, foraging techniques, and
temporal activity segregation, avoiding compe-
tition (De La Ossa et al., 2013; Peres, 1993; Pozo
& Youlatos, 2005; Stevenson et al., 2000). Our
results show no significant difference between
the temporal activity of four sympatric species
(L. lagothricha, S. macrocephalus, L. weddelli, S.
boliviensis). Consequently, it is imperative to
direct our subsequent efforts toward compre-
hending the strategies employed by these spe-
cies to mitigate competition.
Implications of primates as seed dispers-
ers: The ecological importance of primates is
due to the great variety of preferences that spe-
cies present to different factors (disturbances,
vertical strata, and activity time), being able to
develop different functions in the ecosystem
such as seed dispersal. The ability to disperse
seeds by primates is highly related to the use of
the forest and the size of the individual (Bufalo
et al., 2016; Fuzessy et al., 2017; Peres & van
Roosmalen, 2002; Sales et al., 2020). In our
study, the presence of large frugivorous species
such as A. chamek and L. lagothricha in the less
disturbed forest makes them the main seed
dispersers in this type of forest and to a lesser
extent in those with greater disturbance. These
species are considered unique dispersers due to
their ability to move easily through the forest,
and to handle and consume large quantities
of fruits (Luna, 2013; Peres & van Roosmalen,
2002; Stevenson et al., 2002). Unlike these two
species, the seed dispersal capacity of another
large species, A. sara, is reduced by its difficulty
in handling fruits and its more flexible diet,
being able to consume leaves and branches
(Crockett, 1998; Peres & van Roosmalen, 2002).
In more disturbed forests, seed dispersal
occurs mainly through species of medium (S.
macrocephalus) and small size (S. boliviensis,
L. weddelli, A. nigriceps and P. toppini) because
they can withstand disturbance at greater
levels. Medium-sized species require greater
13
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connectivity and consume fruits with almost no
type of restriction (de A. Moura & McConkey,
2007; Wehncke & Domínguez, 2007; Wehncke
et al., 2003). Contrastingly, the smaller ones
do not require extensive areas of forest and
are able to move between patches with small
trees, even using the terrestrial stratum (Milton
& May, 1976). Due to their ability to move in
small trees, smaller primates play a role in the
recovery of connectivity and maintenance of
the diversity of the Amazon Rainforest in places
impacted by humans (Andresen et al., 2018b;
Chagas & Ferrari, 2010; Culot et al., 2010;
Gestich et al., 2019; Helenbrook et al., 2020;
Knogge & Heymann, 2003; Luna et al., 2016;
Müller 1996; Oliveira-Silva et al., 2018; Paim et
al., 2017; Stone, 2007).
The ability to survive in secondary forests
is an important factor for the conservation of
these species and it provides a unique opportu-
nity to study their ecology and adaptability to
different degrees of disturbance. Studies related
to primates and their tolerance to secondary
forests are still scarce. The MLC Biological
Field Station is home to threatened species
(A. chamek and L. lagothricha), so this work
is important because it provides information
on the requirements of these species for their
subsistence. We hope that the results presented
are complemented by more detailed studies on
the use and preference of habitat in secondary
forests and their importance in the regenera-
tion process, since this knowledge is essential
for the design of conservation strategies and
identification of priority sites for the protection
of species.
Ethical statement: the authors declare that
they all agree with this publication and made
significant contributions; that there is no con-
flict of interest of any kind; and that we fol-
lowed all pertinent ethical and legal procedures
and requirements. All financial sources are fully
and clearly stated in the acknowledgments sec-
tion. A signed document has been filed in the
journal archives.
ACKNOWLEDGMENTS
The authors would like to express their
sincere gratitude to Q. Meyer and J. C. Carde-
nas, the founder and CEO, respectively, of
Crees Manu, along with their dedicated team,
for their invaluable support in facilitating our
study. We also extend our appreciation to the T.
& J. Meyer Family Foundation for their gener-
ous funding contribution to Crees Foundation
for Manu, which, in turn, enabled the realisa-
tion of our long-term biodiversity projects. This
paper presents a portion of the results obtained
from this collaborative effort. We are grateful to
J. Vermeer for advising us on the updated tax-
onomy and distribution of some of the primate
species and reviewing the manuscript. Finally,
we thank the two anonymous reviewers for
providing useful comments that improved this
manuscript.
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