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PRIMATES
NEOTROPICAL
ISSN 1413-4703
A J our nal of th e Neotropical Section of the
IUCN/SSC Primate Specialist Group
Volume 25
Number 1
December 2019
Editors
Erwin Palacios
Jessica Ward Lynch
Bruna Bezerra
Liliana Cortés-Ortiz
Júlio César Bicca-Marques
Eckhard Heymann
Anita Stone
News and Book Reviews
Brenda Solórzano
Ernesto Rodríguez-Luna
PSG Chairman
Russell A. Mittermeier
PSG Deputy Chairman
Anthony B. Rylands
Neotropical Primates
A Journal of the Neotropical Section of the IUCN/SSC Primate Specialist Group
Conservation International
2011 Crystal Drive, Suite 500, Arlington, VA 22202, USA
ISSN 1413-4703 Abbreviation: Neotrop. Primates
Editors-In-Chief:
Erwin Palacios, Conservación Internacional Colombia, Bogotá DC, Colombia
Jessica Ward Lynch, Institute for Society and Genetics, University of California-Los Angeles, Los Angeles, CA, USA
Co-editors:
Bruna Bezerra, University of Louisville, Louisville, KY, USA
Liliana Cortés Ortiz, Museum of Zoology, University of Michigan, Ann Arbor, MI, USA
Júlio César Bicca-Marques, Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, Brasil
Eckhard Heymann, Deutsches Primatenzentrum, Göttingen, Germany
Anita Stone, California Lutheran University, ousand Oaks, CA, USA
Founding Editors
Anthony B. Rylands, Global Wildlife Conservation, Austin, TX, USA
Ernesto Rodríguez-Luna, Instituto de Neuroetología, Universidad Veracruzana, Xalapa, México
Editorial Board
Hannah M. Buchanan-Smith, University of Stirling, Stirling, Scotland, UK
Carolyn M. Crockett, Regional Primate Research Center, University of Washington, Seattle, WA, USA
Stephen F. Ferrari, Universidade Federal do Sergipe, Aracajú, Brazil
Russell A. Mittermeier, Global Wildlife Conservation, Austin, TX, USA
Marta D. Mudry, Universidad de Buenos Aires, Argentina
Anthony Rylands, Conservation International, Arlington, VA, USA
Karen B. Strier, University of Wisconsin, Madison, WI, USA
Maria Emília Yamamoto, Universidade Federal do Rio Grande do Norte, Natal, Brazil
Primate Specialist Group
Chairman: Russell A. Mittermeier
Deputy Chairs: Anthony B. Rylands and Christoph Schwitzer
Executive Secretary: Ella M. Outlaw
Vice Chairs, Section on Great Apes: Dirck Byler and Serge Wich
Vice Chair, Section on Small Apes: Susan Cheyne
Vice Chairs, Section on Human-Primate Interactions: Sian Waters and Susan Cheyne
Regional Vice Chairs—Neotropics Mesoamerica:
Liliana Cortés-Ortiz
Andean Countries: Erwin Palacios, Eckhard W. Heymann, Fanny M. Cornejo, Stella de la Torre, and Diana C. Guzmán
Brazil and the Guianas: M. Cecília M. Kierul, Fabiano Rodrigues de Melo, Maurício Talebi, and Leandro Jerusalinsky
Southern Cone: Martin Kowalewski
Regional Vice Chairs —Africa
Rachel Ashegbofe Ikemeh, Inza Koné, David Osei, and Janette Wallis
Regional Vice Chairs —Madagascar
Christoph Schwitzer, Jonah Ratsimbazafy, and Steig Johnson
Regional Vice Chairs — Asia
China: Baoguo Li
South-east Asia/Indochina:Jatna Supriatna, Arif Setiawan, Christian Roos, Benjamin M. Rawson, Ramesh Boonratana, Le Khac Quyet, and Duc Hoang Minh
South Asia: Sanjay Molur and Dilip Chetry
Red List Authority Coordinators: Sanjay Molur, Christoph Schwitzer, and Liz Williamson
Layout: Patricia Salinas Garzón, Bogotá, DC <patrisalinas@gmail.com>
IUCN/SSC Primate Specialist Group logo courtesy of Stephen D. Nash, 2002.
Front cover: White-cheeked spider monkey (Ateles marginatus). Photo taken at Cristalino Private Heritage Reserve (RPPN), northern Mato Grosso,
Brazil. December 2016. Photo taken by Jessica Ward Lynch.
is issue of Neotropical Primates was kindly sponsored by the Margot Marsh Biodiversity Foundation, 432 Walker Road, Great Falls, Virginia 22066,
USA, and the Los Angeles Zoo, Director John R. Lewis, 5333 Zoo Drive, Los Angeles, California 90027, USA.
Neotropical Primates 25(1), December 2019 1
A
DEMOGRAPHIC DYNAMICS OF PERUVIAN BLACKFACED SPIDER MONKEYS (ATELES
CHAMEK) REINTRODUCED IN THE PERUVIAN AMAZON
Farah Carrasco-Rueda1 and Raúl Bello2
1School of Natural Resources and Environment, 103 Black Hall, PO Box 116455, Gainesville, FL 32611, USA.
Email: <farahcarrasco@gmail.com>
2Kawsay Biological Station - Taricaya Ecological Reserve. Puerto Maldonado-Perú. Email: <perbello25@gmail.com>
Abstract
Reintroductions of animals are important conservation tools for dierent taxa around the world. A reintroduction program
in the Peruvian Amazon is focusing on black-faced spider monkeys (Ateles chamek). We investigated life-history parameters
such as stage-specic survival and female fertility rates using a capture-mark-recapture framework and data from the litera-
ture. We estimated growth rate and probability of extinction for a reintroduced group using matrix models, as well as testing
whether population growth depends more on survival of juvenile females or adult females. Our results suggest the popula-
tion of the reintroduced group is decreasing. After projecting the group size for the next 25 years using dierent scenarios,
we found that in order for the group to persist, survival rate of the female adult stage needs to exceed 79 %. Given that group
growth rate is more sensitive to the survival of adult females, management measures actions that target this demographic are
required to guarantee survival of the group. Extrapolations of our results are subject to restrictions imposed by the small
sample size and the conditions specic to this reintroduction program. However, this study may provide valuable lessons for
reintroduction programs attempting the recovery of wild populations of similar species.
Keywords: Ateles chamek, Madre de Dios, matrix models, reintroduction
Resumen
La reintroducción de animales es una herramienta importante para la conservación de diferentes taxa a lo largo del mundo.
Un programa de reintroducción en la Amazonía peruana está enfocada en monos araña negros (Ateles chamek). Investigamos
los parámetros de historia de vida tales como la tasa de supervivencia por etapa especíca y fertilidad de las hembras, utilizan-
do el marco de referencia de captura-marca-recaptura y datos de literatura. Estimamos la tasa de crecimiento poblacional y
la probabilidad de extinción del grupo reintroducido utilizando modelos matriciales, asimismo, probamos si el crecimiento
poblacional depende de la supervivencia en las etapas de hembras juveniles o adultas. Nuestros resultados sugieren que la
población del grupo reintroducido está disminuyendo. Después de proyectar el tamaño grupal para los próximos 25 años
utilizando diferentes escenarios, encontramos que para para persistir la tasa de supervivencia de las hembras adultas debe ex-
ceder 79 %. Dado que la tasa de crecimiento del grupo es más sensible a la supervivencia de las hembras adultas, las acciones
de manejo deben enfocarse en este sector particular de la población para garantizar la supervivencia de la misma. Las extra-
polaciones de nuestros resultados están sujetas a restricciones impuestas por el reducido tamaño muestral y las condiciones
especícas del programa de reintroducción. Sin embargo, este estudio puede proveer lecciones valiosas para programas de
reintroducción que intenten recuperar poblaciones silvestres de especies similares.
Palabras clave: Ateles chamek, Madre de Dios, modelos matriciales, reintroducción
Introduction
Reintroductions consist of the re-establishment of species
in areas of their historical range where they have become
extinct or were extirpated (Seddon et al., 2014). Species
from a variety of taxonomic groups have been successfully
reintroduced in many parts of the world (barred bandicoot,
Backhouse et al., 1994; bison, Pyne et al., 2010; black-foot-
ed ferret, Santymire et al., 2014; California condor, Walters
et al., 2010; golden lion tamarin, Kierul et al., 2012; gray
wolf, Bangs and Fritts, 1996; guanaco, Barri, 2016; red
wolf, Hinton et al., 2013; scimitar-horned oryx, Woodne
and Gilbert, 2016; wild dog, Gusset et al., 2010). Rein-
troduction programs are considered a conservation tool
(Kleiman, 1989; IUCN, 1998), a strategy to deal with de-
faunation (Barri, 2016), and a way to deal with individu-
als conscated from illegal animal-tracking operations
(IUCN, 2002a). For species with high conservation value,
the reintroduction process should be conducted under a
well-dened management plan and result in reintroduced
Neotropical Primates 25(1), December 20192
individuals capable of survival in the wild without external
intervention (Griths et al., 1989; IUCN, 2002b). Fur-
ther, long-term post-release monitoring programs of rein-
troduced individuals or groups should be supported with
knowledge about the species’ ecology (Baker, 2002; Tray-
ford and Farmer, 2012).
A number of non-human primate species have been rein-
troduced into the wild (Konstant and Mittermeier, 1982;
Kleiman et al., 1986; King et al., 2011; Beck, 2017) with
varying degrees of success. Black-handed spider monkeys
(Ateles geoffroyi) on Barro Colorado Island (BCI), Panama,
is an example of a successful reintroduction (Milton and
Hopkins, 2005), which started with few individuals and
currently has a healthy population.
Spider monkeys (Ateles spp.) are long-lived Neotropical
primates that can live > 30 years (Link et al., 2018; Milton
and Hopkins, 2005; Ramos-Fernández et al., 2017), and
that exhibit long periods of maternal care (Di Fiore and
Campbell, 2005). Male:female sex ratios in wild popula-
tions of Ateles chamek (aka Ateles belzebuth chamek) were
reported in the range of 0.56-1 for adult and subadults
(mean 0.77 ± 0.22 SD, Shimooka et al., 2008). Spider
monkeys have a high degree of ssion-fusion dynam-
ics (Aureli et al., 2008; Di Fiore and Campbell, 2005),
where females disperse from social groups in search of
new mates whereas males are philopatric (McFarland
Symington, 1988). Unfortunately, most spider monkey
species are considered as “Endangered”, principally due
to their long-lived, slow reproducing, and social nature
makes them susceptible to habitat loss and overhunting
(Mittermeier et al., 1989). e Taricaya Rescue Center
started the “Program for the reintroduction of spider
monkeys in the southeastern Peruvian Amazon” in 2009
with the goal of reintroducing rescued and rehabilitated
black-faced spider monkeys (Ateles chamek) to the wild.
e Peruvian government legally recognizes this program
and approved of its management plan in 2012. Most of
the spider monkeys in the program were seized from il-
legal trackers or were being kept illegally as pets in Peru.
Twenty two black-faced spider monkeys were released
between 2011 and 2017 with the goal of establishing a
stable, self-sustaining group. Since reintroduction, the
program has carefully tracked the details of the release
process and post-release monitoring activities, including
monitoring animal behavior and resource use by the rein-
troduced spider monkeys (Bello et al., 2018). e future
of the group, constituted by 13 individuals (10 females
and three males) in 2017, is uncertain. Information on
demographic dynamics and projections of population
size over the next few decades is needed to help guide
program management decisions and for planning future
reintroductions.
In this paper, we address the following questions: (1) What
are the stage-specic survival rates and female fertility rates
for the group of reintroduced black-faced spider monkeys?
(2) What is the group’s population growth rate? and, (3)
What is the probability of the group extinction in the up-
coming decades? Based on what is expected for species that
are slow to mature and have low reproductive rates (Stahl
and Oli, 2006), we hypothesize that the population growth
rate of the reintroduced group of black-faced spider mon-
keys is more sensitive to the survival of adults than to any
of the other life stages. In this study we faced the challenge
of working with the small sample size of only a single group
of reintroduced black spider monkeys for estimating demo-
graphic parameters, which is why we also chose to include
estimates found in the literature. e sample size limita-
tion will restrict the extent to which context our results
can be extrapolated, however, we consider this study to be
important since reintroduction programs are only getting
more common, but data available on reintroduced popula-
tions are scarce and the outcomes of these programs are not
commonly reported.
Methods
Study Area
e reintroduction area is located on the south bank of
the Madre de Dios River inside the Tambopata Nation-
al Reserve in Madre de Dios Department, Tambopata
Province, and Tambopata District in southeastern Perú
(12°32’11.882” S, 69°00’14.227” W, 601 m.a.s.l.) (Fig.
1). is area consists primarily of subtropical wet forest
according to Holdridge life zones system; it may ood dur-
ing the wet season (INRENA, 2003) and it experiences an
average temperature and annual precipitation of 26.5 °C
and 2,387 mm, respectively (SENAMHI, 2015). e dry
season occurs from May to September and the wet season
from October to April.
Figure 1. Map with the location of the reintroduction area in
Madre de Dios, Perú.
Spider Monkey Data
We utilized data from seven consecutive years (2011 to
2017) and four release events (2011, 2013, 2014, and
2016) of rehabilitated black-faced spider monkeys (At-
eles chamek). Data were provided by the “Program for
Neotropical Primates 25(1), December 2019 3
the reintroduction of spider monkeys in the southeastern
Peruvian Amazon”. Data were collected by R. Bello and
a team of volunteers during the post-release monitoring
program. Individuals were identied by their body char-
acteristics, face coloration and behavior, and were each
assigned a name (Table S1 in Supplementary Material).
During the rst three months post-release, the activity of
each individual was constantly monitored. Details about
the monitoring procedure can be found in Bello (2018)
and Bello et al. (2018). In the year following the post-
release period, individuals were monitored during 2-3
days a week. Finally, following the rst year after release,
individuals were monitored twice a month to count in-
dividuals. Some individuals were equipped with radio
tracking collars that allowed them to be located more eas-
ily. Individuals were considered dead if they were not
sighted again after a month of searching. Each year that
an individual was sighted again was considered a “recap-
ture” in our analysis. Data collection on reintroduced
black-faced spider monkeys followed international stan-
dard guidelines for non-human primate reintroductions
(IUCN, 2002b).
Following MacFarland Symington (1988) and Shimooka
et al. (2008), each individual was assigned to the follow-
ing life stages: infants (0-12 months of life), juveniles (12-
60 months of life), subadult (60-96 months), and adult
(after 96 months or after the eight year of life). e data
included in this study involved 28 individual life histo-
ries, 22 of them corresponding to individuals that were
released into the wild when they were juveniles, sub-adult,
or adults, and six of them that were subsequently born in
the wild (Table S1 in Supplementary Material). Only six
of the 22 reintroduced individuals survived in the wild to
2017. Predation by harpy eagles (Harpia harpyja; three
events) and casual hunting (one event) accounted for the
death of four reintroduced individuals. In seven cases
(six females and one male) individuals disappeared and
their current whereabouts remains unknown. ough
they may have dispersed out of the study area, they were
considered as deceased for the purpose of this analysis. In
ve cases, four of which were female, individuals in poor
health conditions (individuals with fractures or infec-
tions) or individuals who separated from the group (Bello
et al., 2018) were removed from the wild by the monitor-
ing team and were taken to the Taricaya Rescue Center to
recover. In some cases, a second reintroduction attempt
took place once the individuals recovered to good condi-
tion. For the analysis, we did not consider data from
individuals following a second attempt at reintroduction.
Between 2013 and 2016, six individuals were born in the
wild from reintroduced parents. In 2017, the group of
reintroduced black-faced spider monkeys consisted of
12 individuals (1 adult male, ve adult females, 2 young
males, 4 young females), including six of the original re-
introduced individuals and six new individuals that were
born into this group post-reintroduction.
Parameter Estimation
Capture-Mark-Recapture Model
We used a Capture-Mark-Recapture (CMR) framework
and Cormarck-Jolly-Seber (CJS) models to estimate the
survival parameters as used in other studies (Campell and
Lagueux, 2005; Cormack, 1964; Kraus et al., 2008; Ol-
sen and Vøllestad, 2001). We estimated age-dependent
survival-rate parameters for dierent life stages assuming
post-breeding census. We assumed all individuals had the
same probability of being detected, and that there was no
migration into the group. To generate the models, we
transformed observation histories for each individual into a
Mark format database (Table S2, in Supplementary Mate-
rial). Removal but not subsequent reintroduction of indi-
viduals were accounted for in the analysis, and we only con-
sidered individuals’ life histories up until the rst removal
event. For analysis we pooled infants and juveniles into a
single life stage “young” (infants correspond to young 1), as
well as pooling adults and sub-adults for the analysis, since
reproductive maturity has been reported to occur after the
fth year of life, especially in males (Klein, 1971; Eisen-
berg, 1976; Milton, 1981; van Roosmalen, 1985), but was
also observed in females in this population (Bello et al.,
2018; R. Bello personal communication).
We generated three models using data from 2011 until
2017, considering each year as a discrete occasion. e
rst model was based on age and sex; the second only us-
ing age of the individuals; and the third model was based
on age from the female individuals only. Specic survival
rates for females were used for further analyses related to
fertility rate. We used program E-SURGE (Choquet et
al., 2008; Choquet et al., 2011) to estimate probability of
survival. Models were set to have the same probability of
detection for all individuals and a recapture probability
of one since all individuals were monitored. For details
on how we dened the eects on the parameters for each
model, see Supplementary material. We ran the mod-
els and selected the best model based on deviance values,
quasi Akaike information criterion (QAIC) and QAIC
corrected for small sample sizes (QAICc). e best model
was used to estimate the following parameters: probabil-
ity of an individual in young 1 stage to survive and grow
to young 2 stage (P1); probability of young 2 stage to
survive and grow to young 3 stage (P2); probability of
young 3 stage to survive and grow to young 4 stage (P3);
probability of young stage 4 to survive and grow to adult
stage (P4); and the probability of individuals surviving
and remaining as adults the next year (G5, Fig. 2). We
considered P2 to P4 to be the same (see Supplementary
Materials for model details). Due to the small sample
size, we used a randomization procedure to generate sim-
ulated sets of samples. For this we draw one individual
history at a time with replacement and extracted it from
the pool of individuals of this study. With the randomly
reduced pool of life-histories we ran the selected model in
Neotropical Primates 25(1), December 20194
E-SURGE using the package “R2SURGE” (Hines, 2017)
in R (R Development Core Team, 2015) to estimate the
survival probabilities. We repeated this 200 times to al-
low the model to approach the distribution of the esti-
mated parameters. Next, we estimated the mean value
of survival probability parameters and the condence in-
tervals for each of the dierent life stages. Additionally,
we estimated the percentage of individuals per stage that
survived along the study period, without considering the
individuals that were removed from the wild.
Fertility rate
In order to estimate the fertility rate for females in
the adult stage, we used an average inter-birth interval
34.5 ± 5.8 months (2.88 ± 0.48 years) reported for A.
chamek from wild populations in Manu National Park,
Perú (McFarland Symington, 1988). In other words, on
average 0.35 (range of values 0.3-0.42) individuals were
born per year. Since spider monkeys rarely produce
twins (Link et al., 2006), we standardized the number of
ospring per birth to one. We considered the probabil-
ity of newborns to be female as 0.73 (female:male sex
ratio among neonates 2.67:1 for A. chamek in Syming-
ton, 1987; and 2.7:1 for A. belzebuth Link et al., 2018)
so that the fecundity rate or average number of daugh-
ters per female spider monkey per year was 0.26 (range
of values 0.22 - 0.31). Using data from our study site
(2011-2017), we estimated fertility rates assuming post-
breeding census calculated as l(i)/l(i-1), where l(i) is the
probability of surviving from birth to age i (Caswell,
2001). e estimated fertility rate for reintroduced in-
dividuals was pooled into the life stage “adults”.
Stage-Structured Matrix Models
We constructed a matrix model (Caswell, 2001) including
survival rates per life stage (Fig. 2), including the fertility
rate of adults (F6).
For estimating population growth rate () of the reintro-
duced group, we used the stage-specic survival-rate pa-
rameter estimates obtained with the CMR analysis. We
projected the group size for the next 25 years - a period of
time that covers the life cycle of an individual spider mon-
key. For our projection, we used nine individual females
(number of females in the group by 2017) as initial group
and dierent sets of values for the stage-specic survival
parameters: (A) the estimated values, and (B) using pa-
rameter values reported in the literature for a wild popu-
lation of A. chamek (survival probabilities young 1 = 0.67
and adults = 0.97; McFarland Symington, 1988) and A.
geoffroyi (young = 0.9, from young to adult females = 0.9;
Milton and Hopkins 2005).
We ran an elasticity analysis to determine which life-history
parameters the population growth rate was more sensitive
to, proportionally. With this information, we generated a
fourth scenario (C) changing the parameter to which pop-
ulation growth was more sensitive by the threshold value
at which the population would start growing if all other
survival rate parameters had a value of one. For the analy-
ses, we used the “popbio” package (Stubben and Milligan,
2007) in R (R Development Core Team, 2015).
Figure 2. Life cycle graph of reintroduced black-faced spider
monkeys (Ateles chamek) in Madre de Dios, Perú, between 2011-
2016. P1-P4 are the probability of survival from one state to the
next. F6 is the fertility rate of adult individuals. G5 is the prob-
ability to remain in adult stage. Circles represent stage classes;
arrows and arcs represent transitions in survival and fertility rates.
Results
Parameter Estimation
Direct estimations using the data from individual histories
showed that the percentage of individuals that survived the
entire study period were: 100 % for young in their rst year
of life (for both sex, 4 females and 2 males), 83 % for fe-
males (n = 6) and 100 % for males (n = 1) in young stage
years 2 to 4, and 45 % for adult females (n = 11) and 20 %
for adult males (n = 5).
Under the CMR framework the model based on data from
only adult females showed the lowest QAIC value (Table
1). We used the survival rate parameters obtained from this
model to estimate specic fertility rates for females and for
further analysis (Table 2).
Table 1. Metrics of CMR models for Ateles chamek, Madre de
Dios, Perú, data from years 2011 to 2017. QAICc is QAIC cor-
rected for small sample sizes.
Model Number
of Parameters
Deviance QAIC QAICc
Stage & Sex 7 51.99 65.99 67.54
Stage 4 53.55 61.55 62.09
Females 4 34.25 42.25 43.02
Neotropical Primates 25(1), December 2019 5
Table 2. Stage-specic survival and fertility rates for Ateles cha-
mek in Madre de Dios, Perú, based on data from 2011 to 2017,
for the following scenarios: (A) using estimated parameter values,
(B) using parameter values reported in the literature (McFarland
Symington, 1988; Milton and Hopkins, 2005), and (C) chang-
ing the parameter to which population growth is more sensitive
to the value at which the population starts growing if all the other
parameters are maximized. CI = Condence interval.
Parameter Stage A 95 % CI B C
Survival
rate Young 1 0.717 0.711-0.724 0.67 1
Young 2 1 - 0.9 1
Young 3 1 - 0.9 1
Young 4 1 - 0.9 1
Adult 0.81 0.809-0.813 0.967 0.79
Fertility
rate Adult - 0.25 0.09
Stage-Structured Matrix Models
According to the group growth rates estimated using life
history parameters for female individuals (scenario A), the
reintroduced group will likely decrease (lambda = 0.98).
Under scenario A, we expect that the group would de-
crease to only ve individuals (Figure 3) over the next 25
years. Alternatively, scenario B (lambda = 1.06) predicts
an increase in the population to 40 female individuals (24
adults and 16 young) by year 25. e elasticity analy-
sis indicated that group growth rate was most sensitive
to small proportional changes in the adult stage survival
rate under scenarios A and B (elasticity values 0.49 and
0.67 respectively). When values of all other parameters
are maximized (values of 1.0; scenario C), adult survival
rate must be higher than 0.79 to achieve a positive group
growth rate (Fig. 3).
Figure 3. Projections for a reintroduced group of Ateles chamek
in Madre de Dios, Perú using data from 2011 to 2017 under
scenarios with dierent sets of values of survival probability: (A)
using the estimated parameter values, (B) using parameter values
reported in the literature (McFarland Symington, 1988; Milton
and Hopkins, 2005), (C) changing the parameter (to which group
growth is more sensitive) to the value at which the group starts
growing if all the other stage-specic parameters are maximized.
Discussion
Our results indicate that in order for this reintroduced
group of black-faced spider monkeys to persist over time,
it would be necessary to improve the probability of survival
for female individuals, especially those in adult stages. e
female-only model relies on the critical assumption that
the group requires the presence of adult males to ensure its
persistence in time, thus, the importance of males in the
group cannot be disregarded. e reintroduced population
of Ateles geoffroyi on Barro Colorado Island showed that
the presence of one adult male might be enough to main-
tain the group (Milton and Hopkins, 2005). By 2017, our
study group included one adult male, one infant male, and
Neotropical Primates 25(1), December 20196
one male juvenile of four years old. Losing the male in-
dividuals in the group will imply its extinction. e re-
introduction program will need to guarantee the presence
of males in the group over time to allow for breeding.
Under scenario A, and as a result of our small sampling
size, the estimated survival probability for young 2, young
3 and young 4 was 1.0. e lowest estimated probability
of survival was for female individuals in young 1 life stage.
Probability of adult survival may be biased because we only
had access to seven years of data, which is not enough to
estimate real adult survival rates, considering adults of
other species in the genus have been reported to live ~ 30
years (Milton and Hopkins, 2005; Ramos-Fernández et al.,
2017). is should be taken into account when consider-
ing whether or not to utilize the estimated survival rates
from this study in other contexts. e group remaining by
2017 was composed by 9 female individuals, accompanied
by three males, which can be considered to be adapted to
wild conditions. Group population growth rate based on
estimates from our study group (scenario A) indicated that
the reintroduced group was decreasing and would be close
to extinction in 25 years. However, projections obtained
under scenario B using parameters from the literature
showed the potential for an increase in population size,
reaching 40 individuals in 25 years. is last scenario is
based on survival rate value for a combination of wild (A.
chamek) and reintroduced (A. geoffroyi) individuals, which
imply dierent conditions that may or may not be reached
by the study group.
e elasticity analysis shows that the survival rate of
adult females is critical for population growth. ese re-
sults dier from those obtained in an elasticity analysis
of a free-ranging Ateles geoffroyi population in Yucatán,
Mexico, where survivorship of females during the rst 5
years was critical (Ramos-Fernández et al., 2017; Ramos-
Fernández et al., 2018). e same study also considered
critical the fertility of females between 17 and 21 years
old, which could not be measured in this study since we
ignored the exact age of the oldest adult individuals in
the group.
In the reintroduction experience at BCI, although only
four individuals (3 females, 1 male) survived from a group
of at least 18 individuals that were originally released, this
was sucient to allow the establishment of a group that
persisted over the rst seven years of the project (Milton
and Hopkins, 2005). Even though the context and spe-
cies considered are dierent from this study, it provides a
good example of how resilient species in the genus Ateles
can be. In this study, the group of monkeys reintroduced
in Madre de Dios included ve adult females of repro-
ductive age and only an adult male of reproductive age
since 2014, when a second male of reproductive age was
killed in a hunting event. By December 2016, six new
individuals had been born in the wild, including two o-
spring of the male killed in 2014. Since it is possible that
inbreeding problems will appear with only one reproduc-
tive male in the group, the survival of the other males
until their reproductive maturity needs to be guaranteed.
In order to secure the persistence of the population over
time, female survival rate of adult females needs to remain
above the specic thresholds of 0.79, below which the
population size of the group will not increase.
ere are several factors that were not considered in our
analysis of group population growth and may have aect-
ed our results. First, under the CMR framework it is not
possible to distinguish true mortality from permanent
emigration (Hunter et al., 2010). is may be critical for
spider monkeys because females emigrate to other groups.
Indeed, apparently two of the reintroduced females,
which are not in the group anymore, could have left after
remaining in the group for only two and three years (R.
Bello, personal communication). ese individuals were
in the age range for dispersal for Ateles belzebuth belzebuth
(63 to 79 months, Link et al., 2018). Moreover, ve fe-
male individuals were sighted two kilometers away from
the study group in August 2017, in an area where the
species is locally absent. According to Shimooka et al.
(2008), females may travel long distances searching for
new groups to join. It is likely that some of the individu-
als sighted away from the original group were considered
as deceased in this study. Another factor not considered
in our analysis is natal philopatry of males (McFarland
Symington, 1988). While male immigration may occur
under certain demographic circumstances (Aureli et al.,
2013), this exibility in their social system could inu-
ence the sex ratio in the group (Aureli et al., 2013). In
addition, we do not include habitat measurements that
would be useful to estimate the carrying capacity of the
area where the reintroductions are taking place. Further,
a study of the predator presence would be instrumental
for management decisions, since they play a key role in
the persistence of any group of spider monkeys (Shimoo-
ka et al., 2008).
Management actions are necessary to avoid extinction of
the group of black-faced spider monkeys reintroduced to
the Tambopata National Reserve in Perú. Specically, ac-
tions should focus on minimizing mortality risk of adults
and males in general. Reintroduced individuals that were
previously kept as pets may have issues in their adapta-
tion to the wild (Bello, 2018), despite the great eorts
to prepare them made by the reintroduction program
specialists. Reducing access of local hunters to the area,
and temporary removal and subsequent release of injured
individuals also might contribute to population growth.
In addition, future attempts to increase the size of the
group should focus on reintroducing reproductively t
individuals that arrive at the Taricaya Rescue Center
in early life stages. Further, individuals that will be re-
leased together should spend their rehabilitation period
as a group, avoiding future negative interactions in the
wild. To have a self-sustaining population, establishment
Neotropical Primates 25(1), December 2019 7
of other groups of reintroduced individuals in the same
area would be benecial, as it would allow movement of
females among groups. e nal goal is to create a meta-
population where the groups or populations could inter-
act and persist over time.
Finally, extrapolations of our results to populations of
free-ranging spider monkeys is not recommended due to
the restrictions imposed to our results as a consequence
of small sample size and specic conditions (i.e., intense
post-monitoring program, reintroduction area without
human activities). However, the life-history parameters
we estimated may serve as reference for other reintroduc-
tion eorts. Most reintroduction programs start with
only a few individuals sometimes releasing only one
group that may not persist in the wild in the mid-term.
However, this study may provide valuable lessons for re-
introduction programs attempting the recovery of wild
populations of similar species.
Acknowledgments
We thank Fernando Rosemberg and Stuart Timson from
Taricaya Ecological Reserve, Gabriel Ramos-Fernández for
sharing important references for this work, Madan Oli for
supporting FCR during the process of conceiving the ideas
of this article and early review, Diego Juarez-Sanchez for
early review of the manuscript, Jean-Dominique Lebre-
ton, Miguel Acevedo, James Hines, for their guidance in
data analysis, and John Blake, Dominique Lebreton, and
Mathew Hallett for their review of the manuscript. We
also thank Robinson Botero-Arias for support during early
stages of data analysis, and Flora W. Marynak and Liselot
Lange for grammar and spelling revision.
References
Aureli, F., Di Fiore, A., Murillo-Chacon, E., Kawamura, S.,
and Schaner, C. M. (2013) Male philopatry in spider
monkeys revisited. Am. J. Phys. Anthropol. 152(1): 86–95.
Aureli, F., Schaner, C. M., Boesch, C., Bearder, S. K.,
Call, J., Chapman, C. A., Connor, R., Di Fiore, A.,
Dunbar, R. I. M., Henzi, S. P., Holekamp, K., Korstjens,
A. H., Layton, R., Lee, P., Lehmann, J., Manson, J. H.,
Ramos-Fernández, G., Strier, K. B., Van Schaik, C. P.
2008. Fission-Fusion Dynamics: New Research Frame-
works. Curr. Anthropol. 49: 627–654.
Backhouse, G. N., Clark, T. W. and Reading, R. P. 1994.
Reintroductions for recovery of the eastern barred
bandicoot Perameles gunnii in Victoria, Australia. In:
Reintroduction biology of Australian and New Zealand
fauna, M. Serena (ed), pp.209–218. Surrey Beatty and
Sons, Chipping Norton, Victoria, Australia.
Baker, L. R. 2002. Guidelines for nonhuman primate re-
introductions. Re-introduction NEWS 21: 29–57.
Bangs, E. E. and Fritts, S. H. 1996. Reintroducing the
gray wolf to central Idaho and Yellowstone National
Park. Wildl. Soc. Bull. 24: 402–413.
Barri, F. R. 2016. Reintroducing Guanaco in the upper
belt of Central Argentina: Using population viability
analysis to evaluate extinction risk and management
priorities. Plos One 11(10): e0164806.
Beck, B. B. 2017. A History of Primate Reintroduction.
Website: http://www.drbenjaminbeck.com. Accessed 1
April 2018.
Bello, R. 2018. Comportamiento de monos arañas (At-
eles chamek) reintroducidos en el sureste de la amazonia
peruana. MSc esis, Universidad Nacional Agraria La
Molina, Lima, Peru. Pp. 100.
Bello, R., Rosemberg, F., Timson, S. and Escalante, W.
2018. Importancia del monitoreo postliberación de
monos araña (Ateles chamek) reintroducidos en el sur-
este de la Amazonia peruana. In: La primatología en
Latinoamérica 2. Ediciones IVIC, B. Urbani, M. Kow-
alewski, R. Grasseto Teixeira da Cunha, S. de la Torre
and L. Cortés-Ortiz (eds). Instituto Venezolano de In-
vestigaciones Cientícas (IVIC). Caracas, Venezuela.
Pp. 625–637
Campell, C. L., Lagueux, C. J. 2005. Survival probability
estimates for large juvenile and adult green turtles (Che-
lonia mydas) exposed to an artisanal marine turtle sh-
ery in the western Caribbean. Herpetologica 61: 91–103.
Caswell, H. 2001. Matrix population models. Second edi-
tion. Sinauer Associates, Sunderland, Massachusetts,
USA.
Choquet, R. and Nogue, E. 2011. E-SURGE 1.8 User’s
manual. CEFE, Montpellier, France.
Choquet, R., Lauriane, R. and Pradel, R. 2008. Program
E-SURGE: a software for fitting multievent models. In:
Modeling Demographic Processes in Marked Populations,
D. L. omson, E. G. Cooch, M. J. Conroy (eds),
pp.845–866. Environmental and Ecological Statistics,
Springer, New York, USA.
Cormack, R. M. 1964. Estimates of survival from sight-
ing of marked animals. Biometrika 51: 429–438.
Di Fiore, A. and Campbell, C. 2005. e atelines: Varia-
tion in ecology, behavior, and social organization. In:
Primates in perspective, C. J. Campbell, A. F. Fuentes,
K. C. MacKinnon, M. Panger, and S. Bearder (eds),
pp155–188. Oxford University Press, Oxford, United
Kingdom.
Dreitz, V. J. 2006. Issues in species recovery: An example-
based on the Wyoming toad. Bioscience 56: 765–771.
Eisenberg, J. F. 1976. Communication mechanisms and
social integration in the black spider monkey, Ateles fus-
ciceps robustus and related species. Smithsonian Contri-
bution to Zoology 213: 1–108
Griths, B., Scott, J., Carpenter, J. W. and Reed, C.
1989. Translocation as a species conservation tool: Sta-
tus and strategy. Science 245: 477–480.
Gusset, M., Stewart, G. B., Bowler, D. E. and Pullin, A.
S. 2010. Wild dog reintroductions in South Africa: A
systematic review and cross-validation of an endangered
species recovery programme. J. Nat. Conserv. 18(3):
230–234.
Neotropical Primates 25(1), December 20198
Hines, J. E. 2017. R2ESURGE- R package to automate
use of E-SURGE software. USGS-PWRC. http://www.
mbr-pwrc.usgs.gov/software/r2esurge.html.
Hinton, J. W., Chamberlain, M. J., Rabon, D. R., Jr.
2013. Red Wolf (Canis rufus) Recovery: A Review with
Suggestions for Future Research. Animals 3: 722–744.
Hunter, C. M., Caswell, H., Runge, M. C., Regehr, E. V.,
Amstrup, S. C. and Stirling, I. 2010. Climate change
threatens polar bear populations: a stochastic demo-
graphic analysis. Ecology 91(10): 2883–2897.
INRENA. 2003. Mapicación y Evaluación Forestal del
Bosque de Producción Permanente del Departamento
de Madre de Dios. Instituto Nacional de Recursos Na-
turales, Lima, Peru.
IUCN. 1998. International Union for Conservation of
Nature Guidelines for Re-introductions. IUCN/SSC
Re-introductions Specialist Group. IUCN Gland, Swit-
zerland and Cambridge, United Kingdom.
IUCN. 2002a. Guidelines for the Placement of Cons-
cated Animals. IUCN/SSC Re-introduction Specialist
Group. IUCN Gland, Switzerland, and Environmental
Research and Wildlife Development Agency, Abu Dha-
bi, United Arab Emirates. Website: https://portals.iucn.
org/library/sites/library/les/documents/2002-004.pdf.
Accessed 1 April 2018
IUCN. 2002b. Guidelines for Nonhuman Primate Re-
introductions. Special: Primate Issue. Newsletter of
the Re-introduction Specialist Group of IUCN’s Spe-
cies Survival Commission. News Re-introduction 21(6):
1560–3709.
Kierul, M. C. M., Ruiz-Miranda, C. R., Procopio de
Oliveira, P., Beck, B. B., Martins, A., Dietz, J. M.,
Rambaldi, D. M., Baker, A. J. 2012. e Golden lion
tamarin Leontopithecus rosalia: a conservation success
story. Int. Zoo Yearb. 46: 36–45.
King, T., Chamberlan, C. and Courage, A. 2011. Assessing
initial reintroduction success in long-lived primates by
quantifying survival, reproduction, and dispersal param-
eters: Western lowland gorillas (Gorilla gorilla gorilla) in
Congo and Gabon. Int. J. Primatol. 33(1): 134–149.
Kleiman, D. G. 1989. Reintroductions of captive mam-
mals for conservation: guidelines for reintroducing en-
dangered species into the wild. BioScience 39: 152–161.
Kleiman, D. G., Beck, B. B., Dietz, J. M., Dietz, L. A.,
Ballou, J. D. and Coimbra-Filho, A. F. 1986. Conser-
vation Program for the Golden Lion Tamarin: Captive
Research and Management, Ecological Studies, Educa-
tional Strategies, and Reintroduction. In: Primates, K.
Benirschke (ed), pp959–983). Proceedings in Life Sci-
ences. Springer, New York, USA.
Konstant, W. R. and Mittermeier, R. A. 1982. Introduc-
tion, reintroduction and translocation of Neotropical
primates: past experiences and future possibilities. Int.
Zoo Yearb. 22: 69–77.
Kraus, C., Eberle, M., Kappeler, P. M. 2008. e costs of
risky male behaviour: sex dierences in seasonal survival
in a small sexually monomorphic primate. Proc. R. Soc.
B. 275: 1635–1644.
Link, A., Milich, K., Di Fiore, A. 2018. Demography and
life history of a group of white-bellied spider monkeys
(Ateles belzebuth) in western Amazonia. Am. J. Primatol.
80 (8).
Link, A., Palma, A. C., Vélez, A. and de Luna, A.G. 2006.
Costs of twins in free-ranging white-bellied spider mon-
keys (Ateles belzebuth belzebuth) at Tinigua National
Park, Colombia. Primates 47(2): 131–9.
McFarland Symington, M. 1988. Demography, Ranging
Patterns, and Activity Budgets of Black Spider Monkeys
(Ateles paniscus chamek) in the Manu National Park,
Peru. Am. J. Primatol. 15: 45–67.
Milton, K. 1981. Estimates of reproductive parameters for
free-ranging Ateles geoffroyi. Primates 22(4): 574–579.
Milton, K., and Hopkins, M. E. 2005. Growth of a rein-
troduced spider monkey (Ateles geoffroyi) population on
Barro Colorado Island, Panama. In: New Perspectives in
the Study of Mesoamerican Primates: Distribution, Ecol-
ogy, Behavior, and Conservation, A. Estrada, P. A. Gar-
ber, M. S. M. Pavelka, and L. LeAndra Luecke (eds), pp
417–435. Springer, New York, USA.
Mittermeier, R. A., Kinzey, W. G. and Mast, R. B. 1989.
Neotropical primate conservation. J. Hum. Evol. 18:
597–610.
Olsen, E. M., and Vollestad, L. A. 2001. Estimates of
survival of stream-dwelling brown trout using mark-
recaptures. J. Fish Biol. 59: 1622–1637. DOI: 10.1006/
jfbi.2001.1812
Pyne, M. I., Byrne, K. M., Holfelder, K. A., McManus, L.,
Buhnerkempe, M., Burch, N., Childers, E., Hamilton, S.,
Schroeder, G., Doherty, P. F. 2010. Survival and Breeding
Transitions for a Reintroduced Bison Population: a Multi-
state Approach. J. Wildl. Manage. 74: 1463–1471.
R Development Core Team. 2015. R: A language and
environment for statistical computing. R Foundation
for Statistical Computing, Vienna, Austria. Website:
http://www.r-project.org. Accessed 10 April 2017.
Ramos-Fernández G., Smith Aguilar, S., Spaan, D., Ran-
gel Rivera, C. E., Schaner, C. M., Vick, L. G. and
Aureli, F. 2017. Demography and population viability
of spider monkeys Ateles geoffroyi. In: Proceedings of the
54th Annual Meeting of the Association for Tropical Biol-
ogy and Conservation, pp74. Mérida, Yucatán, México.
Ramos-Fernández, G., Aureli, F., Schaner, C. M. and
Vick, L. G. 2018. Ecología, comportamiento y conser-
vación de los monos araña (Ateles geoffroyi): 20 años de
estudio. Cap. 8. In: La primatología en Latinoamérica
2. Ediciones IVIC, B. Urbani, M. Kowalewski, R. Gras-
seto Teixeira da Cunha, S. de la Torre and L. Cortés-
Ortiz (eds). Instituto Venezolano de Investigaciones
Cientícas (IVIC). Caracas, Venezuela. Pp. 531–-543.
Santymire, R. M., Livieri, T. M., Branvold-Faber, H.,
Marinari, P. E. 2014. e Black-Footed Ferret: On the
Brink of Recovery? Reproductive Sciences in Animal Con-
servation: Progress and Prospects 753: 119–134.
Seddon, P. J., Griths, C. J., Soorae, P. S. and Armstrong,
D. P. 2014. Reversing defaunation: restoring species in
a changing world. Science 345(6195): 406–412.
Neotropical Primates 25(1), December 2019 9
SENAMHI. 2015. Datos históricos. Website: http://
www.senamhi.gob.pe/main_mapa.php?t=dHi. Ac-
cessed 17 Apr 2017.
Shimooka Y., Campbell, C., Di Fiore, A., Felton, A.,
Izawa, K., Nishimura, A., Ramos-Fernández, G. and
Wallace, R. 2008. Demography and group composition
of Ateles. In: Spider monkeys: Behavior, ecology and evolu-
tion of the Genus Ateles, C. J. Campbell, (ed), pp329–
350. Universidad Cambridge Press, New York, USA.
Stahl J. T. and Oli, M. K. 2006. Relative importance of
avian life-history variables to population growth rate.
Ecol. Model. 198: 23–39.
Stubben, C. J. and Milligan, B. G. (2007) Estimating
and Analyzing Demographic Models Using the popbio
Package in R. J. Stat. Softw. 22: 11.
Trayford, H. R. and Farmer, K. H. 2012. An assessment
of the use of telemetry for primate reintroductions. J.
Nat. Conserv. 20: 311–325.
Van Roosmalen, M. G. M. 1985. Habitat preferences,
diet, feeding strategy and social organization of the
black spider monkey (Ateles paniscus paniscus Linnaeus
1758) in Surinam. Acta Amaz. 15(3/4): 1-238.
Walters, J. R., Derrickson, S. R., Fry, D. M., Haig, S.
M., Marzlu, J. M., and Wunderle, J. M. 2010. Status
of the California condor (Gymnogyps californianus) and
eorts to achieve its recovery. Auk 127: 969–1001.
Woodne, T., Gilbert, T. 2016. e fall and rise of the
scimitar-horned oryx: a case study of ex-situ conserva-
tion and reintroduction in practice. Antelope conserva-
tion: from diagnosis to action [Conservation Science and
Practice no 16]: 280–296.
Supplementary material
Model parameter definitions
We dened eects on the parameters for each model as fol-
lows. e rst model is based on age and sex and we use
the notation g(3).a(1,2 3 4) + g(3).a(5) & g(1) + g(4).a(1,2
3 4) + g(4).a(5)&g(2), In this model, g(3) correspond to
young males, g(4) to young females, g(1) to adult males,
g(2) to adult females, and “a” refers to the age of young
individuals; the plus (+) sign separates individuals by
stage and sex. In the section that corresponds to males,
g(3).a(1,2,3,4) + g(3).a(5) & g(1), the rst part (before the
plus sign) accounts for the young males who stayed in that
stage during the rst four years of life. Since we deem the
youngest individuals to have lower survival probabilities,
we are considering the survival probabilities for ages 2, 3,
4 to be the same, the notation is (a(1,2 3 4)). e sec-
ond part correspond to adult male individuals, including
young males that reached the fth year of life and became
adults (g(3).a(5)) as well as the ones that were adults when
released into the wild (g(1)). For female individuals, the
interpretation is similar.
In the second model, the notation was g(1 2) & g(3 4).a(5)
+ g(3 4).a(1,2 3 4). e rst part before the plus sign cor-
responds to the adult stages including individuals of both
sexes that were already adults (g(1 2)) and the young in-
dividuals from both sexes that became adults in their fth
year of life (g(3 4).a(5)). e second part corresponds to
young individuals of both sexes during each of their rst 4
years of life: g(3 4).a(1,2,3,4).
In the third model, we dened the eects on the param-
eters for the model as follows: g(1)&g(2).a(5)+g(2).a(1,2
3 4). e rst part before the plus sign corresponds to
the female adult stages that were already adults (g(1)) and
the young female individuals that became adults in their
fth year of life (g(2).a(5)). e second part corresponds to
young female individuals during each of their rst 4 years
of life: g(2).a(1,2 3 4).
Table S1. Data for 28 individual life histories
ID Sex Age when
released
2011 2012 2013 2014 2015 2016 2017 Comments
RIVER female adult 1 1 1 1 1 1 1
ABIE female 3 1 1 1 1 1 1 1
MAQUI female adult 1 1 1 0 0 0 0 Removed
NIZZA female adult 0 0 1 0 0 0 0 Predated
WAWA female 0 0 0 1 1 1 1 1 Born in the wild
LUCHA female adult 0 0 0 1 1 1 1
MAYA female adult 0 0 0 1 1 0 0 Disappeared
CHOLA female adult 0 0 0 1 0 0 0 Disappeared
LILA female adult 0 0 0 1 1 1 1
SHUSHU female adult 0 0 0 1 1 1 0 Disappeared
Neotropical Primates 25(1), December 201910
(cont.)
ID Sex Age when
released
2011 2012 2013 2014 2015 2016 2017 Comments
CHINA female adult 0 0 0 1 1 1 1
GAIA female 0 0 0 0 0 1 1 1 Born in the wild
NICOL female adult 0 0 0 0 0 1 0 Disappeared
FE female adult 0 0 0 0 0 1 0 Disappeared
LOLA female 0 0 0 0 0 0 1 1 Born in the wild
ALIAH female 0 0 0 0 0 0 1 1 Born in the wild
NENA female 4 0 0 0 0 0 1 0 Removed same year
of release
FLACA female 3 0 0 0 0 0 1 0 Disappeared
PACHA female 4 0 0 0 0 0 1 0 Removed next
year of release
MARUJA female 5 0 0 0 0 0 1 0 Removed next
year of release
SAMBO male 3 1 1 1 1 1 1 1
CHAMEK male 4 1 1 1 1 0 0 0 Hunted
BALOU male 3 1 0 0 0 0 0 0 Predated
SIMON male adult 0 0 1 0 0 0 0 Removed same
year of release
OTTO male 4 0 0 1 0 0 0 0 Predated
PERU male infant 0 0 1 1 1 1 1
MARTIN male adult 0 0 0 0 0 1 0 Disappeared
RAYO male infant 0 0 0 0 0 1 1
Table S2. Individual histories in Mark format for the 28 individu-
als considered in this study. First column shows the individual
histories, second column correspond to adult males, third column
to adult female, fourth column to young males and fth column
to young females. “-1” indicates the individual was removed from
the group.
1111111 0 1 0 0 ;
1111111 0 0 0 1 ;
1110000 0 -1 0 0 ;
10000 0 1 0 0 ;
11111 0 0 0 1 ;
1111 0 1 0 0 ;
1100 0 1 0 0 ;
1000 0 0 0 1 ;
1111 0 1 0 0 ;
1110 0 1 0 0 ;
1111 0 1 0 0 ;
111 0 0 0 1 ;
10 0 1 0 0 ;
10 0 1 0 0 ;
11 0 0 0 1 ;
11 0 0 0 1 ;
10 0 0 0 -1 ;
10 0 0 0 1 ;
10 0 0 0 -1 ;
10 0 -1 0 0 ;
1111111 0 0 1 0 ;
1111000 0 0 1 0 ;
1000000 0 0 1 0 ;
10000 -1 0 0 0 ;
10000 0 0 1 0 ;
11111 0 0 1 0 ;
10 1 0 0 0 ;
11 0 0 1 0 ;
Neotropical Primates 25(1), December 2019 11
PROLONGED INTERSPECIFIC ASSOCIATION BETWEEN ATELES FUSCICEPS FUSCICEPS
AND ALOUATTA PALLIATA AEQUATORIALIS ATELIDAE IN A FOREST FRAGMENT IN NORTH
WESTERN ECUADOR
Paola Moscoso Rosero1,4, Sam Shanee2, Santiago Burneo3, Nathalia Fuentes 4, Felipe Alfonso-
Cortés4, Martín Obando5 and Diego G. Tirira5
1 Evolution Behaviour & Environment, School of Life Sciences, University of Sussex, Brighton, United Kingdom,
E-mail: < paola.moscoso.rosero@gmail.com>
2 Neotropical Primate Conservation, Manchester, United Kingdom
3 Museo de Zoología, Escuela de Biología, Pontificia Universidad Católica del Ecuador, Quito, Ecuador
4 Fundación Naturaleza y Arte, Proyecto Washu, Quito, Ecuador
5 Fundación Mamíferos y Conservación, Quito, Ecuador
Abstract
Changes in the behavior of primates caused by habitat disturbance are important indicators of their survival ability in frag-
mented landscapes. In Ecuador, few studies have examined the eect of habitat fragmentation on primate behavior. We
present data of a prolonged interspecic association between a brown-headed spider monkey (Ateles fusciceps fusciceps) living
within a troop of Ecuadorian mantled howler monkeys (Alouatta palliata aequatorialis) in a protected forest fragment in
northwestern Ecuador. We collected 274 hours of observations, at 10-minute intervals, on the A. f. fusciceps individual in
both the wet and dry seasons. Data included the amount of time that the A. f. fusciceps individual spent associating with,
and apart from, the A. p. aequatorialis troop. Our observations suggest a close relationship between the individuals of the
two species, with similarities in their behavior and diets found during the study. Interspecic communication was observed
frequently, with all A. p. aequatorialis individuals interacting directly with the A. f. fusciceps individual. e behavior of the
A. f. fusciceps individual was similar to that found in studies of other Ateles spp. living in fragmented and disturbed habitats,
but diered from that observed in other studies of the same species in continuous forest, suggesting adaptation to conditions
in fragmented habitat and possibly to living in close proximity with the howler troop.
Keywords: Primate behavior, habitat disturbance, symbiosis, adaptation.
Resumen
Cambios en el comportamiento de primates causados por la intervención de hábitat son indicadores importantes de habi-
lidad de supervivencia en ecosistemas fragmentados. En Ecuador existen pocos estudios que examinen los cambios en el
comportamiento de especies causados por la fragmentación. Este estudio documenta la asociación interespecíca entre un
mono araña de cabeza café (Ateles fusciceps fusciceps) conviviendo con una tropa de monos aulladores de la costa (Alouatta
palliata aequatorialis) dentro de un remanente de bosque protegido en el noroccidente del Ecuador. Colectamos 274 horas
de muestras instantáneas, registradas cada 10 minutos, de A. f. fusciceps durante las estaciones lluviosa y seca. El registro de
datos incluyó tiempo en el que A. f. fusciceps estaba asociado y separado de la tropa de A. p. aequatorialis. Los resultados
sugieren que la relación entre ambas especies es estrecha, con similitudes en los patrones de comportamiento y dieta en-
contrados a lo largo del estudio. Se observó con frecuencia una comunicación interespecíca, con todos los individuos de
A. p. aequatorialis interactuando de cierta forma directamente con A. f. fusciceps individualmente. El comportamiento del
individuo A. f. fusciceps fue similar a lo encontrado en otros estudios de Ateles spp. viviendo en hábitats fragmentados e inter-
venidos, pero diferente de lo observado en otros estudios de la misma especie en bosque continuo. Esto último sugiere una
adaptación a las condiciones de fragmentación de hábitat y posiblemente a la estrecha proximidad de la tropa de aulladores.
Palabras clave: Comportamiento de primates; alteración de hábitat; simbiosis; adaptación.
Introduction
Habitat destruction has led to reductions and isolation
of many primate populations and, as consequence, vari-
ous adaptations in behavioral and ecological responses in
primate communities have occurred (Marsh et al., 2013).
is has included changes in dietary selection, population
densities and group sizes, reproductive tness, stress levels
and susceptibility to disease (Martínez-Mota et al., 2007;
Schwitzer et al., 2011; Abondano and Link, 2012; Marsh
et al., 2013; Carretero-Pinzón et al., 2016; Rondón et al.,
2017) and those better able to adapt are, probably, more
likely to survive this habitat alteration, at least for the short
term (Schwitzer et al., 2011).
Neotropical Primates 25(1), December 201912
e four species of primates that inhabit the coastal region
of Ecuador are threatened by hunting, habitat loss and frag-
mentation (Rowe and Myers, 2016). e most threatened
species, the brown-headed spider monkey (Ateles fusciceps
fusciceps), is restricted to remaining areas of forest on Ecua-
dor’s Pacic coast. is species is listed as Critically Endan-
gered (Tirira et al., 2017; IUCN, 2018a) and is considered
one of the 25 most threatened primate species (Schwitzer
et al., 2017) due to a nearly 80 % reduction in its habi-
tat (Tirira et al., 2017). Hunting is also a major problem
for remnant populations of this species (IUCN, 2018a).
Similarly, the Ecuadorian mantled howler monkey (Alouat-
ta palliata aequatorialis) is threatened due to population
reduction from habitat loss and hunting (IUCN, 2018b)
and is considered Vulnerable by the IUCN (2018b) and
Endangered in the Red Book of the Mammals of Ecuador
(Tirira, 2011). Despite these species’ sympatry, no infor-
mation on a close long-term relationship between them has
been published to date.
Inter-specic associations have been documented in various
Neotropical primates (e.g. van Roosmalen, 1985; Pontes,
1997; de la Torre, 2000; Heymann and Buchanan-Smith,
2000; Deer, 2004; Lehman et al., 2006; Shanee et al.,
2007; Haugaasen and Peres, 2009; Silva and Ferrari, 2009;
Oliveira and Dietz, 2011; Shaer et al., 2016). ese as-
sociations provide advantages such as increased access to
resources and predator avoidance (Norconk, 1990; Ter-
borgh, 1990; de la Torre, 2000; Oliveira and Dietz, 2011).
Some studies report low levels of interspecic interactions
for Ateles spp. (van Roosmalen and Klein, 1988; Haugaas-
en and Peres, 2009), however, there are several published
observations of inter-specic associations between spider
monkeys and other sympatric primates (van Roosmalen,
1985; Deer, 2004; Shanee et al., 2007; Blake et al., 2010;
Link et al., 2011). Interspecic associations have also been
reported between Alouatta spp. and other primates (Pontes,
1997; Lehman et al., 2006; Haugaasen and Peres, 2009;
Silva and Ferrari, 2009), including with spider monkeys
(Cristóbal-Azkarate et al., 2015).
We conducted a short study on the activity budgets, diet
and inter-specic interactions of a solitary A. f. fusciceps liv-
ing with a group of A. p. aequatorialis in a forest fragment
in Ecuador. e aim of this study was to describe the pos-
sible behavioral and ecological responses of both species to
the intense anthropogenic disturbance in the area and their
close interspecic association.
Methods
Study site
e study was carried out in the Ashiringa Ecological Re-
serve, a private reserve in Pichincha province, Northwest-
ern Ecuador (00°04’24.9’’S, 78°58’04.4’’W). e reserve
consists of approximately 107 hectares of remnant forest
(~50 hectares of primary forest and ~57 hectares of second-
ary forest), and altitudes ranging from 500 to 700 meters.
e reserve is surrounded by a matrix of orchards, pasture
and artisanal sh farms. An unpaved road runs through the
reserve (Fig. 1).
Forests in the area are pre-montane evergreen Western
Andes Cordillera forest (Sierra, 1999) with multiple veg-
etation strata, with both lowland and premontane forests
(Guevara and Morales, 2013). Canopy height is 15 to 19
m with occasional emergent trees of up to 30 m with an
average diameter at breast height of 405 cm (Moscoso,
2010). Weather is very humid sub-tropical with daytime
temperatures between 17 and 26 °C and annual rainfall of
3,000 mm, and 500 mm in the wettest month (Hijmans
et al., 2005). Topography in the area is characterized by
steep hills which have contributed to the conservation of
remnant forest areas. e principle threats to habitat in
the area come from mining and human population growth
with its associated expansion of the agricultural frontier
leading to deforestation and isolation of remaining forest
fragments (Centro de Investigaciones Sociales del Milenio,
2006; Vandegrift et al., 2018).
Figure 1. Map showing the location of the study area, Ashiringa Ecological
Reserve, Pichincha Province, northwestern Ecuador.
Neotropical Primates 25(1), December 2019 13
Field surveys
Field work was carried out for four months in two periods:
during the wet season (September to October 2008) and
the dry season (June to July 2009). Focal animals were
followed daily between 06:00 and 18:00 (Brockelman and
Ali, 1987). At the start of the study period the A. p. ae-
quatorialis troop consisted of four individuals: one adult
male; one adult female with a dependent infant; and one
juvenile female. A juvenile male joined the group during
the last week of the study (July 2009). During the study
period, we did not nd any con-specics of A. f. fusciceps
in the surrounding area. Other groups of howler monkeys
are found in adjacent fragments, however no interactions
were observed with the A. f. fusciceps individual during the
study period.
We used a combination of focal animal sampling for ob-
servations of the A. f. fusciceps individual, and group scan
sampling for observations of the A. p. aequatorialis group
(Altmann, 1974), recording activity of each visible indi-
vidual in turn. We recorded activities every ten minutes
using ve previously dened, mutually exclusive behavioral
categories based on Martin and Batenson (2007): resting,
feeding, social activities, travelling, and vocalization (Ap-
pendix 1). We considered associations to be any time when
the A. f. fusciceps individual was with the howler group.
Details of all inter-specic interactions between individu-
als of both species were recorded in ve categories: body
contact, avoidance, aggression, play, and other. We identi-
ed food types consumed as: young leaves, mature leaves,
unripe fruit, ripe fruit, owers and other (including buds,
bark, nectar, bromeliads, ferns, and insects). Plant resourc-
es consumed by both species were collected and identied.
We also recorded forest strata used by all individuals at 10
minute intervals.
Data analysis
We calculated activity budgets using the frequency of oc-
currence of each behavioral category. We selected a 10
minutes interval between scans, and all data were averaged
to reduce pseudoreplication (Martin and Bateson, 2007).
Similarly, only non-parametric statistics were used as sam-
ple sizes were small and data may not have been normally
distributed. To estimate dietary preference, we calculated
frequencies for consumption of each food type as well as
frequencies of plant families and species consumed by A. f.
fusciceps. We tested for dierences in activity budgets and
dietary preferences using chi-square tests. To examine the
relationship between the A. f. fusciceps individual and the
A. p. aequatorialis troop we calculated frequencies for each
type of interaction between each pair of individuals, also
examining possible correlations in interactions between
seasons. We also compared activity budgets from our study
with those reported in the literature for Ateles spp. and Al-
ouatta spp.
Results
Activity budgets and association times
We collected 274 hours of behavioral data over 41 days (23
full day follows and 18 partial follows). ese were split
between 147.3 hours (21 days) and 126.6 hours (20 days)
during the wet and dry seasons, respectively. ere were
no dierences in seasonal activity budgets for each species
(all x², p > 0.05). Signicant dierences in activity budgets
were found between species in the wet season (x² = 25.259,
df = 4, p < 0.001), dry season (x² = 9.634, df = 4, p = 0.047)
(Fig. 2). Post-hoc tests (Bonferroni), with Alpha signi-
cance set to 0.05 (adjusted signicance for 10 compari-
sons = 0.005), showed that these dierences were in the
frequencies of resting and locomoting.
Figure 2. Comparative activity budgets between the wet and dry
seasons for Ateles fusciceps fusciceps and Alouatta palliata aequato-
rialis at Ashiringa Ecological Reserve, Pichincha Province, north-
western Ecuador.
Comparisons of the activity budget for A. f. fusciceps from
this study showed large dierences with those found for
Ateles spp. in other studies (Table 1).
Neotropical Primates 25(1), December 201914
Table 1. Comparison of activity budgets of Ateles spp. and Alouatta spp. from this and other studies.
Species Rest Social Feed Travel Vocalization Other Source
Ateles f. fusciceps 46 4 17 33 1 <1 is study
At. f. fusciceps 10 23* 37 30 - - Gavilánez-Endara (2006)
At. f. fusciceps 8 - 17 58 17 - Moscoso (2010)
At. f. fusciceps 20 10 20 34 14 - Moscoso (2010)
At. f. fusciceps - 10 - 80 - 10 Moscoso (2010)
At. f. fusciceps 25 4 36 30 - 4* Fuentes et al. 2018
Ateles belzebuth 61 - 22 10 - 7*** Klein and Klein (1977)
At. belzebuth 45 - 18 36 - 1*** Nunes (1995)
At. belzebuth 58 - 17 25 - 17*** Suarez (2006)
Ateles. chamek 45 - 29 26 - 12*** Symington (1988)
At. chamek 46 - 19 30 - 6*** Wallace (2001)
Ateles geoffroyi (Continuous
forest average)** 34 - 40 15 - 11 Chavez et al. (2011)
At. geoffroyi (Fragmented forest
average)** 34 - 48 9 - 10 Chavez et al. (2011)
At. geoffroyi 24 - 34 33 - 10*** Chapman et al. (1989)
Alouatta p. aequatorialis 50 5 18 25 2 <1 is study
Al. p. aequatorialis 14 39* 23 19 * - Gavilánez-Endara (2006)
Alouatta belzebul 59 - 20 18 - 3*** Pinto (2002)
Al. belzebul 56 - 8 19 - 17*** Bonvicino (1989)
Alouatta caraya. 62 - 16 18 - 5*** Bicca-Marques (1993)
Alouatta guariba 72 - 17 11 - 0*** Mendes (1989)
Al. guariba 58 - 19 19 - 5*** De Marques (1995)
Al. guariba 64 - 19 13 - 4*** Chiarello (1993)
Alouatta palliata 66 - 16 10 - 8*** Milton (1980)
Al. palliata 80 - 17 2 - 1*** Estrada et al (1999)
Al. palliata 73 - 18 8 - 2*** Teaford and Glander (1996)
Al. palliata 56 - 25 14 - 6*** Stoner (1996)
Al. palliata 57 - 14 27 - 2*** Williams-Guillen (2003)
Al. p. aequatorialis 66 8* 16 10 - - Milton (1980)
Alouatta pigra 62 - 24 10 - 4*** Silver et al (1998)
Al. pigra 83 - 10 4 - 3 Pozo-Montuy et al. (2013)
Alouatta seniculus 79 - 13 6 - 3*** Gaulin and Gaulin (1982)
Al. seniculus 67 - 22 11 - - Neves and Rylands
(1991)
Al. seniculus 63 - 22 10 - - Palma et al. (2011)
=* Including vocalizations, ** Author calculation, *** includes social, In Di Fiore et al. (2011).
Inter-specific interactions
Inter-specic associations between the species accounted
for 218.2 observation hours (80 %). Time spent in asso-
ciation between seasons was very similar, 83 % and 79 %
during the wet and dry seasons, respectively. Over half of
associations, 56 %, lasted the full follow, with the remain-
ing days’ associations being partial (34 %) or absent (10 %).
e 82 direct interspecic interactions observed were di-
vided into ve categories: body contact (42 %), avoiding
(22 %), aggression (7 %), play (17 %) and other (12 %).
Individual inter-specic interactions between the A. f.
fusciceps and A. p. aequatorialis group members showed
dierences between individuals. e juvenile female had
the most inter-specic interactions (41 %), followed by
Neotropical Primates 25(1), December 2019 15
Figure 3. Percentage of dietary components between season for
Ateles fusciceps fusciceps and Alouatta palliata aequatorialis.
Discussion
In this study both species had similar activity budgets,
which may be surprising due to the intrinsic dierences
in the species’ biology and ecology (Di Fiore et al., 2011).
Primates of the genus Ateles are physiologically adapted
to travel large distances in a short time which has a large
impact on their dietary requirements (Strier, 1992). On
the other hand, Alouatta spp. are known for their sedentary
behaviors and lower energetic requirements (Strier, 1992).
However, studies on Ateles spp. in fragmented and dis-
turbed habitats (i.e., under sub-optimal conditions), have
shown that they can adapt their behavior and diet to better
cope with available resources (Abondano and Link, 2012;
Schaner et al., 2012).
e only signicant dierences observed between the spe-
cies’ activity budgets, was, as expected, greater instances of
travelling and lower instances of resting by the A. f. fusciceps
individual. Spider monkeys tend to spend a large portion
of their time travelling, much higher than howler monkeys
(see Table 2). On the other hand, similar changes in activ-
ity budgets have been observed in some species of Ateles
living in fragmented habitat. Schaner et al. (2012) found
that a group of A. geoffroyi yucatanensis substantially altered
their activities in the aftermath of two hurricanes, reduc-
ing time spent travelling, whilst increasing time spent feed-
ing on leaves, compared to prior to the hurricanes. Other
studies have shown similar patterns in the behavior of A.
geoffroyi and A. hybridus in fragmented habitats (Abondano
and Link, 2012; Chaves et al., 2011). For example, Chavez
et al. (2011) reported that A. geoffroyi living in fragmented
forests spent less time traveling and more time feeding than
groups in continuous forest (Table 1).
Another interesting observation was the high percentage of
resting seen in the A. f. fusciceps individual (Fig. 2), which
again could be an adaptive behavior to living in sub-opti-
mal habitat (Abondano and Link, 2012; Schaner et al.,
the adult male (21 %), juvenile male (14 %), adult female
(13 %) and infant (10 %). Table 2 presents qualitative de-
tails of the interaction types observed. We also observed
multi-member interactions, and vocal communication be-
tween the howler group and the A. f. fusciceps individual
(group members responding to calls when ripe fruits were
encountered). On occasion the A. p. aequatorialis group
members would become agitated and vocally active when
the A. f. fusciceps individual would approach the juvenile
female, especially at the end of the dry season.
Table 2. Qualitative details of inter-specic interactions between
the A. f. fusciceps individual and A. p. aequatorialis group members.
A. palliata
group member
Frequency of
interaction (%)
Description
Juvenile
female
41 Body contact, involving
hugging, attempted
mounting, pulling of tails
and other body parts (by the
A. fusciceps), often received
with evasion or as play.
Adult
male
21 Evasion, as moving away
when the A. fusciceps came
close, aggression and
exploration of new areas
away from the group.
Juvenile
male
14 Aggression, evasion and body
contact
Adult
female
13 Body contact on few
occasions received with
evasion
Infant 10 Play
Diet
We observed 48 dierent plant species from 19 families
consumed by the A. f. fusciceps individual during the study
period (Appendix 2). Species from three families made
up over 50 % of plant resources consumed: Moraceae
(24 %), Fabaceae (17 %) and Cecropiaceae (12 %). Ripe
fruit was the most commonly consumed food type by the
A. f. fusciceps individual during the wet season (43 %),
followed by immature leaves (41 %). During the dry sea-
son this changed to a higher consumption of immature
leaves (62 %) and lower consumption of immature fruits
(15 %); these dierences were found to be signicant (x2
47.21, df = 5, p < 0.001). For A. p. aequatorialis immature
leaves were the most commonly consumed food type dur-
ing the wet season (52 %), followed by ripe fruit (34 %).
During the dry season, there was a higher consumption
of immature leaves (73 %) and lower of fruits (ripe fruit
9 % and immature fruit 8 %) these dierences were also
signicant (x2 29.62, df = 5, p < 0.001) (Fig. 3).
Neotropical Primates 25(1), December 201916
2012), although comparative resting times in Ateles geof-
froyi groups living in fragmented and continuous forest did
not show such marked patterns (Chaves et al., 2011 and
table 1). Similarly, Abondano and Link (2012) found that
A. hybridus living in heavily fragmented habitat in Colom-
bia spent more time resting than either feeding or travel-
ling (~40 % resting, and ~25 % in feeding and travelling,
respectively).
A. f. fusciceps individual in our study and those from other
studies of the same species (Gavilanez-Endara, 2006; Mos-
coso, 2010; Fuentes et al., 2018) show large dierences in
activity budgets (Table 1), especially in resting times, which
are generally much lower in A. f. fusciceps (Gavilanez-Enda-
ra, 2006; Moscoso, 2010; Fuentes et al., 2018). is may
have had a knock-on eect, including lower resource con-
sumption, as energetic requirements are lower with lower
activity levels (van Roosmalen, 1985; Symington, 1988;
Nunes, 1998; Suárez, 2006), and, the lower levels of travel
similarly related to less need to nd food, or vice-versa.
e inter-specic relationship observed is almost per-
manent and should not be considered as a casual asso-
ciation. e reason for the association could be that, as
social animals (Strier, 2015), the A. f. fusciceps individual
associated with the group as he could nd no conspecif-
ics in the area. Several well documented interspecic as-
sociations in Neotropical primates exist; in the Ecuadorian
Amazon, Sapajus macrocephalus and Saimiri cassiquiarensis
have a symbiotic relationship, where S. cassiquiarensis takes
advantage of the ability of S. macrocephalus to access other-
wise unattainable resources whilst S. macrocephalus gains an
early warning system against predation (de la Torre, 2000).
ere are also reports of multi-specic relationships, for ex-
ample between Callitrichids in the Bolivian, Brazilian and
Peruvian Amazon where species travel together all taking
advantage of the increased defensive benet and foraging
opportunities (Heymann and Buchanan-Smith, 2000).
e advantages of Ateles spp. ecological cognitive abilities
(Di Fiore and Suarez, 2007), combined with faster reaction
times, when compared to those of Alouatta spp. could be
useful in group defense.
ere have also been a handful of reports of inter-specic
relationships with species of the genus Ateles. Van Roos-
malen (1985) reported the formation of temporal sub-
groups with Chiropotes satanas. Most interestingly for this
study, Deer (2004) mentions a female A. belzebuth living
within a troop of A. seniculus in Colombia, and Shanee et
al. (2007) reported a solitary A. belzebuth associating with a
troop of Lagothrix flavicauda in Peru. at same individual
was seen associating with the same L. flavicauda troop on
several subsequent occasions (S. Shanee, pers. obs.), the
nearest known population of A. belzebuth is found ~10 km
to the Northwest. Possibly a dispersing animal got lost or
failed to be accepted into a new group and now associates
with the nearest acceptable alternative, although in this case
it is not a permanent association (S. Shanee, pers. obs.).
Even so, observations of interspecic associations, and par-
ticularly long-term associations, with Ateles spp. are scarce,
especially in competitive situations (van Roosmalen and
Klein, 1988). e types of interactions observed between
the A. f. fusciceps individual and each member of the howler
group was dierent. ere was a high level of interaction
with the juvenile female, the only reproductively available
member of the group when she reached the reproductive
age. Conversely, interactions observed with the group’s
males were more of a solely cooperative nature, commonly
observed intra-specically in groups of both Alouatta spp.
and Ateles spp. (Di Fiore et al., 2011).
Dietary preferences observed in the A. f. fusciceps individual
were similar to those reported for some other Ateles spp.
(van Roosmalen and Klein, 1988; Suárez, 2006). Although
the choice of items diered from previous studies on this
species (Gavilánez-Endara, 2006; Estévez-Noboa, 2009;
Tirira, 2011). e low consumption of ripe fruits by the
A. f. fusciceps individual was initially surprising, as was the
high consumption of young leaves in a predominantly fru-
givorous species. However, this kind of adaptation has been
seen in both A. hybridus and A. geoffroyi in fragmented or
heavily disturbed areas (Chaves et al., 2011; Abondano and
Link, 2012; Schaner et al., 2012; De Luna et al., 2017),
with both species consuming a much higher percentage of
leaves then expected from previous studies of Ateles spp.
Although diets were similar between the two species there
was separation in food resource consumption, especially
during the wet season, which might have reduced inter-
specic competition and facilitated the acceptance of the
A. f. fusciceps by the howler troop. Dietary separation was
noted by Deer (2004) as a possible mechanism to avoid
conict between sympatric populations of A. belzebuth and
Lagothrix lagothricha in the southern Colombian Amazon.
e dierences found in the diets of both species between
seasons will probably be a result of dierences in resource
availability (van Shaik et al., 1993), with both species con-
suming a wide variety of food types. e comparatively
high consumption of fruits by the A. p. aequatorialis group
could result from their availability (Milton, 1981; Janson
and Chapman, 1999) and possibly, from the absence of
other large bodied arboreal frugivorous in the Ashiringa
Reserve (José Macas, pers. comm.). e high consump-
tion of leaves by the A. f. fusciceps individual is probably
an adaptive behavior to survive in this highly fragmented
area (Abondano and Link, 2012; Schaner et al., 2012;
De Luna et al., 2017), where higher quality resources are
scarce, especially during the dry season.
An alternative, or at least complementary hypothesis for
the similarities we found between the species’ behaviour
and diets in this study, stems from the fact that similar
species living under the same ecological conditions and
environmental pressures can develop similar behavioural
and ecological tendencies, even more so than two sepa-
rate populations of the same species living under dierent
Neotropical Primates 25(1), December 2019 17
conditions (Strier, 2015). e similarity in activity budgets
between the species could be an adaptation of the A. f. fus-
ciceps’ activity rhythms to living with the A. p. aequatorialis
group, as well as to fragmentation. e observed associa-
tion could represent a symbiotic relationship, rather than
more tolerance (or even diculty on the part of the A. p
aequatorialis group in ‘escaping’ the presence of the A. f.
fusciceps individual), in that both benet from the relation-
ship (Strier, 2015). e A. f. fusciceps individual benets
from incorporation into a group, winning greater protec-
tion and social contact (Chance, 1955). Whereas, the A.
p. aequatorialis group benets through increased group size
for vigilance and in locating resources. e association also
appears to be stable, with the A. f. fusciceps individual re-
lating socially with all the howler group members. It is
likely that the philopatric dispersal system of Alouatta spp.
(Di Fiore et al., 2011) facilitated the acceptance/tolerance
of the A. f. fusciceps individual and/or that the individual
was adopted by the howler troop as an infant, which has
previously been reported by Strier (2015). However, this
interpretation would need much more investigation before
being accepted.
is study shows that forest fragmentation and popula-
tion reductions can lead to various adaptations in behav-
ioral and ecological responses in primates (Schwitzer et al.,
2011). It is possible that observations such as ours will
become more common in the future as habitats are reduced
and groups/individuals become increasingly isolated from
populations of conspecics.
Acknowledgments
We thank the Iniciativa de Especies Amenazadas Fernando
Ortiz Crespo of the Programa de Becas de Investigación
para la Conservación (PBIC), led by Fundación EcoCien-
cia and Conservation International for their nancial
support to this project. Rodrigo Arcos, Tjitte de Vries
and Omar Torres-Carvajal for their helpful suggestions.
Juan F. Freile for helping during the eldwork. e Her-
bario Nacional, especially Miguel Ángel Chinchero, for
the identications of botanical records. And Macas fam-
ily, landowners of Ashiringa Ecological Reserve, for their
help and hospitality.
References
Abondano, L. and Link, A. 2012. e social behavior of
brown spider monkeys (Ateles hybridus) in a fragmented
forest in Colombia. Int. J. Primatol 33: 1-15.
Altmann, J. 1974. Observational study of behavior: Sam-
pling methods. Behaviour 49: 227–266.
Blake, J. G., Guerra, J., Mosquera, D., Torres, R., Loiselle,
B. A. and Romo, D. 2010. Use of Mineral Licks by
White-Bellied Spider Monkeys (Ateles belzebuth) and Red
Howler Monkeys (Alouatta seniculus) in Eastern Ecuador.
Int. J. Primatol 31: 471-483.
Brockelman, W. Y. and Ali, R. 1987. Methods of surveying
and sampling forest primate populations. In: Primate Con-
servation in the Tropical Rain Forest, C. W. Marsh and R.
A. Mittermeier (eds.), pp.23–62. Alan R. Liss, New York.
Carretero-Pinzón, X., Deer, T. R., McAlpine, C. A. and
Rhodes, J. R. 2016. What do we know about the eect
of patch size on primate species across life history traits?
Biodiv. Cons. 25: 37-66.
Centro de Investigaciones Sociales del Milenio. 2006. Ob-
jetivos de desarrollo del Milenio. Estado de situación
2006. Provincia de Pichincha, Quito.
Chance, M. R. A. 1955. e Sociability of Monkeys. Man
55: 162–165.
Chaves, Ó. M., Stoner, K. E. and Arroyo-Rodríguez,
V. 2011. Seasonal dierences in activity patterns of
Georoyi´s Spider Monkeys (Ateles geoffroyi) living in
continuous and fragmented forests in Southern Mexico.
Int. J. Primatol. 32: 960-973.
Cristóbal-Azkarate, J., Urbani, B. and Asensio, N. 2015.
Interactions of Howler monkeys with other vertebrates:
A review. In: Howler monkeys: Behavior, ecology, and con-
servation, M. M. Kowalewski, P. A. Garber, L. Cortés-
Ortiz, B. Urbani and D. Youlatos (eds). pp.141-164.
Springer, New York.
De la Torre, S. 2000. Primates de la Amazonía del Ecuador.
Sociedad para la Investigación y Monitoreo de la Biodi-
versidad, Quito.
De Luna, A., Link, A., Montes, A., Alfonso, F., Mendieta,
L. Di Fiore, A. 2017. Increased folivory in brown spider
monkeys Ateles hybridus living in a fragmented forest in
Colombia. Endangered Species Res. 32: 123–134.
Deer, T. R. 2004. Primates of Colombia. Serie de Guías
Tropicales de Campo 4 Conservation International.
Bogotá.
Di Fiore, A. and Suárez, S. A. 2007. Route-based travel
and shared routes in sympatric spider and woolly mon-
keys: cognitive and evolutionary implications. Anim.
Cogn. 10: 317–329.
Di Fiore, A. F., Link, A. and Campbell, C. J. 2011. e
Atelines: behavior and socioecological diversity in a New
World monkey. In: Primates in Perspective. C. J. Camp-
bell, A. Fuentes, K. C. Mackinnon, R. M. Stumpf, and S.
K. Bearder (eds.), pp.156–185. Oxford University Press,
Oxford, UK.
Estévez-Noboa, M. 2009. Estudio poblacional y uso de hábi-
tat de Alouatta palliata, Ateles fusciceps y Cebus capucinus en
el Bosque Protector Los Cedros, provincia de Imbabura.
Bachelor thesis, Universidad Central del Ecuador, Quito.
Fuentes, N., Alfonso-Cortes, F., Duch-Latorre, I., Fonseca,
K., Cervera, L., Macías, Q., Loor, A., Kincez, K., Ur-
bina, S. 2018. Patrón de actividad, uso de estrato y dieta
del mono araña de cabeza café (Ateles fusciceps) en frag-
mentos de bosque del Cantón Flavio Alfaro, Provincia
de Manabí. In: Book of abstracts IV Congreso de ecu-
atoriano de Mastozoología, Loja
Gavilánez-Endara, M. 2006. Demografía, actividad y pref-
erencia de hábitat de tres especies de primates (Alouatta
palliata, Ateles fusciceps y Cebus capucinus) en un bosque
Neotropical Primates 25(1), December 201918
nublado del noroccidente Ecuatoriano. Bachelor thesis,
Ponticia Universidad Católica del Ecuador, Quito.
Guevara, J. and Morales, C. 2013. BsPn01 Bosque siem-
preverde piemontano de cordillera Occidental de los An-
des. In: Sistema de clasificación de los ecosistemas del Ec-
uador continental, MAE (ed.), pp.83–84. Ministerio del
Ambiente del Ecuador, Quito.
Haugaasen, T. and Peres, C. A. 2009. Interspecic primate
associations in Amazonian ooded and unooded forests.
Primates 50: 239–251.
Heymann, E. W. and Buchanan-Smith, H. M. 2000. e
behavioural ecology of mixed-species troops of Callitrich-
ine primates. Bio. Rev. 75: 169–190.
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G.
and Jarvis, A. 2005. Very high-resolution interpolated
climate surfaces for global land areas. Int. J. Climatol. 25:
1965–1978.
IUCN. 2018a. Ateles fusciceps. e IUCN Redlist of
reatened Species 2008. http://dx.doi.org/10.2305/
IUCN.UK.2008.RLTS.T135446A4129010.en. Ac-
cessed 21 May 2018.
IUCN. 2018b. Alouatta palliata ssp. aequatorialis. IUCN
Redlist of reatened Species 2008. http://www.iuc-
nredlist.org/details/919/0. Accessed 25 June 2018. Ac-
cessed 21 May 2018.
Janson, C. H. and Chapman, C. A. 1999. Resources and
primate community structure. In: Primate communities.
(eds.), pp.237–267. Cambridge University Press, Cam-
bridge, UK.
Lehman, S. M., Sussman, R. W., Phillips-Conroy, J. and
Prince, W. 2006. Ecological biogeography of primates in
Guyana. In: Primate biogeography: Progress and prospects.
S. M. Lehman, and J. G. Fleagle (eds.), pp.105–130.
Springer US, Boston, MA.
Link, A., Galvis, N., Fleming, E. and Di Fiore, A. 2011.
Patterns of mineral lick visitation by spider monkeys and
howler monkeys in Amazonia: are licks perceived as risky
areas? Am. J. Primatol. 73: 386–396.
Martínez-Mota, R., Valdespino, C., Sánchez-Ramos, M. A.
and Serio-Silva, J. C. 2007. Eects of forest fragmenta-
tion on the physiological stress response of black howler
monkeys. Anim. Cons. 10: 374–379.
Marsh, L. K., Chapman, C. A., Arroyo-Rodríguez, V.,
Cobden, A. K., Dunn, J. C., Gabriel, D., Ghai, R., Nij-
man, V., Reyna-Hurtado, R., Serio-Silva, J. C. and Was-
serman, M. D., 2013. Primates in fragments 10 years
later: once and future goals. In: Primates in fragments
(editors) (eds.), pp.505–525. Springer, New York.
Martin, P. and Bateson, P. 2007. Measuring behaviour: An
introductory guide. Cambridge University Press, United
Kingdom.
Milton, K. 1981. Food choice and digestive strategies of
two sympatric primate species. Am. Nat. 117: 496–505.
Moscoso, P. 2010. Estado poblacional del mono araña de
cabeza café (Ateles fusciceps) en el noroccidente del Ecua-
dor, con notas ecológicas de una relación interespecíca
con Alouatta palliata. Bachelor thesis, Ponticia Univer-
sidad Católica del Ecuador, Quito.
Neves, A. M. S. and Rylands, A. B. 1991. Diet of a group
of howling monkeys, Alouatta seniculus, in an isolated
forest patch in Central Amazonia. Acta Primatologica 3:
263–274.
Norconk, M. A. 1990. Introductory remarks: Ecological
and behavioral correlates of polyspecic primate troops.
Am. J. Primatol. 21: 81–85.
Nunes, A. 1998. Diet and feeding ecology of Ateles bel-
zebuth belzebuth at Maracá Ecological Station, Roraima,
Brazil. Folia. Primatol. 69: 61–76.
Oliveira, L. C. and Dietz, J. M. 2011. Predation risk and
the interspecic association of two Brazilian Atlantic for-
est primates in Cabruca agroforest. Am. J. Primatol. 73:
852–860.
Palma, A. C., Vélez, A., Gómez-Posada, C., López, H.,
Zárate, D. A. and Stevenson, P. R. 2011. Use of space,
activity patterns, and foraging behavior of red howler
monkeys (Alouatta seniculus) in an Andean forest frag-
ment in Colombia. Am. J. Primatol. 73: 1062–1071.
Pontes, A. R. M. 1997. Habitat partitioning among pri-
mates in Maracá Island, Roraima, Northern Brazilian
Amazonia. Int. J. Primatol. 18: 131–157.
Pozo-Montuy, G., Serio-Silva, J.C., Chapman, C.A. and
Bonilla-Sánchez, Y.M. 2013. Resource Use in a Land-
scape Matrix by an Arboreal Primate: Evidence of Sup-
plementation in Black howlers (Alouatta pigra). Int. J.
Primatol. 34: 714–731.
Rondón, S., Ortiz, M., León, C., Galvis, N., Link, A. and
González, C. 2017. Seasonality, richness and prevalence
of intestinal parasites of three Neotropical primates (Al-
ouatta seniculus, Ateles hybridus and Cebus versicolor) in a
fragmented forest in Colombia. Int. J. Parasitol Parasites
Wildl. 6: 202–208.
Rowe, N. and Myers, M. 2016. All the worlds primates. Po-
gonias Press. Providence, País.
Schaner, C. M., Rebecchini, L., Ramos-Fernandez, G.,
Vick, L. G. and Aureli, F. 2012. Spider Monkeys (Ateles
geoffroyi yucatenensis) Cope with the Negative Conse-
quences of Hurricanes rough Changes in Diet, Activ-
ity Budget, and Fission–Fusion Dynamics. Int. J. Prima-
tol. 33: 922–936.
Schwitzer, C., Glatt L, Nekaris, K. A. I. and Ganzhorn J. U.
2011. Responses of animals to habitat alteration: an over-
view focussing on primates. End. Species Res. 14: 31–38.
Schwitzer, C., Mittermeier, R. A., Rylands, A. B., Chiozza,
A. B., Williamson, E. A., Mace, E. J., Wallis, J. and Cot-
ton, A. 2017. Primates in Peril: e World’s 25 Most En-
dangered Primates 2014-2016. IUCN/SSC Primate Spe-
cialist Group, International Primatological Society (IPS),
and Conservation International, Arlington, VA.
Shaer, C. A., Barnett, A. A., Gregory, T., De Melo, F.,
Moreira, L., Alvim, T. H., Moura, V. S., Filó, A., Car-
doso, T., PortCarvalho, M. and Santos, R. R. D., 2016.
Mixedspecies associations in cuxiús (genus Chiropotes).
Am. J. Primatol. 78: 583–597.
Shanee, S., Shanee, N. and Maldonado, A. M. 2007. Inter-
specic association between Oreonax and Ateles, Amazo-
nas, Peru. Neotrop. Primates 14: 34–35.
Neotropical Primates 25(1), December 2019 19
Sierra, R. 1999. Propuesta preliminar de un Sistema de cla-
sificación de vegetación para el Ecuador continental. Quito:
INEFAN/GEF-BIRF and EcoCiencia, Quito.
Silva, S. S. B and Ferrari, S. F. 2009. Behavior patterns of
southern Bearded Sakis (Chiropotes satanas) in the frag-
mented landscape of Eastern Brazilian Amazonia. Am. J.
Primatol. 71: 1–7.
Strier, K. B. 1992. Atelinae adaptations: Behavioral strat-
egies and ecological constraints. Am. J. Phys. Anthropol.
88: 515–524.
Strier, K. B. 2015. Primate Behavioral Ecology. Routledge,
New York.
Suárez, S. A. 2006. Diet and travel costs for spider mon-
keys in a nonseasonal, hyperdiverse environment. Int. J.
Primatol. 27: 411–436.
Symington, M. M. 1988. Demography, ranging patterns,
and activity budgets of black spider monkeys (Ateles
paniscus chamek) in the Manu National Park, Peru. Am.
J. Primatol. 15: 45–67.
Terborgh, J. 1990. Mixed ocks and polyspecic associa-
tions: Costs and benets of mixed groups to birds and
monkeys. Am. J. Primatol. 21: 87–100.
Tirira, D. G. (ed.). 2011. Libro Rojo de los mamíferos del Ec-
uador. 2nd edition. Fundación Mamíferos y Conservación,
Ponticia Universidad Católica del Ecuador y Ministerio
del Ambiente del Ecuador. Publicación Especial. 8. Quito.
Tirira, D. G., Méndez-Carvajal, P. G., and Morales-Jimé-
nez, A. L. 2017. Brown-Headed Spider Monkey Ateles
fusciceps Gray, 1866. In: Primates in Peril: e World’s 25
Most Endangered Primates 2016–2018. C. Schwitzer, R.
A. Mittermeier, A. B. Rylands, F. Chiozza, E. A. William-
son, E. J. Mace, J. Wallis and A. Cotton (eds.), pp.40–
43. IUCN SSC Primate Specialist Group, International
Primatological Society, Conservation International, and
Bristol Zoological Society, Arlington, VA.
Vandegrift, R., omas, D., Bitty, A.R., and Levy, M.
2018. Alcance de las concesiones mineras recientes en Ecua-
dor. Unpublished report. Rainforest Information Center,
Nimbin, New South Wales, Australia.
van Roosmalen, M. G. 1985. Habitat preferences, diet,
feeding strategy and social organization of the Black Spi-
der Monkey [Ateles paniscus paniscus Linnaeus, 1758] in
Surinam. Acta Amaz. 15: 7–238.
van Roosmalen, M. G. and Klein, L. 1988. e spi-
der monkeys, genus Ateles. In: Ecology and Behavior of
Neotropical Primates, Vol. 2. R. A. Mittermeier, A. B. Ry-
lands, A. Coimbra-Filho, and G. A. B. da Fonseca (eds.),
pp.455–537. World Wildlife Fund, Washington, D.C.
van Shaik, C. P., Terborgh, J. W. and Wright, S. J. 1993.
e phylogeny of tropical forests: adaptive signicance
and consequences for primary consumers. Annu. Rev.
Ecol. Syst. 24: 353–377.
Appendices
Appendix 1. Description of behavioral denitions for Ateles fusciceps fusciceps and Alouatta
palliata aequatorialis at Ashiringa Ecological Reserve, Pichincha Province, northwestern Ecuador.
Behavioral
category
Behavioral
sub-category
Definition
Resting To be inactive in either a standing, sitting or lying position (either alone or in a
group) including auto-grooming.
Feeding
Feeding To handle, process or consume any food item.
Foraging To be actively and engaged in searching for food items as the predominant
behavior.
Locomotion
To purposefully change location, either within or between trees, or further.
is is exclusive of incidental movement whilst foraging or engaged in another
behavior within the same tree.
Vocalization To be primarily active in calling, exclusive of vocalizations during play, aggressive
or sexual encounters.
Social
activities
Play To be actively engaged in repetitive, exaggerated and disjointed, solitary or social
behavior with no observable goal (exclusive of all other active behaviors).
Sexual To be engaged in copulation or related behaviors.
Allo-grooming
To be primarily engaged in non-aggressive physical contact with another
individual (either grooming or being groomed by another individual or
individuals, exclusive of sexual contact).
Aggression/evasion
To attack, provoke or show fear towards a conspecic from within the same
group or with another group (including vocalizations, branch shacking, mooning
and physical contact).
Other Watching observer.
Out of sight.
Neotropical Primates 25(1), December 201920
Family Scientific name
Item
Apocynaceae Aspidosperma
spruceanum
Young leaves
Apocynaceae Forsteronia
myriantha
Young leaves
Bromeliaceae Bromelia spp. Young leaves
Boraginaceae Cordia hebeclada Flowers
Boraginaceae Cordia eriostigma
fruits
Cardiopteridaceae Dendrobangia
boliviana
Mature fruits
Cecropiaceae Cecropia garciae Hearts
Cecropiaceae Coussapoa herthae
fruits
Cecropiaceae Coussapoa contorta Mature leaves
Cecropiaceae Coussapoa spp. Fruits
Cecropiaceae Pourouma spp. Leaves
Ericaceae Macleania pentaptera Flowers
Euphorbiaceae Tetrorchidium
macrophyllum
Mature fruits
Fabaceae Dioclea spp.Young leaves
Fabaceae Pterocarpus officinalis Young leaves
Fabaceae Abarema
barbouriana
Leaves
Fabaceae Inga acuminata Fruits
Fabaceae Inga pezizifera Leaves
Fabaceae Inga lallensis Leaves/mature
fruits
Fabaceae Inga nobilis Leaves
Fabaceae Inga silanchensis Fruits
Fabaceae Inga oerstediana Fruits/leaves
Fabaceae Dussia lehmannii Mature fruits
Family Scientific name
Item
Meliaceae Carapa guianensis Bark
Meliaceae Guarea kunthiana Mature fruits
Moraceae Castilla spp. Fruits
Moraceae Sorocea jaramilloi Mature fruits
Moraceae Ficus trigona Leaves
Moraceae Ficus spp. Young leaves
Moraceae Ficus tonduzii Leaves
Moraceae Ficus maxima Young leaves
Moraceae Ficus rieberiana Leaves
Moraceae Ficus cuatrecasasiana Young leaves
Moraceae Naucleopsis naga Leaves
Moraceae Maquira guianensis Young leaves
Moraceae Ficus cuatrecasasiana Leaves
Moraceae Ficus carchiana Young leaves/hearts
Moraceae Brosimum utile Leaves/mature
fruits
Myristicaceae Virola reidii Mature fruits
Myrtaceae Myrcia fallax Leaves/mature
fruits
Myrtaceae Psidium spp. Mature fruits
Rubiaceae Guettarda ochreata Mature fruits
Rubiaceae Guettarda hirsuta Mature fruits
Sapindaceae Paullinia capreolata Leaves
Sapindaceae Billia rosea Mature fruits
Sapotaceae Pouteria capacifolia Young leaves/fruits
Solanaceae Solanum spp.Fruits
Violaceae Gloeospermum
grandifolium
Mature fruits/leaves
Appendix 2. List of plants consumed by A. f. fusciceps at Ashiringa Ecological Reserve, Pichincha Province, northwestern Ecuador.
Neotropical Primates 25(1), December 2019 21
DEMOGRAPHY, HABITAT USE AND ACTIVITY BUDGET OF A WILD GROUP OF BLACK-FACED
BLACK SPIDER MONKEYS (ATELES CHAMEK) IN LAS PIEDRAS, SOUTH-EASTERN PERÚ
Liselot Roos Lange1, 2 and Nicola Marie Robson3
1Association for Research and Conservation in the Amazon (ARCAmazon),
Jr. Billinghurst 433, Puerto Maldonado, Madre de Dios, Peru. E-mail <liselotlange@gmail.com>
2 Junglekeepers Peru, Jr. Junin 17C-18, Puerto Maldonado, Madre de Dios, Peru.
3Faculty of Health and Medical Sciences, University of Surrey, Stag Hill, Guildford GU2 7XH, United Kingdom.
E-mail <nickirobson.uk@gmail.com>
Abstract
Spider monkeys are one of the main seed-dispersal agents in the Amazonian ecosystem and therefore help regenerate the
rainforest. e black-faced black spider monkey (Ateles chamek) is internationally recognized as Endangered, and its range
is limited to Peru, Bolivia and Brazil. Spider monkeys are a dicult genus to study and little is known about their popula-
tions in the wild. Here we present the results of a study on demography, habitat use, activity budget and preliminary notes
on ranging pattern and diet of a wild group of A. chamek studied in a oodplain forest in south-eastern Peru. e group
(in total eight to nine individuals) had a home range of approximately 1.6 km2 (160 hectares) with a daily path length of
approximately 1,200 m. e group was encountered at canopy levels above 20 m in height 75.2% of the time and rarely
descended to lower forest levels. ere was a weak but signicant positive correlation between the number of encounters
with individuals of the study group and the number of feeding trees in an area (R2 = 0.38, N = 93, P > 0.001). e majority
of their diet consisted of fruits, followed by leaves. Resting accounted for 41.9% of their activity budget, with foraging
accounting for 30% and traveling 23.8%. Most ndings of this study are consistent with other studies on the species, but
we found that the group size in our study was unusually small. However, this did not seem to have an inuence on home
range size or activity budget.
Keywords: spider monkey, Ateles, demography, home range, activity budget, habitat use, ranging pattern, diet.
Resumen
Los monos araña son uno de los principales agentes de dispersión de semillas en el ecosistema amazónico y por lo tanto
ayudan a regenerar la selva. El mono araña negro (Ateles chamek) está reconocido internacionalmente como En Peligro, y
su área de distribución se limita a Perú, Bolivia y Brasil. Los monos araña son un género difícil de estudiar y se sabe poco
sobre sus poblaciones en estado silvestre. Aquí se presentan los resultados de un estudio sobre demografía, uso del hábitat,
presupuesto de actividades y notas preliminares sobre la pauta de distribución y la dieta de un grupo silvestre de A. chamek
estudiado en un bosque de llanura inundable en el sudeste del Perú. El grupo (en total, ocho o nueve individuos) tenía un
área de distribución de aproximadamente 1.6 km2 (160 hectáreas) con una longitud de recorrido diario de aproximadamente
1,200 m. El grupo se encontró en niveles de copas de más de 20 m de altura el 75,2 % del tiempo y rara vez descendió a
niveles inferiores del bosque. Hubo una correlación positiva, débil pero signicativa, entre el número de encuentros con los
individuos del grupo de estudio y el número de árboles en que se alimentan en una zona (R2 = 0,38, N = 93, P > 0,001). La
mayoría de su dieta consistió en frutos, seguidos de hojas. El descanso representó el 41,9% de su presupuesto de actividades,
la búsqueda de alimento el 30% y los viajes el 23,8%. La mayoría de los hallazgos de este estudio son consistentes con otros
estudios sobre la especie, pero encontramos que el tamaño del grupo en nuestro estudio era inusualmente pequeño. Sin
embargo, esto no pareció tener inuencia en el tamaño del área de distribución o en el presupuesto de actividades.
Palabras clave: mono araña, Ateles, demografía, rango de hogar, presupuesto de actividad, uso de hábitat, patrón de reco-
rrido, dieta.
Introduction
Spider monkeys (genus Ateles, Fig. 1) represent some of
the most charismatic and ecologically-important primates
found in the neotropical rainforest. e genus Ateles con-
sists of seven species (following Groves, 2001; Morales-Ji-
ménez et al., 2015) which occur in tropical forests ran-
ging from Mexico to Bolivia (Collins, 2008). However,
Ateles are under serious threat from both habitat loss and
poaching. Little is known about the demography and
behavior of distinct populations, as Ateles are a particular-
ly hard genus to study due to their preference for higher
canopy levels. Ateles have evolved distinct morphological
characteristics which allow them to thrive in the highest
level of the forest canopy (Campbell et al., 2005; Rosen-
berger et al., 2008; Hooper, 2014). Many aspects of their
Neotropical Primates 25(1), December 201922
physiology are distinct from other primates and are spe-
cialized for movements such as below-branch suspension
and brachiation, rather than leaping and quadrupedal tra-
vel (Fontaine, 1990; Rosenberger et al., 2008; Lindshield
and Rodrigues, 2009). For instance, skeletal modica-
tions to the wrist and elbow, and the absence or reduction
of the thumb, all assist Ateles in these suspensory activities
which are essential for life in the canopy (Rosenberger et
al., 2008; Lindshield and Rodrigues, 2009). In addition
to specialized forelimbs, Ateles also possess a prehensi-
le tail that can support the animal’s entire body weight
(Youlatos, 2008).
visiting clay licks, eating soil or decaying wood, and during
social conicts (Campbell et al., 2005).
Ateles exhibit a larger home range than other primates in
the same habitat due to the distribution of fruit patches
(Takahashi, 2008; Deer, 2010). Home ranges of Ateles
have been recorded between 32 and 900 ha with daily path
lengths between 500 and 5,600 m (McFarland Symington,
1988a; Wallace, 2006, 2008; Spehar, Di Fiore and Link,
2010; González-Zamora et al., 2012, 2015; Velázquez-Váz-
quez et al., 2015).
e activity budget of Ateles is often described using four
mutually exclusive categories: resting, foraging, traveling,
and other (see Table 1) (McFarland Symington, 1988a;
Wallace, 2001). On average, social behaviors account for
less than ve percent of Ateles activity budgets (Slater, Scha-
ner and Aureli, 2007, 2009), which is less than for most
primates. e largest portion of Ateles daily activity budget
(nearly half) consists of resting (White, 1986; McFarland
Symington, 1988a; Nunes, 1995; Wallace, 2001). Trave-
ling accounts for between 14.8 and 32.6% of the activity
budget, and foraging between 18 and 50.5% (Chapman,
Chapman and McLaughlin, 1989; Wallace, 2006). Time
spent resting and traveling is likely inuenced by levels of
fruit abundance and distribution.
Ateles feed 70 to 90% of the time on large-seeded fruits
(Di Fiore et al., 2008; Felton et al., 2008). Ateles are very
important seed dispersal agents as they rarely masticate the
seeds and instead swallow them whole, therefore contri-
buting to the regeneration of forests (Link and Di Fiore,
2006; González-Zamora et al., 2012; Link et al., 2012).
In times of fruit scarcity, Ateles complement their diet with
leaves, owers, seeds, decaying wood, clay, soil, and a very
small percentage of invertebrates (Di Fiore et al., 2008;
Rylands and Mittermeier, 2013).
Spider monkeys are of particular interest to primatologists
because they exhibit a ssion-fusion social structure similar
to that of chimpanzees, which is unique among Neotro-
pical primates (Anaya-Huertas and Mondragón-Ceballos,
1998). is structure involves the division of a group, that
can consist of over 50 individuals, into temporary sub-
groups (Shimooka et al., 2008). Subgroups uctuate in
size and composition throughout the day, averaging three
to four individuals at a time (Van Roosmalen, 1985; Cha-
pman, 1988; Shimooka, 2005; Lange, 2016). Due to the
clumped distributions of their primary food sources (Gon-
zález-Zamora et al., 2008) and the fact that Ateles often de-
plete fruit supplies in their feeding trees (Chapman, 1988),
this social system evolved to reduce intragroup competition
for food resources (Asensio et al., 2008; Spehar and Di Fio-
re, 2013). erefore, group ssion is evoked when fruit is
scarce, and conversely, fusion occurs in instances of high
fruit availability (Asensio et al., 2008; Aureli and Schaner,
2008). Hence, subgroups need to visit fewer food patches
to nd sucient food (Aureli and Schaner, 2008).
Figure 1. An example of Ateles chamek with its distinct morpholo-
gical characteristics, e.g. the long limbs and prehensile tail. Photo
credit: Liselot Lange (2016).
Ateles usually prefer primary, closed-canopy forests (Mi-
chalski and Peres, 2005; Wallace, 2008; Salvador et al.,
2011), and they are found to spend more than 70% of the
time in the higher canopy levels above 25 m (Van Roos-
malen, 1985; Wallace, 2008). Ateles may be restricted to
the highest canopy levels due to dietary and physical spe-
cialization. Ateles are extremely frugivorous (Campbell et
al., 2005; Wallace 2008), and ripe fruit is seldom found in
lower forest levels (Campbell et al., 2005). Furthermore,
their shoulder joint modications and elongated forelimbs
do not allow for terrestrial quadrupedism, making it harder
for Ateles to visit the ground (Campbell et al., 2005). ey
are believed to descend to the forest oor only for drinking,
Neotropical Primates 25(1), December 2019 23
Most research on spider monkeys has been conducted in
protected areas (González-Zamora et al., 2008), and little is
known about their behavioral ecology in unprotected areas
(Hagell, Whipple and Chambers, 2013). In this study, we
report the demography, habitat use, activity budget and
preliminary notes on ranging patterns and diet of Ateles
chamek in an area not part of a national park or reserve.
Methods
Study site
is study was conducted at the Las Piedras Amazon Cen-
ter (LPAC), a 4,465-hectare ecotourism and conservation
concession run by the non-governmental organization
(NGO) the Alliance for Research and Conservation in the
Amazon (ARCAmazon). e site is located in the Madre
de Dios department of Peru (-12.0709367 S, -69.5005917
W), approximately 65 km from the town of Puerto Mal-
donado and 55 km from the border with Brazil. e site
consists of terra rme and oodplain forest ranging from
200 to 400 m in elevation along the Las Piedras River. Our
research was conducted between May 2016 and Decem-
ber 2017. During this time, minimum temperature ave-
raged 22°C, maximum temperature 35°C, humidity levels
averaged between 60 and 90% and average daily rainfall
between 10 and 220 mm (Weather Underground, 2019;
World Weather Online, 2019). Field work was based out
of the research center at LPAC, which takes up less than
one hectare of the land and consists of sleeping platforms
and communal areas. e concession contains approxima-
tely 37 km of mapped trails, some of which were used to
observe the focal group in the north-east of the concession.
A stream (the Loboyoc) cuts from the south-west to the
north-east of the concession and joins with the Las Piedras
River. e stream is traversable by the study group which
has multiple crossing points along its course. Within the
concession, multiple groups of spider monkeys are found
without any major geographical boundaries separating the
groups. is study solely focused on one of the groups in
the north-east of the concession.
e river shed of Las Piedras is an extraction forest, and
most concessions are used for the exportation of Brazil nuts
and timber. Hunting (mostly illegal) is a common prac-
tice in the concessions surrounding LPAC, as the region
does not lie within a national park or reserve and there is
little protection for wildlife. ARCAmazon acquired the
LPAC-concession in April 2015 with the aim to preserve
the land and create a corridor for ora and fauna while
forming alliances with other NGOs and landowners. Ten
species of non-human primates are found within the con-
cession (Lange, 2016).
Subjects
e focal group consisted of eight well-habituated, indivi-
dually recognizable Ateles chamek at the start of the study
(May 2016). As there had been tourism in the years befo-
re the study, the spider monkeys had become accustomed
to the presence of humans. ere were three adult males
(Ezra, Luca, Scar) and ve females, where we group both
subadult and adult females into one category (Juno, Mami,
Manchas, Flor, Rose). e individuals were identied by
facial characteristics and were given names to ease data
collection and communication in the eld. roughout
the study, the group’s composition uctuated due to dea-
th and newborn individuals. In August 2016 an infant
male (Leaf) was born to Juno. Later in June 2017, the ol-
dest female (Manchas) passed away from natural causes.
e remains were discovered in a decomposing state, after
which it was discovered that the subject’s left ankle and
foot were missing. Post-mortem examination showed the
animal had worn teeth and brittle bones; indicators of old
age. e individual also had a healed fracture of the left
humerus, but did not show limitations in movement whi-
lst alive. Around the same time of this death, a female
infant (Maya) was born to Mami. By the end of the study
(December 2017), the group consisted of three adult males
(Ezra, Luca, Scar), two (sub)adult females (Flor, Rose), two
lactating females (Juno, Mami), one juvenile male (Leaf),
and one infant female (Maya).
Data collection
e data on Ateles chamek were collected through focal fo-
llows of the study subjects. Follows took place in surveys
between 05:00 and 19:00, covering all hours in which
Ateles are known to be active. Existing trails within the
concession were walked at a slow speed (between one and
two km/h) to locate the study group. Upon encountering
a subgroup or the entire group, a random individual was
chosen for the focal observations. In this study data were
collected only on adult individuals, as the infants and ju-
veniles’ behavior is strongly correlated with their mother’s
behavior. Data were collected on adult males, sub and
adult females (without ospring), and lactating females
(with ospring). Behavioral data were collected on the
focal individual every fth minute, using instantaneous
focal sampling (Altmann, 1974). For gathering data on
their activity budget, the following categories were used;
traveling, resting, foraging, and other (Table 1). e
forest level use of the focal individual was also recorded
every fth minute (between the ground and 10 m high,
between 10 m and 20 m high, or above 20 m high). e
focal animal was followed for one hour, until out of sight
for more than ten minutes, until no longer possible to
follow, or until the sun set and the focal settled at a slee-
ping site. After one hour of following a focal individual, a
new individual was selected. e focal individual’s move-
ments were recorded by creating a track with a handheld
GPS-system (GARMIN 64s).
Data were also collected on diet by recording and identif-
ying food items consumed by the spider monkeys (fruits,
owers, leaves, bark, clay or invertebrates). Additionally,
ad libitum data were taken on social interactions and group
composition. Finally, all feeding trees and sleeping sites
were marked with the GPS-system.
Neotropical Primates 25(1), December 201924
Table 1. Description of the used activity categories.
Activity categories Description
Traveling Moving for more than thirty seconds or
between trees
Resting Sleeping, being stationary or small
movements less than thirty seconds
Foraging e looking for, handling of, or ingestion
of food or water
Other Behaviors not tting into any of the other
categories, e.g. social interactions between
individuals, interaction with observers,
defecating and/or urinating
Data analysis
All GPS data were uploaded into the computer software
Basecamp (Garmin Ltd., 2019). By creating a polygon
of the outer points of A. chamek encounters and follows,
we calculated the home range (in ha) and created a map
presenting habitat usage (Fig. 2). Additionally, a second
map was created showing the distribution of the feeding
trees and sleeping sites within the home range (Fig. 3). A
non-parametric regression analysis was used to verify whe-
ther a correlation exists between grid-cell use and the num-
ber of feeding trees present within that cell. An estimation
of the encountered subgroups’ daily path length was made
by calculating their average speed during a follow and mul-
tiplying this by average time spent traveling per day. e
group’s activity budget was calculated by combining the
frequency of behavior in all samples. e activity budgets
of adult males, (sub)adult females (without ospring) and
lactating females (with ospring) are compared through
descriptive analyses. No statistical analyses were applied
due to the small sample size. All food items consumed
were categorized (fruits, owers, bark, clay and invertebra-
tes) and frequency of consumption of each category was
expressed as a percentage of all feeding observations throu-
ghout the study.
Results
A total of 1,519 instants, obtained from 149 focal fo-
llows, were analyzed. On average the focal follows lasted
45.60±20.11 minutes.
Demography
Total group size uctuated between eight and nine indivi-
duals over the course of the study due to one death and two
newborns. Observed subgroup size ranged from one to
nine individuals, with an average of 4.63±1.92 members.
e subgroups also varied in composition (Fig. 2). e
most common type of subgroup consisted of one or more
females with their ospring, which accounted for 41.2%
of encounters. e second most common group observed
was both males and females with ospring, which accoun-
ted for 31.9% of subgroups. Interestingly, while 10.9% of
observed subgroups consisted of males only, female-only
subgroups without ospring were never encountered. e
percentage of solitary encounters were low, with solitary
females and males accounting for only 3.4 and 3.6% of
subgroups respectively. For the group as a whole, male to
female ratio at the start of the study was 1:1.67, but this
decreased to 1:1.25 by the end of the study.
Figure 2. A histogram showing the relative frequency of A. cha-
mek subgroup types encountered (n= 119 encounters).
Habitat use
e group occupied forest levels higher than 20 m for
75.2% of the time, levels between 10 and 20 m for 23.2%
of the time and were rarely found below 10 m. e home
range was approximately 160 ha, consisting entirely of
oodplain forest. Figure 3 shows the intensity of area use
within the home range and includes bordering areas (repre-
sented in white) rarely or not visited by the study group.
A signicant positive correlation was found between the
number of feeding trees within a cell and the frequency
of Ateles chamek encounters within that cell (R2 = 0.38,
N = 93, P < 0.001). Figure 4 shows the distribution of
79 feeding trees and four sleeping sites that were located
throughout the study period.
Neotropical Primates 25(1), December 2019 25
Figure 4. One-hectare grid map with the distribution of feeding
trees and sleeping sites throughout the home range of the focal
Ateles chamek group at the Las Piedras Amazon Center, Peru.
Preliminary notes on ranging pattern
On average, the individuals encountered traveled two
hours and 47 minutes per day and their speed was approxi-
mately 440 m per hour. is means the group’s estimated
daily path length was 1,200 m per day. More in-depth
research is required to determine whether subgroup size has
an inuence on ranging patterns.
Activity budgets
e activity budget of the spider monkeys consisted of
41.9% resting, 23.8% traveling, 30% foraging and 4.3%
other behaviors. e category ‘other’ consisted of 3.8%
social interactions between group members, for instance
aliative behaviors such as playing and handling other
female’s ospring, and also agonistic behaviors such as ag-
gressive chases. e remaining time was spent on behaviors
such as urination, defecation, and interaction with obser-
vers. Our results (see Figure 5) show that lactating fema-
les (with ospring) spent the least time resting out of the
three age-sex classes of A. chamek, and (sub)adult females
(without ospring) spent most time resting. In regard to
traveling, adult males traveled most and lactating females
(with ospring) least. Lactating females (with ospring)
spent far more time foraging than the other two age-sex
classes, with adult males spending the least amount of time
foraging. Lastly, adult males demonstrated other behaviors
more frequently, such as interactions with observers and
social behaviors.
Preliminary notes on diet
A total of 383 records of foraging events were analyzed for
the study period. e majority of the group’s diet con-
sisted of fruits (84.4%, n=325), with leaves being the se-
cond most consumed item (9.7%, n=37). e group su-
pplemented these food items with small amounts of seeds,
owers and bark. One instance of geophagy was observed
where a lactating female (with ospring) consumed clay
from an arboreal ant nest.
Figure 3. One-hectare grid map of the approximately 160 ha
home range of the focal Ateles chamek group at the Las Piedras
Amazon Center, Peru, showing the frequency of encounters wi-
thin each cell.
Figure 5. Dierences in activity budgets between three dierent
age-sex classes of Ateles chamek.
Discussion
e total size of this particular group (eight to nine indi-
viduals) is unusually small at this site. Other (sub)groups
within the concession with larger numbers of individuals
(usually between 15 and 20) were sighted and we have no
clear understanding of why the study group in particular
is so small. Despite no clear geographical boundaries exis-
ting within the concession, no interactions were recorded
between the study group and other Ateles groups. Previous
Neotropical Primates 25(1), December 201926
research on the genus and species report larger group sizes,
between 15 and 50 individuals per group (Van Roosmal-
en, 1985; McFarland Symington, 1988a; Shimooka et al.,
2008). However, one long-term study by Ramos-Fernan-
dez et al. (2005) followed a group of Ateles geoffroyi of a
similar size (8 adults); this group lived within a fragmen-
ted forest, and the habitat was likely a major limitation on
their group size. e average subgroup size that we found
was, however, very similar to other studies (van Roosmalen,
1985; Chapman, 1988; Shimooka et al., 2008). erefore,
it appears that subgroup size is not correlated with group
size. We propose that a possible reason for subgroup size to
be around this number is to maximize safety. It is possible
that smaller subgroups are less likely to detect a potential
predator whilst more likely to be predated upon. Further-
more, it is likely that smaller subgroups are less capable of
defending their territory against rival Ateles groups. e sub-
group composition also stayed similar to groups with more
individuals (Chapman 1990), where females with ospring
were the most common composition of subgroups. is is
expected, as females without ospring are known to display
maternal behaviors towards other female’s ospring, poten-
tially to practice motherhood themselves and, therefore,
stay close to these females (Slater et al. 2007). e male
to female ratio within the focal study group was found to
be lower than most other groups studied (Chapman, et al.
1989), however, we do not consider this surprising due to
the extremely small size of the focal group.
e home range that we found is similar to the home ranges
reported in other studies (McFarland Symington, 1988a;
Wallace, 2008). We had anticipated a much smaller home
range considering the small size of this group compared
to group size in other studies on the genus. Campos et al.
(2014) state that there is a positive relationship between
primate group size and home range size, and it would be
reasonable to assume that a smaller group would experien-
ce less competition for resources and thus would not have
to travel as far to meet resource demand. erefore, their
equally sized home range could be explained by a potential
fruit scarcity in the focal group’s home range, causing them
to travel further to nd sucient resources. By conducting
a more in-depth study on the ecology of their home range
(through botanical plots) we could more accurately reveal
whether fruit abundance has an inuence on home range
size in this case. In contrast to Campos, Wallace (2008)
found that home range size did not correlate with resident
Ateles group size, and therefore there may be other factors
contributing to home range size other than group size and
food availability. For instance, noise disturbance and the
presence of humans could force communities to retreat to
less disturbed areas (Kirkby et al., 2000; González-Zamora
et al., 2012), hence increasing home range size. We expect
that a construction project that took place at the Las Pie-
dras Amazon Center (within the group’s home range) du-
ring the study could have caused the group to range further
than expected. However, comparative data from after the
construction period is required to determine whether home
range size and ranging patterns were aected.
Daily path lengths for spider monkeys appear to vary large-
ly (Symington et al., 1988a, Nunes, 1998). Our ndings
present a shorter average daily path length than the average
reported by Symington et al. (1988a) and Nunes (1998),
however this is likely due to the larger group size of the
groups in those studies (18 to >35 individuals). Larger
group size would likely mean the spider monkeys need to
cover more distance on a daily basis to nd sucient re-
sources, hence explaining why the study group has shorter
daily path lengths.
During the study we observed one feeding event of geopha-
gy, in which a lactating female (with ospring) consumed
clay from an arboreal ant’s nest. e main reasons for soil
consumption by animals are to supplement the animal’s
diet with minerals otherwise unobtainable, and that the
consumption of soil supposedly aids in detoxication and
alleviation of gastrointestinal problems (Link et al., 2011).
It appears that geophagy is more common during particu-
lar life history events like lactation or pregnancy (Link et
al., 2011, Pebsworth, et al., 2018). Whereas other studies
report Ateles spp. consume clay at clay licks, we did not
identify any clay licks within the group’s home range. Ar-
boreal ant nests and termitaria could be a source of mine-
rals for primates in areas where there are fewer or no clay
licks available. e mineral composition of termitaria and
ant nests is usually even higher than that of topsoil (Veiga
and Ferrari, 2007). is allows Ateles to obtain minerals
whilst staying in the canopy. Further research is required to
better understand the physiological factors driving geopha-
gy in spider monkeys, to gain insight into the increased
consumption of clay during specic life events and nally
to understand the use of arboreal ant nests and termitarium
for clay consumption.
Lactating females (with ospring) rested least out of the
dierent age-sex classes. We expected lactating females to
spend the most time resting in order to compensate for the
exertion of carrying and nursing a young. However, time
spent resting can sometimes serve as a pool from which
time needed to accomplish other behaviors can be drawn
(Dunbar, 1988). In this case, it is possible that resting time
was substituted for foraging time as the lactating females
spent the most time foraging. We assume that this is due to
the energy demands for lactating females being higher than
those without a dependent young.
Although the study site is not located within any govern-
ment-protected area, no noticeable dierences were found
in the habitat use and activity budget of the study group
in comparison with studies conducted within governmen-
tal-protected areas. Further research is required on the
populations of Ateles along the Las Piedras River shed to
create large-scale conservation strategies for this region.
Neotropical Primates 25(1), December 2019 27
Acknowledgements
We thank the sta at ARCAmazon and LPAC for all su-
pport provided throughout the study and all volunteers
and research assistants that helped with data collection and
analysis.
References
Altmann, J. 1974. Observational Study of Behavior: Sam-
pling Methods. Behaviour, 49(3): 227–266.
Anaya-Huertas, C. and Mondragón-Ceballos, R. 1998.
Social behavior of Black-Handed Spider Monkeys (Ate-
les geoffroyi) reared as home pets. Int. J. Primatol. 19(4):
767–784.
Asensio, N., Korstjens, A.H., Schaner, C. M., Aureli, F.
2008. Intragroup aggression, ssion-fusion dynamics
and feeding competition in Spider Monkeys. Behaviour.
145(7): 983–1001.
Aureli, F., Schaner, C. M., Verpooten, J., Slater, K. and
Ramos-Fernández, G. 2006. Raiding parties of male Spi-
der Monkeys: Insigths into human warfare? Am. J. Phys.
Anthropol. 131: 486–497.
Aureli, F. and Schaner, C. M. 2008. Social interactions,
relationships and the social system of spider monkeys.
In: Spider Monkeys: Behavior, Ecology and Evolution of the
Genus Ateles, C. J. Campbell (ed.), Rev. ed., pp. 236–265,
Cambridge University Press, Cambridge, New York.
Bello, R., Rosemberg, F., Timson, S. and Escate, W. 2017.
Importancia del monitoreo postliberación de monos ara-
ña (Ateles chamek) reintroducidos en el sureste de la Ama-
zonia peruana. In: La primatología en Latinoamérica 2, B.
Urbani, et al. (eds). Instituto Venezolano de Investigacio-
nes Cientícas (IVIC), Caracas.
Campbell, C. J., Aureli, F., Chapman, C. A., Ramos-Fer-
nández, G., Matthews, K., Russo, S. E., … Vick, L.
2005. Terrestrial behavior of Ateles spp. Int. J. Primatol.
26(5): 1039–1051.
Campos, F. A., Bergstrom, M. L., Childers, A., Hogan, J.
D., Jack, K. M., Melin, A. D., … Fedigan, L. M. 2014.
Drivers of home range characteristics across spatiotem-
poral scales in a Neotropical primate, Cebus capucinus.
Anim. Behav. 91: 93–109.
Chapman, C. A. 1988. Patch Use and Patch Depletion by
the Spider and Howling Monkeys of Santa Rosa National
Park, Costa Rica. Behaviour. 105(1): 99–116.
Chapman, C. A. and Chapman, L. J. 1990. Reproductive
biology of captive and free-ranging spider monkeys. Zoo
Biol. 9: 1–9.
Chapman, C. A., Chapman, L. J. and McLaughlin, R. L.
1989. Multiple central place foraging by spider monkeys:
travel consequences of using many sleeping sites. Oecolo-
gia. 79: 506–511.
Chapman, C. A., Fedigan, L. M. and Chapman, L. J.
1989. Post-weaning resource competition and sex ratios
in spider monkeys. Oikos. 54(3): 315–319.
Chapman, C. A. and Lefebvre, L. 1990. Manipulating fo-
raging group size. Spider monkey food calls at fruiting
trees, Anim. Behav. 39: 891–896.
Collins, A. C. 2008. e taxonomic status of spider
monkeys in the twenty-rst century. In: Spider Monkeys:
Behavior, Ecology and Evolution of the Genus Ateles, C. J.
Campbell (ed.), Rev. ed., pp. 50–80. Cambridge Univer-
sity Press, Cambridge.
Deer, T. R. 2010. Historia Natural de Los Primates Co-
lombianos. 2nd ed. Universidad Nacional de Colombia,
Bogotá.
Di Fiore, A., Link, A. and Dew, J. L. 2008 Diets of wild
spider monkeys. In: Spider Monkeys: Behavior, Ecology and
Evolution of the Genus Ateles, C. J. Campbell (ed.), Rev.
ed., pp. 81–137. Cambridge University Press, Cambridge.
Dunbar, R. I. M. 1988. Primate social systems. Croom
Helm, London and Sydney.
Estrada, A., Luecke, L., Van Belle, S., Barrueta, E., Meda,
M. R. 2004. Survey of black howler (Alouatta pigra) and
spider (Ateles geoffroyi) monkeys in the Mayan sites of
Calakmul and Yaxchilán, Mexico and Tikal, Guatemala.
Primates. 45(1): 33–39.
Fedigan, L. M., Fedigan, L., Chapman, C. A., Glander, K.
E. 1988. Spider Monkey home ranges: A comparison of
radio telemetry and direct observation. Am. J. Primatol.
16: 19–29.
Felton, A. M., Felton, A., Wood, J., Lindenmayer, D. B.
2008 Diet and feeding ecology of Ateles chamek in a bo-
livian Semihumid Forest: e importance of Ficus as a
staple food resource. Int. J. Primatol. 29: 379–403.
Fontaine, R. 1990. Positional behavior in Saimiri boliviensis
and Ateles geoffroyi. Am. J. Phys. Anthropol. 82: 485–508.
Garmin Ltd. 2019. Garmin BaseCamp. Available at: https://
www.garmin.com/nl-NL/shop/downloads/basecamp.
Gibson, K. N. 2010. Male mating tactics in spider
monkeys: Sneaking to compete. Am. J. Primatol. 72(9):
794–804.
Gómez-Posada, C. and Londoño, J. M. 2012. Alouatta se-
niculus: Density, home range and group structure in a
bamboo forest fragment in the Colombian Andes. Folia
Primatol. 83(1): 56–65.
González-Zamora, A., Arroyo-Rodríguez, V., Chaves, Ó.
M., Sánchez-López, S., Stoner, K. E., Riba-Hernández, P.
2008. Diet of Spider Monkeys (Ateles geoffroyi) in Mesoa-
merica: Current knowledge and future directions. Am. J.
Primatol. 70: 1–13.
González-Zamora, A., Arroyo-Rodríguez, V., Oyama, K.,
Sork, V., Chapman, C. A., Stoner, K. E. 2012. Sleeping
sites and latrines of Spider Monkeys in continuous and
fragmented rainforests: Implications for seed dispersal
and forest regeneration. PLoS ONE. 7(10): 1–11.
González-Zamora, A., Arroyo-Rodríguez, V., Escobar, F.,
Oyama, K., Aureli, F., Stoner, K. E. 2015. Sleeping-tree
delity of the spider monkey shapes community-level
seed-rain patterns in continuous and fragmented rain fo-
rests. J. Trop. Ecol. 31(4): 305–313.
Neotropical Primates 25(1), December 201928
Groves, C. P. 2001. Primate Taxonomy. Smithsonian Press,
Washington, London.
Hagell, S., Whipple, A. V. and Chambers, C. L. 2013.
Population genetic patterns among social groups of the
endangered Central American spider monkey (Ateles geo-
ffroyi) in a human-dominated landscape. Ecol. Evol. 3(5):
1388–1399.
Hooper, J. 2014. An assessment of enrichment strategies for
sanctuary-housed spider monkeys (Ateles geoffroyi). Mas-
ter’s dissertation, Oxford Brookes University, Oxford, UK.
Kirkby, C. A., Doan, T. M., Lloyd, H., Farfán, A. C., Arria-
ga, W. A., Marín, A. P. 2000. “Project Tambopata 1” Tou-
rism development and the status of neotropical lowland
wildlife in Tambopata, south-eastern Peru: recommenda-
tions for tourism and conservation. Unpublished report,
TReeS-RAMOS.
Lange, L. R. 2016. Conservation of Peruvian primates and
behaviour of Peruvian black spider monkeys (Ateles cha-
mek) in south-eastern Peru. Master’s dissertation, Oxford
Brookes University, Oxford, UK.
Lindshield, S. M. and Rodrigues, M. A. 2009. Tool use
in wild spider monkeys (Ateles geoffroyi). Primates. 50:
269–272.
Link, A., Galvis, N., Fleming, E., Di Fiore, A. 2011. Pa-
tterns of mineral lick visitation by Spider Monkeys and
Howler Monkeys in Amazonia: Are licks perceived as ris-
ky areas? Am. J. Primatol. 73: 386–396.
Link, A., Galvis, N., Marquez, M., Guerrero, J., Solano,
C., Stevenson, P. R. 2012. Diet of the Critically Endan-
gered Brown Spider Monkey (Ateles hybridus) in an in-
ter-andean lowland rainforest in Colombia. Am. J. Pri-
matol. 74(12): 1097–1105.
Link, A. and Di Fiore, A. 2006. Seed dispersal by spi-
der monkeys and its importance in the maintenance
of neotropical rain-forest diversity. J. Trop. Ecol. 22(3):
235–246.
Link, A. and Di Fiore, A. 2013. Eects of predation risk on
the grouping patterns of White-Bellied Spider Monkeys
(Ateles belzebuth belzebuth) in western Amazonia. Am. J.
Phys. Anthropol. 150: 579–590.
McFarland Symington, M. 1987. Sex ratio and maternal
rank in wild spider monkeys: when daughters disperse.
Behav. Ecol.Sociobiol. 20(6): 421–425.
McFarland Symington, M. 1988a. Demography, ranging
patterns, and activity budgets of Black Spider Monkeys
(Ateles paniscus chamek) in the Manu National Park, Peru.
Am. J. Primatol. 15: 45–67.
McFarland Symington, M. 1988b. Food competition and
foraging party size in the black spider monkey (Ateles pa-
niscus chamek). Behaviour. 105: 117–134.
Michalski, F. and Peres, C. A. 2005. Anthropogenic deter-
minants of primate and carnivore local extinctions in a
fragmented forest landscape of southern Amazonia. Biol.
Conserv. 124(3): 383–396.
Morales-Jiménez, A. L., Disotell, T. and Di Fiore, A. 2015.
Revisiting the phylogenetic relationships, biogeography,
and taxonomy of spider monkeys (genus Ateles) in light of
new molecular data. Mol. Phylogenet. Evol. 82: 467–483.
Nunes, A. 1995. Foraging and ranging patterns in Whi-
te-Bellied Spider Monkeys. Folia Primatol. 65: 85–99.
Nunes, A. 1998. Diet and feeding ecology of Ateles bel-
zebuth belzebuth at Maracá ecological station, Roraima,
Brazil. Folia Primatol. 69: 61-76.
Pebsworth, P. A., Human, M. A., Lambert, J. E., Young, S.
L. 2018. Geophagy among nonhuman primates: A syste-
matic review of current knowledge and suggestions for fu-
ture directions. Am. J. Phys. Anthopol. 168 (S67): 164-194.
Ramos-Fernández, G., Mateos, J. L., Miramontes, O., Co-
cho, G., Larralde, H., Ayala-Orozco, B. 2004. Lévy walk
patterns in the foraging movements of spider monkeys
(Ateles geoffroyi). Behav. Ecol. Sociobiol. 55(3): 223–230.
Ramos-Fernández, G. 2005. Vocal communication in a
ssion-fusion society: Do Spider Monkeys stay in touch
with close associates? Int. J. Primatol. 26(5): 1077–1092.
Rosenberger, A. L., Halenar, L., Cooke, S. B., Hartwig,
W. C. 2008. Morphology and evolution of the spider
monkey, genus Ateles. In: Spider Monkeys: Behavior, Eco-
logy and Evolution of the Genus Ateles, C. J. Campbell
(ed.), Rev. ed., pp. 81–137. Cambridge University Press,
Cambridge, New York.
Rylands, A. B. and Mittermeier, R. A. 2013. Family Ateli-
dae. In: Handbook of the Mammals of the World - Volume
3 Primates. R. A. Mittermeier, A. B. Rylands and D. E.
Wilson (eds), pp. 484–549. Lynx Edicions, Barcelona.
Salvador, S., Clavero, M. and Leite Pitman, R. 2011. Lar-
ge mammal species richness and habitat use in an upper
Amazonian forest used for ecotourism. Mamm. Biol.
76(2): 115–123.
Scheel, M. H. and Edwards, D. 2012. Captive spider
monkeys (Ateles geoffroyi) arm-raise to solicit allo-groo-
ming. Behav. Processes. 89: 311–313.
Shimooka, Y. 2005. Sexual dierences in ranging of Ate-
les belzebuth belzebuth at La Macarena, Colombia. Int. J.
Primatol. 26(2): 385–406.
Shimooka, Y., Campbell, C. J., Di Fiore, A., Felton, A.
M., Izawa, K., Link, A. Nishimura, A., … Wallace, R.
B. 2008. Demography and group composition of Ateles.
In: Spider Monkeys: Behavior, Ecology and Evolution of the
Genus Ateles, C. J. Campbell (ed.), Rev. ed., pp. 329-348.
Cambridge University Press, Cambridge, New York.
Slater, K. Y., Schaner, C. M. and Aureli, F. 2007. Embra-
ces for infant handling in spider monkeys: evidence for a
biological market? Anim. Behav., 74: 455–461.
Slater, K. Y., Schaner, C. M. and Aureli, F. 2009. Sex di-
erences in the social behavior of wild Spider Monkeys
(Ateles geoffroyi yucatanensis). Am. J. Primatol. 71: 21–29.
Spehar, S., Di Fiore, A. and Link, A. 2010. Male and fema-
le range use in a group of white-bellied spider monkeys
(Ateles belzebuth) in Yasuní National Park, Ecuador. Am.
J. Primatol. 72: 129–141.
Spehar, S. N. and Di Fiore, A. 2013. Loud calls as a me-
chanism of social coordination in a ssion-fusion taxon,
the white-bellied spider monkey (Ateles belzebuth). Behav.
Ecol. Sociobiol. 67(6): 947–961.
Takahashi, J. 2008. A literature review of the spider monkey,
Ateles sp., with special focus on risk for extinction. Degree
Neotropical Primates 25(1), December 2019 29
project, Swedish University of Agricultural Sciences,
Uppsula, Sweden.
Van Roosmalen, M. G. M. 1985. Habitat preferences, diet,
feeding strategy and social organization of the black spi-
der monkey (Ateles paniscus paniscus Linnaeus 1758) in
Surinam. Acta Amazonica. 15: 0–234.
Veiga, L. M. and Ferrari, S. F. 2007. Geophagy at termita-
ria by Bearded Sakis (Chiropotes satanas) in southeastern
Brazilian Amazonia. Am. J. Primatol. 69: 816–820.
Velázquez-Vázquez, G., Reyna-Hurtado, R., Arroyo-Rodrí-
guez, V., Calmé, S., Léger-Dalcourt, M., Navarrete, D.
A. 2015. Sleeping sites of Spider Monkeys (Ateles geoffro-
yi) in logged and unlogged tropical forests. Int. J. Prima-
tol. 36(6): 1154–1171.
Wallace, R. B. 2001. Diurnal activity budgets of Black Spi-
der Monkeys, Ateles chamek, in a southern Amazonian
tropical forest. Neotrop. Primates. 9(3): 103–107.
Wallace, R. B. 2005. Seasonal variations in diet and fora-
ging behavior of Ateles chamek in a southern Amazonian
tropical forest. Int. J. Primatol. 26(5): 1053–1075.
Wallace, R. B. 2006. Seasonal variations in Black-Faced
Black Spider Monkey (Ateles chamek) habitat use and ran-
ging behavior in a southern Amazonian tropical forest.
Amer. J. Primatol. 68: 313–332.
Wallace, R. B. 2008. Factors inuencing spider monkey
habitat use and ranging patterns. In: Spider Monkeys:
Behavior, Ecology and Evolution of the Genus Ateles, C. J.
Campbell (ed.), Rev. ed., pp. 138–155. Cambridge Uni-
versity Press, Cambridge, New York.
Weather Underground. 2019. Monthly climate history of the
Puerto Maldonado International Airport, Peru. Website:
www.wunderground.com. Accessed 22 April 2019.
White, F. 1986. Census and preliminary observations on
the ecology of the black-faced black spider monkey (Ate-
les paniscus chamek) in Manu National Park, Peru. Am. J.
Primatol. 11: 125–132.
World Weather Online. 2019. Puerto Maldonado Monthly
Climate Averages, Madre de Dios, Peru. Website: www.
worldweatheronline.com. Accessed 22 April 2019.
Youlatos, D. 2002. Positional behavior of Black Spider
Monkeys (Ateles paniscus) in French Guiana. Int. J. Pri-
matol. 23(5): 1071–1093.
Youlatos, D. 2008. Locomotion and positional behavior
of spider monkeys. In: Spider Monkeys: Behavior, Ecology
and Evolution of the Genus Ateles, C. J. Campbell (ed.),
Rev. ed., pp. 185–219. Cambridge University Press,
Cambridge, New York.
Neotropical Primates 25(1), December 201930
DENSIDAD POBLACIONAL Y COMPOSICIÓN DE GRUPOS DE AOTUS NANCYMAAE EN
ÁREAS DE APROVECHAMIENTO DE LA ESPECIE PARA EXPERIMENTACIÓN BIOMÉDICA EN
EL TRAPECIO AMAZÓNICO COLOMBIANO
Néstor Roncancio-Duque1, Mariela Osorno1, Liza M. Calderón-Espitia1, Amilvia Acosta-
Castañeda1, Lina M. García-Loaiza1, Natalia Gómez-Melendro1 and Beatriz E. Henao1
1Instituto Amazónico de Investigaciones Científicas – Sinchi, E-mail: <nroncanciod@gmail.com>
Resumen
El uso de fauna, así como de otros recursos naturales, es fundamental para el desarrollo y bienestar humano. No obstante,
garantizar su conservación depende de un manejo basado en información conable, es decir, rigurosamente colectada y ana-
lizada, y adecuados esquemas de regulación; de lo contrario se pueden sobreexplotar dichos recursos. La sobreexplotación es
uno de los cinco motores de perdida de diversidad y ha sido identicada como una amenaza directa para algunos primates.
Las poblaciones de las especies del género Aotus en el sur de la Amazonía colombiana han sido usadas para experimenta-
ción biomédica desde hace aproximadamente 30 años, no obstante, el impacto de este proceso no ha sido sucientemente
evaluado. Ante la reciente conrmación de un nuevo taxón para Colombia, Aotus nancymaae, el adecuado diagnóstico del
estado de conservación de sus poblaciones, la revisión de los planes de manejo y monitoreo, incluidos los procedimientos
de aprovechamiento, cobran mayor importancia, dada su restringida área de distribución y aprovechamiento inespecíco,
que determinan como Vulnerable a la especie en Colombia. Se presentan resultados preliminares de algunos parámetros
poblacionales, como paso inicial para determinar la salud de estas poblaciones. Los resultados y la comparación con otros
estudios permiten concluir que existe una alta carga de incertidumbre sobre información básica para poder hacer un manejo
sostenible de las especies en este paisaje.
Palabras clave: Especies amenazadas, experimentación biomédica, manejo de vida silvestre.
Abstract
e use of wildlife as a natural resource is fundamental to human welfare and development. However, to guarantee wildlife
conservation, wildlife management needs to be based on reliable information, in other words, data that are rigorously col-
lected and analyzed, and an accurate regulatory system; otherwise wildlife overexploitation can occur. Overexploitation
is one of the ve drivers of biodiversity loss and has been identied as a direct threat to some primate species. Captured
animals from the wild populations of Aotus species in the southern Colombian Amazon have been used for biomedical
experimentation since approximately 30 years ago; however, the impact of this process needs to be evaluated further. Since
the recent conrmation of a new taxon to Colombia, Aotus nancymaae, it has become even more important to accurately as-
sess the conservation status of owl monkey populations in this region, as well as to review the management and monitoring
plan, including protocols for use. Due to its restricted distribution and its human use, this species is considered Vulnerable
in Colombia. Here we show preliminary results of some population parameters as an initial step to determine the health of
this population. e results and the comparison with other studies allow us to conclude that there is a very high uncertainty
about basic information needed to plan sustainable management of these species in this landscape.
Keywords: reatened species, biomedical experimentation, wildlife management.
Introducción
Los seres humanos siempre han cazado y explotado recur-
sos naturales para sobrevivir. La explotación, a diferencia
de la cosecha, implica la extracción de individuos o partes
de individuos de poblaciones silvestres y no de plantacio-
nes o producciones animales (Sutherland, 2000). Se esti-
ma que la sobreexplotación amenaza cerca de un tercio de
las especies de vertebrados raros, vulnerables o amenazados
(Groombridge, 1992). En gran parte del mundo los recur-
sos son explotados lo más rápido posible. Si existe un mer-
cado para un producto, los habitantes locales lo buscarán y
lo venderán usando cualquier método disponible para ob-
tener el recurso. La sobreexplotación de una especie se da
rápidamente cuando se empieza su aprovechamiento en un
lugar donde anteriormente no era usada y tanto el comer-
cio legal como ilegal son responsables de la reducción de
algunas especies. La sobreexplotación de un recurso ocurre,
entre otras razones, por falta de conocimiento del sistema
de aprovechamiento (Primack, 2010).
Actualmente los primates son el orden más amenazado de
mamíferos en Colombia, con 26 de sus 46 taxones inclui-
dos en las categorías de amenaza de la Unión Internacional
Neotropical Primates 25(1), December 2019 31
para la Conservación de la Naturaleza (UICN, 2017).
Para algunos primates, como por ejemplo, Saguinus oedi-
pus y S. leucopus, además de la destrucción del hábitat, la
extracción de individuos para experimentación biomédica
o para comercio como mascota se ha denido como una
amenaza para su conservación (Deer, 2010). Las especies
del género Aotus en el sur de la Amazonia colombiana, de
quienes hasta ahora no hay conclusiones denitivas acerca
de su distribución (Bloor et al., 2014) y abundancias, han
sido usadas durante los últimos 30 años como modelos bio-
lógicos para experimentación biomédica. Desde octubre
de 2005 hasta junio de 2012 se extrajeron de las pobla-
ciones silvestres a orillas del río Amazonas en Colombia,
poco más de 4,500 individuos (Registros Corpoamazonia).
Estas extracciones no necesariamente pueden considerarse
mortalidades, dado que como parte del proceso de la expe-
rimentación biomédica se contempla la reincorporación de
los individuos aprovechados al medio natural. Así, entre
octubre de 2006 y septiembre de 2012 fueron liberados
4,041 individuos en la región (Registros Corpoamazonia).
Sin embargo, el impacto de los diferentes procedimientos
del proceso de aprovechamiento sobre las especies del gé-
nero en esta zona (Fidic, 2007; Hernández y Díaz, 2010;
Maldonado, 2011), no puede determinarse adecuadamen-
te, ya que el estado de conservación de sus poblaciones no
ha sido determinado con suciencia.
Un paso inicial para conocer el estado de una población
es hacer una estimación empírica de su abundancia, no
obstante una estimación de la densidad poblacional de
una especie es preferible dado que este parámetro reeja
la relación que hay entre la población y el área que ocupa
(Begon et al., 2009). La densidad poblacional es un pa-
rámetro dinámico espacial y temporalmente, por tanto, la
estimación inicial de la densidad es útil mientras se asuma
como base de un programa de seguimiento, que permita
determinar sus tendencias. De esta forma se pueden es-
timar tasas de crecimiento poblacional y evaluar el com-
portamiento de este parámetro en poblaciones sometidas
a diferentes niveles de aprovechamiento (Anzures-Dadda y
Manson, 2007; Arroyo-Rodríguez et al., 2008). Siguiendo
estas consideraciones, se estimó la densidad poblacional de
Aotus nancymaae en un área en la cual se extrajeron 184
individuos entre febrero de 2011 y abril de 2012 (Registros
Corpoamazonia). Adicionalmente se presentan estimacio-
nes de composición de grupo de esta especie a una escala es-
pacial más amplia, como primer paso en la evaluación de la
población de esta recién conrmada especie para Colombia
(Bloor et al., 2014) y que se encuentra categorizada como
vulnerable (VU) (Maldonado et al., 2017).
Materiales y métodos
Área de estudio
El área de estudio está ubicada en el Resguardo Ticoya, juris-
dicción del municipio de Puerto Nariño, departamento de
Amazonas, Colombia. Para la determinación de la compo-
sición de grupos los muestreos se hicieron especícamente
en sitios cercanos a las comunidades: San Pedro de Tipisca
(-70°35’36’’W, -3°41’12’’S), Doce de Octubre (-70°30’15’’,
-3°44’10’’), Naranjales (-70°31’47’’, -3°52’18’’), San Juan
de Atacuari (-70°39’34’’W, -3°49’26’’) y Santa Clara de Ta-
rapoto (-70°24’51’’, -3°48’02’’). El muestreo para estimar
la densidad poblacional de la especie se llevó a cabo en los
alrededores de la comunidad Naranjales, en aproximada-
mente 19 km2 de área inferencial, es decir, de donde se pue-
de asumir que el muestreo es representativo, conformados
por un mosaico de humedales permanentes y zonas altas
inundables conocidas localmente como “restingas” (Fig. 1).
Figura 1. Área de estudio. El circulo en la comunidad de Naranjales corresponde a la zona en donde se
establecieron los transectos para la estimación de la densidad poblacional. Los puntos negros son los sitios
de capturas de individuos o grupos de Aotus nancymaae.
Neotropical Primates 25(1), December 201932
Para la ejecución del proyecto, se elevó la consulta previa
reglamentaria ante el Ministerio del Interior y se obtuvo
respuesta aclarando que no se requería la consulta debido
a que el proyecto de investigación no generaba ninguna
afectación a los grupos étnicos. No obstante, se socializó
el proyecto en las 22 comunidades del resguardo Ticoya.
Entre julio y noviembre de 2012 se desarrolló el trabajo
de campo.
Toma de datos
Densidad poblacional
Para estimar la densidad de A. nancymaae alrededor de la
comunidad de Naranjales, se empleó el método de mues-
treo por distancias con transectos lineales, mediante el cual
se registra el número de animales vistos por un observador
que camina a lo largo de un transecto, y la distancia perpen-
dicular hasta el punto donde se observaron los animales o
hasta el centro geográco del grupo observado (Buckland
et al., 2007; Buckland et al., 2015; omas et al., 2010).
Los transectos se ubicaron de acuerdo a la conguración
del área, dado que existen humedales permanentes que
impiden el acceso. Se establecieron 18 transectos con una
longitud total de 29.6 km y un promedio de 1,644.4 m
(DS ± 407.6 m); algunos correspondieron a caminos ya
existentes, mientras se pudieran satisfacer los supuestos de
que a 0 metros de distancia perpendicular la probabilidad
de detección sería del 100 % y de la independencia de las
observaciones, es decir, que no hubiera probabilidad de
contar los mismos animales más de una vez en un mismo
recorrido (rectitud del transecto) y, de que no se contara
el mismo grupo en dos transectos distintos en recorridos
simultáneos por las acciones evasivas del grupo ante una
primera detección. Cada transecto fue recorrido en pro-
medio 2.89 veces, con una distancia promedio de 4.9 km
por transecto, acumulando un esfuerzo de muestreo de
88.6 km. Los transectos fueron recorridos silenciosamen-
te escrutando la vegetación, a una velocidad promedio de
1.03 km/h. Se realizaron conteos simultáneos con un ob-
servador por transecto. Los transectos fueron recorridos
desde las 3:30 hasta las 5:30 horas, y desde las 17:35 hasta
las 19:35 horas. En los muestreos sólo se incluyeron los re-
gistros visuales. El recorrido de los transectos y la hora en
que éste se efectuó, se distribuyó proporcionalmente entre
los observadores, para eliminar posibles sesgos asociados a
un mismo observador recorriendo repetidamente un mis-
mo transecto y/o haciéndolo a la misma hora (Roncancio
et al., 2009). Con el objetivo de mantener constante la
probabilidad de detección a lo largo de un transecto, se
procuró tener la misma velocidad durante el recorrido;
por tal motivo, una vez ubicado un grupo, el observador
permaneció máximo hasta 15 minutos con el grupo para
intentar su conteo completo (Peres, 1999). Cada vez que
fue localizado un grupo, se registró la hora, el número de
individuos, se midió la distancia perpendicular al transec-
to, se registró la coordenada y la actividad que los animales
desarrollaban.
Estructura y composición de grupos
Los datos para estos análisis se colectaron en el marco de
la investigación para determinar la identidad de las espe-
cies del género Aotus que habitan en el trapecio amazónico
colombiano (cinco localidades evaluadas en el resguardo
Ticoya) y algunos de sus parámetros demográcos, lo cual
implicaba la captura de individuos libres. Estas capturas
fueron hechas por un equipo conformado por un biólogo,
un veterinario y expertos locales. Todo el proceso de cap-
tura, toma de muestras y marcaje de los animales se ejecutó
bajo tres principios: 1. garantizar la integridad física de las
personas que participaban en el proceso, 2. garantizar la
integridad física de los animales y 3. garantizar la calidad
de las muestras y los datos. El procedimiento se desarro-
lló de la siguiente forma: inicialmente los expertos locales
hacían jornadas de búsqueda y seguimiento a partir de la
3:00 y hasta la 6:30 horas, en las cuales intentaban ubi-
car un grupo de Aotus y seguirlo hasta su nido. Una vez
el grupo entraba al nido, los colectores permanecían hasta
aproximadamente las 6:30 horas vericando que el grupo
no se desplazará a otro lugar. Posteriormente, los colecto-
res regresaban al sitio de reunión con el resto del equipo e
informaban las características del nido y la viabilidad de la
captura conforme a los tres principios de seguridad y ca-
lidad. Las capturas se realizaron a partir de las 9:30 y las
10:00 y hasta las 15:00 horas, periodo en el que los indivi-
duos de la especie de este género se encuentran menos aler-
ta. En esta zona los nidos de Aotus son básicamente de dos
clases. Los primeros están ubicados en vegetación densa en
la parte alta de un árbol “Chamiceras”, mientras los otros
están ubicados en huecos de árboles. El primer tipo de
nido solo se puede alcanzar por medio de tala de entre 300
y 500 m2 alrededor del árbol y poda del árbol en el que se
encuentra el nido, por tanto, los grupos que se encontraron
en este tipo de nido no se intentaron capturar. Por otro
lado, los primates que se encontraron en huecos de árboles
se capturaron de dos formas dependiendo de la altura y la
cantidad de huecos de salida que tenía el nido. La primera
fue por medio de un acceso sigiloso, respetando la distan-
cia mínima de fuga a los huecos o hueco del nido, con el
objetivo de taparlos con tela plástica usando varas de palma
“marona”, si la distancia de acceso lo demandaba. La se-
gunda técnica implicó la intimidación de los animales para
que no se fugaran del nido, utilizando varas de alrededor de
40 cm de longitud, lanzadas desde el suelo mientras uno o
dos integrantes del equipo asciende a tapar el nido con tela
plástica o mallas. Luego de que el nido estaba asegurado, se
vericaba la profundidad del mismo y se procedía a la ex-
tracción de los animales obligando su desplazamiento hasta
el fondo del nido, la boca del agujero del mismo o, hasta
una abertura hecha para su extracción. Para esta actividad
se contó con equipo certicado de ascenso a dosel el cual
incluía cuerda, arneses, cascos, cordinos, cintas tubulares,
mosquetones, ascendedores, descendedores (Ocho y ATC)
y guantes. Cada integrante del equipo recibió previamente
entre seis y 12 horas de instrucción en el manejo de los
equipos y en técnicas de ascenso a dosel.
Neotropical Primates 25(1), December 2019 33
Una vez capturados los individuos, estos fueron ubicados
individualmente en bolsas de tela negra; en el suelo, cada
animal fue tranquilizado con Ketamina vía intramuscular
en la parte posterior del muslo, con dosis de entre 5 y 15
mg/kg de peso (los individuos eran pesados previa inocu-
lación del medicamento). Este proceso fue monitoreado a
través de la lectura continua de la temperatura, frecuencia
cardiaca y frecuencia respiratoria. A los animales captu-
rados se les tomaron los siguientes datos: peso, longitud
total, longitud oreja, longitud de pie, longitud de cola,
longitud corporal, circunferencia, sexo, estado reproducti-
vo (gestante, lactante, presencia de testículos escrotales), se
hicieron registros fotográcos de diferentes planos, de los
dientes y de un tatuaje que se le hacía en la cara ventral de
muslo (para identicar recapturas). Para la estructura de la
población se denieron preliminarmente cuatro categorías
de desarrollo, adultos, subadultos, juveniles e infantes con
base en los criterios utilizados por Castaño et al. (2010).
Análisis de datos
Densidad poblacional
La densidad poblacional de A. nancymaae en Naranjales se
estimó con el programa DISTANCE 7.1 (omas et al.,
2010). El objetivo del análisis del muestreo a distancia es
ajustar una función de detección de las distancias perpendi-
culares de las observaciones y usar esta función para estimar
la proporción de objetos que no se detectaron en el mues-
treo (Buckland et al., 2001; Buckland et al., 2015). Para la
estimación de la densidad de individuos se usó el tamaño
de grupo estimado E(s), a partir de la regresión entre la pro-
babilidad de detección y el tamaño de grupo, de tal forma
que se evite el sesgo generado por la reducción en la detec-
tabilidad de los grupos más pequeños registrados durante
los muestreos en los transectos. Se comparó la distribución
de frecuencias de las distancias perpendiculares con seis
modelos: 1. Half normal con serie de expansión Coseno,
2. Half normal con Hermite polynomial, 3. Uniforme con
Coseno, 4. Uniforme con Simple polynomial, 5. Hazard-rate
con Coseno y 6. Hazard-rate con Simple polynomial. De los
anteriores modelos se eligió el que presentó el menor valor
de AIC (Criterio de Información de Akaike). El AIC es
un método cuantitativo para la selección del modelo que
mejor se ajusta a los datos y que emplea el menor número
de parámetros (Burnham y Anderson, 2002).
Tamaño y composición de grupos
Para determinar el tamaño medio de grupo en esta zona
del trapecio amazónico (cinco localidades del resguardo Ti-
coya) se tuvo en cuenta la información de todos los grupos
(capturados y no capturados) para los cuales se logró su con-
teo completo. Para determinar la composición de los grupos
se tuvieron en cuenta aquellos grupos que fueron capturados
en su totalidad; para la composición se evaluó la proporción
de cada categoría de edad y de los géneros. Se evaluó además
la relación entre machos adultos y hembras adultas y entre
hembras adultas e inmaduros (juveniles más infantes).
Resultados
Densidad poblacional
Se obtuvieron 24 registros visuales de A. nancymaae. La
distribución de frecuencias de las distancias perpendicu-
lares presentó un mejor ajuste al modelo Uniforme con
serie de expansión coseno. La densidad poblacional de
A. nancymaae en la localidad de Naranjales fue de 23.9
individuos/km2 (IC95 % = 13,6 – 42,3) y 8.8 grupos/
km2 (IC95 % = 5,1 – 15,2), con coecientes de variación
del 28,8 % y 27,2 % respectivamente. La varianza de la
densidad fue inuenciada por la probabilidad de detección
(59,6 %), la tasa de encuentro (29,1 %) y el tamaño de gru-
po (11,3 %).
Tamaño y composición de grupos
Se capturaron 150 individuos de A. nancymaae en las cinco
localidades. Cincuenta y ocho por ciento de los individuos
capturados fueron adultos (37 % hembras y 21 % machos),
5 % subadultos y 29 % inmaduros (Tabla 3).
Tabla 3. Estado de desarrollo y género por localidad de los individuos capturados del género Aotus.
Estado de desarrollo Adulto Infante Juvenil Subadulto Total
Localidad/Género H M H M H M H M
Doce de Octubre 8 7 4 3 1 23
Naranjales 11 2 2 6 4 1 26
San Juan de Atacuari 23 13 1 6 3 2 2 50
Santa Clara de Tarapoto 13 10 10 10 4 4 51
Sub-total 55 32 1 1 22 22 10 9 150
Total 87 2 44 8
De las 55 hembras adultas capturadas 62 % estaban repro-
ductivamente activas (19 gestantes y 15 lactantes). Se cap-
turó un infante, aparentemente nacido durante la primera
quincena de noviembre. El tamaño promedio de grupo fue
de 3.06 individuos (IC 95 % = 2.89 – 3.22, n = 138) con un
rango de dos a cinco individuos; 36 con dos individuos, 51
Neotropical Primates 25(1), December 201934
con tres, 34 con cuatro y 11 con cinco. Se registraron seis
individuos solitarios. Se capturaron 17 grupos completos:
la relación hembras: machos fue 1: 0.94 y, de hembras: in-
maduros 1: 0.52.
Discusión
Para la localidad de Naranjales se estimó una densidad
poblacional de alrededor de 24 ind/km2 y para las cinco
localidades evaluadas un tamaño promedio de grupo de
tres individuos. Comparando los intervalos de conanza
(Cumming et al., 2007), la densidad encontrada no pre-
senta diferencia signicativa con otras estimaciones hechas
para la especie o al menos para especies gemelas en la cuen-
ca del Amazonas en Perú (Aquino y Encarnación, 1986;
Aquino y Encarnación, 1988), y en áreas cercanas a esta lo-
calidad en Colombia (Fidic, 2007; corregido de Hernández
y Díaz 2010; Maldonado, 2011) (Fig. 2). No obstante, un
resultado publicado por Maldonado (2011) el cual indica
una densidad de cerca de 7 ind/km2 en Perú, podría ser sig-
nicativamente menor, pero este no fue tenido en cuenta,
dado que presenta un coeciente de variación de entre 3.3
y 4.1 ind/km2, el cual deja por fuera el estimador puntual,
reejando un error en el análisis o en la presentación de los
resultados.
La ausencia de diferencias signicativas entre estos resul-
tados puede deberse a que los coecientes de variación de
la densidad poblacional para todas las localidades fueron
altos (>10 % para los que presentan medidas de dispersión).
Esta imprecisión en la estimación de la densidad está in-
uenciada usualmente, en mayor proporción, por la varia-
ción en la tasa de encuentro, producto del bajo número de
transectos dispuestos para los muestreos (Hernández y Díaz
2010). El método de muestreo por distancia con transectos
lineales, apegado al principio de replicación de inferencia
estadística, está propuesto para ser implementado con un
tamaño de muestra de entre 25 y 30 transectos (Buckland
et al., 2001; Buckland et al., 2007; Buckland et al., 2010a;
omas et al., 2010). No obstante, los estudios citados
usan entre seis y ocho transectos y el presente 18. Es ne-
cesario diseñar muestreos con un mayor tamaño muestreal
para aumentar la precisión de los estimados y de esta forma
poder detectar diferencias espaciales y temporales si las hay
(evitar cometer error tipo II al no detectar diferencias cuan-
do las hay), y de esta forma poder tomar las decisiones de
manejo correspondientes (Elzinga, 2001; Janson, 2011). A
pesar de la imprecisión señalada, en general los resultados
previos a este estudio indican que la densidad de esta espe-
cie está usualmente entre los 20 y 40 ind/km2, valor que
puede ser considerado como línea de base y umbral para
denir objetivos de manejo, es decir, para determinar si es
necesario aumentar o se puede mantener la densidad pobla-
cional de la especie en las localidades evaluadas.
Con relación al tamaño de grupo, tres de seis estimacio-
nes hechas recientemente (Maldonado, 2011; Hernández y
Díaz, 2010) fueron signicativamente menores (2.0 ± 0.22
en Chineria & Yahuma-Perú; 1.88 ± 0.16 en Vista Alegre-Pe-
rú y 2.05 ± 0.13 en Calderón, Maldonado, 2011). Las esti-
maciones de Mocagua (3.3 ± 1.4, Maldonado, 2011), Reser-
vas Privadas-Colombia (3.5 ± 0.11 Maldonado, 2011) y San
Juan de Atacuari-Siete de Agosto (2.74 ± 0.96 Hernández y
Díaz, 2010) no resultaron signicativamente diferentes. La
estimación del tamaño de grupo en este estudio se hizo con
base en grupos para los cuales se asumió conteo completo.
Las estimaciones de los otros estudios se hicieron durante
los muestreos para estimar la densidad.
Figura 2. Comparación de densidades poblacionales de Aotus sp. en la cuenca del
Río Amazonas.; Calderón, Mocagua, San Martín.
Neotropical Primates 25(1), December 2019 35
Cuando se estiman densidades poblacionales con el méto-
do de muestreo por distancias con transectos lineales, hacer
el conteo completo de los grupos es usualmente difícil y
esto se ve reejado en relaciones encontradas entre el ta-
maño de grupo y la probabilidad de detección o entre la
distancia perpendicular y el tamaño de grupo (cuando el
grupo es más grande, mayor probabilidad de detección o, a
mayor distancia perpendicular la estimación del tamaño de
grupo tiende a ser menor, porque es más difícil contarlo);
en este sentido, si se usa el tamaño medio de grupo, las
densidades tienden a subestimarse; por tanto, la densidad
debe ser calculada con el tamaño estimado de grupo dada la
regresión (Buckland et al., 2007). Los estimados de tama-
ño de grupo presentados por Maldonado (2011) no especi-
can si son los estimados con base en la regresión o son el
tamaño medio. Si son el tamaño medio de grupo contado
durante los muestreos de densidad, probablemente estén
subestimados, más aún, tratándose de una especie con há-
bitos nocturnos (Buckland et al., 2010a; Buckland et al.,
2010b). Por otro lado, las diferencias encontradas, pueden
estar reejando cambios ecológicos reales y en este sentido
habría que plantear hipótesis para dilucidar qué factores es-
tán determinando estas diferencias (Janson, 2011).
La relación machos adultos-hembras adultas es típica para
las especies de esta familia, en donde los grupos están con-
formados por la pareja reproductiva y sus crías (Wright,
1978; Aquino y Encarnación, 1986; Aquino y Encarna-
ción, 1988; Fernandez-Duque et al., 2001; Castaño et
al., 2010; Hernández y Díaz, 2010). La población de
A. nancymaae evaluada presentó una baja proporción de
individuos inmaduros, con una relación hembras adul-
tas: inmaduros (1: 0,5). Esta situación, de ser generali-
zada, podría llevar a un incorrecto remplazamiento de
los individuos adultos (Deer, 1981). La relación entre
el número de hembras adultas: inmaduros (juveniles más
infantes), puede ser un indicativo del “estado de salud” de
una población; donde relaciones menores a 1: 0,75 sugie-
ren poblaciones en dicultades o en disminución (Heltne
et al., 1976; Estrada et al., 2002). No obstante, sólo con
estudios a largo plazo, se puede determinar si una pobla-
ción está aumentando o disminuyendo, o si simplemente
existen uctuaciones intra e interanuales en el número de
individuos, debido a la variación intrínseca en la natali-
dad o supervivencia de los juveniles (Struhsaker., 1981).
En este sentido, no se puede concluir acerca del impacto
que generan los diferentes procedimientos (captura, ex-
tracción y liberación) del proceso de experimentación,
a la población. Esta incertidumbre se asocia en primer
lugar, con la falta de robustez de los diseños de muestreo
y consecuentemente una baja potencia estadística que no
permite comparar las densidades entre zonas con y sin
intervención y, segundo, con la falta de trazabilidad de los
animales capturados; integrantes de la comunidad local
manifestaron que algunos de los individuos ingresados
a la FIDIC como provenientes de Naranjales fueron ex-
traídos realmente de la zona de Caballococha en el Perú.
Adicionalmente las liberaciones pueden estar cumpliendo
el papel de refuerzos o suplementos como estrategia de
conservación basada en el desplazamiento de organismos
vivos (UICN 2013). De los 150 individuos capturados,
19 eran individuos que estuvieron en la FIDIC y fueron
liberados (basados en el hallazgo de los tatuajes de la FI-
DIC). Los animales encontrados tenían un tiempo de
sobrevivencia de entre siete meses y tres años-nueve meses
(según registros de Corpoamazonia). Todos los indivi-
duos capturados que estaban marcados pertenecían a gru-
pos conformados por dos o tres individuos.
Con base en estos resultados consideramos que, todo el
procedimiento de manejo de la especie y en general de las
especies del género Aotus aprovechadas con nes biomédi-
cos, debe ser revisado y ajustado muy conservadoramente
considerando 1) la falta de conocimiento básico, especial-
mente de parámetros poblacionales, 2) que para A. nancy-
maae no había permiso de aprovechamiento dado que su
presencia en Colombia no había sido conrmada, 3) que
su área de distribución podría ser muy reducida (aproxima-
damente 652 km2) (Maldonado et al., 2017) y, 4) que los
protocolos de los diferentes procedimientos no garantizan
trazabilidad de los sitios de extracción de los individuos
para su posterior liberación (Roncancio, 2012) y por lo
tanto no se puede evaluar el impacto de todo el proceso de
aprovechamiento, ni planicar su manejo adaptativamente
(CMP, 2007).
Agradecimientos
Esta investigación fue hecha con el apoyo técnico y nan-
ciero del Instituto Sinchi, el Instituto de Genética de la
Universidad Nacional de Colombia, la Corporación Autó-
noma Regional de la Amazonia y el Ministerio de Ambien-
te y Desarrollo Sostenible. El trabajo de campo se logró
gracias a la participación de las comunidades del resguardo
Ticoya (Ticuna, Cocama y Yagua) y sus expertos locales.
Referencias
Anzures-Dadda, A. y Manson, R. H. 2007. Patch-and
Landscape-scale Eects on Howler Monkey distribution
and abundance in rainforest fragments. Anim. Conserv.
10(1): 69–76.
Aquino, R. y Encarnación, F. 1986. Population structure
of Aotus nancymai (Cebidae: Primates) in Peruvian Ama-
zon lowland forest. Am. J. Primatol. 11(1): 1–7.
Aquino, R. y Encarnación, F. 1988. Population densities
and geographic distribution of Night Monkeys (Aotus
nancymai and Aotus vociferans) (Cebidae: Primates) in
northeastern Peru. Am. J. Primatol. 14(4): 375–381.
Arroyo-Rodríguez, V., Asensio, N. y Cristóbal-Azkarate,
J. 2008. Demography, life History and migrations in a
Mexican Mantled Howler group in a rainforest fragment.
Am. J. Primatol. 70(2): 114–118.
Begon, M., Townsend, C. R. y Harper, J. L. 2009. Ecolo-
gy: From Individuals to Ecosystems. John Wiley & Sons,
Oxfort, UK.
Neotropical Primates 25(1), December 201936
Bloor, P., Ibañez, C., Arciniegas, S., Hoyas, M. y Hernán-
dez, S. 2014. Estudio genético del género Aotus al sur
de la Amazonia de Colombia. Asociación Colombiana
de Zoología. 2015. La biodiversidad sensible: patrimo-
nio natural irreemplazable. IV Congreso Colombiano de
Zoología. Libro de resúmenes. Asociación Colombiana
de Zoología. Disponible en línea: www.congresocolom-
bianodezoologia.org / www.aczcolombia.org.
Buckland, S., Anderson, D., Burnham, K., Laake, J., Bor-
chers, D. y omas, L. 2001. Introduction to the Distance
sampling: Estimating Abundance of Biological Populations.
Oxford University Press, Oxford, UK.
Buckland, S. T., Anderson, D. R., Burnham, K. P. y o-
mas. L. 2007. Advanced Distance Sampling: Estimating
Abundance of Biological Populations. Oxford University
Press, Oxford, UK.
Buckland, S.T., Rexstad, E.A., Marques, T.A. y Oedeko-
ven, C.S. 2015. Distance Sampling: Methods and Applica-
tions. Springer, Switzerland.
Buckland, S. T., Plumptre, A. J. omas, L. y Rexstad, E.
A. 2010. Line transect sampling of Primates: can ani-
mal-to-observer distance methods work?. Int. J. Primatol.
31(3): 485–499.
Buckland, S. T., Plumptre, A. J., omas, L., Rexstad, E.A.
2010. Design and analysis of line transect surveys for Pri-
mates. Int. J. Primatol. 31(5): 833–847.
Burnham, K. P., Anderson, D. R. 2002. Model Selection
and Multimodel Inference: a Practical Information-theoretic
Approach. 2nd ed. Springer, New York.
Castaño, J., Cardona, D. y Botero, J. 2010. Ecología del
mono nocturno andino (Aotus lemurinus) en fragmentos
de bosque subandinos de Colombia. En: Primatologia en
Colombia: avances al principio del milenio, V. Pereira-Ben-
goa, P. R. Stevenson, M. L. Bueno y F. Nassar-Montoya
(eds.), pp.69-90. Fundación Universitaria San Martín,
Bogotá, Colombia.
CMP-e Conservation Measures Pantnership. 2007. e
Open Standards for the Practice of Conservation, Release
2.0. USAID.
Cumming, G., Fidler, F. y Vaux, D. L. 2007. Error Bars in
Experimental biology. J. Cell Biol. 177(1): 7–11.
Deer, T. R. 2010. Historia Natural de Los Primates Co-
lombianos. Universidad Nacional de Colombia, Bogotá,
Colombia.
Deer, T. R. 1981. e Density of Alouatta seniculus in the
Eastern Llanos of Colombia. Primates 22(4): 564–569.
Elzinga, C. L. 2001. Monitoring Plant and Animal Popula-
tions. Blackwell Science, Malden, Mass.
Estrada, A., Castellanos, L., Garcia Y., Franco, B., Muñoz,
D., Ibarra A., Rivera, A., Fuentes E., Jiménez, C. 2002.
Survey of the black howler monkey, Alouatta pigra, popu-
lation at the Mayan site of Palenque, Chiapas, Mexico.
Primates 43(1): 51–58.
Fernandez-Duque, E., Rotundo, M. y Sloan, C. 2001.
Density and population structure of Owl Monkeys (Ao-
tus azarae) in the Argentinean Chaco. Am. J. Primatol.
53(3): 99–108.
Fundación Instituto de Inmunología de Colombia-FI-
DIC. 2007. Estimación del estatus actual de las pobla-
ciones naturales de micos del género Aotus en San Juan
de Atacuari en el trapecio amazónico colombiano. Le-
ticia, Amazonas.
Groombridge, B. 1992. Global Biodiversity. Status of the
Earth’s Living Resources: a Report. Chapman & Hall, Lon-
don-New York.
Heltne, P. G., Turner, D. C. y Scott. N. J. 1976. Compa-
rison of census data on Alouatta villosa (= palliata) from
Costa Rica and Panama. En: Neotropical Primates: Field
Studies and Conservation, R.J. orington and P.G. Helt-
ne (eds.), pp.10-19. National Academy of Sciences, Was-
hington, DC.
Hernández, A. y Díaz, A. 2010. Estado preliminar pobla-
cional del mono nocturno (Aotus sp. Humboldt 1812) en
las comunidades indígenas siete de agosto y San Juan de
Atacuari - Puerto Nariño, departamento de Amazonas,
Colombia. Ibagué, Tolima: Universidad del Tolima.
IUCN/SSC. 2013. Guidelines for Reintroductions and Other
Conservation Translocations. Version 1.0. IUCN Species
Survival Commission, Gland, Switzerland
IUCN 2017. e IUCN Red List of reatened Species.
Version 2017–2. <http://www.iucnredlist.org>. Down-
loaded on 14 September 2017.
Janson, C. H. 2011. Reconciling rigor and range: observa-
tions, experiments, and quasi-experiments in eld Prima-
tology. Int. J. Primatol. 33(3): 520–541.
Maldonado Rodríguez, Á. M. 2011. Tráco de monos noc-
turnos Aotus spp. en la frontera entre Colombia, Perú y
Brasil: efectos sobre sus poblaciones silvestres y violación
de las regulaciones internacionales de comercio de fauna
estipuladas por CITES. Rev. Acad. Colomb. Cienc. Exact.
Fis. Nat. 35(135): 225–242.
Maldonado, A., Shanee, S., Deer, T.R. y Roncancio, N. 2017.
Aotus nancymaae. e IUCN Red List of reatened Species
2017: e.T41540A17923258. http://dx.doi.org/10.2305/
IUCN.UK.2017-1.RLTS.T41540A17923258.en. Down-
loaded on 14 November 2017.
Peres, C. A. 1999. General guidelines for standardizing li-
ne-transect surveys of tropical forest primates. Neotrop.
Primates 7: 1–16.
Primack, R. B. 2010. Essentials of Conservation Biology. Si-
nauer Associates, Sunderland, Mass., USA.
Roncancio, N., Rojas, W. & Estevez, J. 2009. Densidad
poblacional y tamaño de grupo de Saguinus leucopus en
Parches de Bosque en el Departamento de Caldas, Co-
lombia. Neotrop. Primates 15 (2): 63–67.
Roncancio, N. 2012. Producto No. 4. Informe de avance
con la revisión inicial de los protocolos de reincorporación
de ejemplares del género Aotus a la vida silvestre. Informe
no publicado, Instituto Amazónico de Investigaciones
Cientícas SINCHI, Leticia, Amazonas, Colombia.
Struhsaker, T. T. 1981. Forest and primate conservation in
East Africa. Afr. J. Ecol. 19(1-2): 99–114.
Sutherland, W. J. 2000. e Conservation Handbook: Re-
search, Management and Policy. Wiley, Norwich, UK.
Neotropical Primates 25(1), December 2019 37
omas, L., Buckland, S.T., Rexstad, E.A., Laake, J. L.,
Strindberg, S., Hedley, S. L., Bishop, J. R.B., Marques,
T. A. y Burnham. K. P. 2010. Distance software: design
and analysis of distance sampling surveys for estimating
population size. J. Appl. Ecol. 47: 5–14.
Wright, P. C. 1978. Home range, activity pattern, and ago-
nistic encounters of a group of Night Monkeys (Aotus
trivirgatus) in Peru. Folia Primatol. 29(1): 43–55.
Neotropical Primates 25(1), December 201938
FIRST RECORDS OF GASTROINTESTINAL PARASITES IN WOOLLY MONKEYS (LAGOTHRIX
LAGOTHRICHA) IN COLOMBIA, FROM WILD, CAPTIVE AND REINTRODUCED INDIVIDUALS
Camilo Quiroga-González1, Elisa Jiménez1, Nelson F. Galvis1, Mónica A. Ramírez1
Mario Ortiz2, Camila Gonzalez2 and Pablo R. Stevenson1
1 Laboratorio de Ecología de Bosques Tropicales y Primatología (LEBTYP). Departamento de Ciencias Biológicas. Facultad de
Ciencias. Universidad de los Andes Bogotá, Colombia. E-mail:ca.quiroga158@uniandes.edu.co
2 Centro de Investigaciones en Microbiología y Parasitología Tropical (CIMPAT). Departamento de Ciencias Biológicas. Facultad
de Ciencias. Universidad de los Andes, Bogotá, Colombia. E-mail:mario-or@uniandes.edu.co
Abstract
Interest about parasites in vertebrate populations during translocation and reintroduction programs is increasing; thus, a
description of parasites in captivity infecting animals to be relocated is necessary. is study aimed to characterize the com-
munities of gastrointestinal parasites in woolly monkeys (Lagothrix lagothricha) from captive and wild individuals, as well
as the change in parasite prevalence in four individuals during a reintroduction process. To accomplish this goal, we used
a fecal otation technique to analyze the collected samples. In captivity, 95 % of the screened samples were infected with
at least one parasite, while only 77 % of wild primate samples showed infection, indicating higher prevalence in captive vs.
wild individuals. Overall, wild and captive woolly monkeys shared many groups of parasites (Strongylidae, Oxyuridae and
Entamoebidae) and we found a trend of lower parasite prevalence after release in captive individuals. Our data showed a
consistent dierence between captive and reintroduced individuals suggesting that variables related to diet, overcrowding
and human presence may be the most important factors explaining parasite communities.
Keywords: conservation ex-situ, woolly monkeys, nematodes, intestinal parasites.
Resumen
El interés sobre el impacto de los parásitos en las poblaciones de vertebrados durante los programas de translocación y rein-
troducción ha aumentado últimamente; esto hace necesario una descripción de los parásitos que infectan a los animales en
cautiverio que van a ser reubicados. El objetivo de este estudio fue el de caracterizar las comunidades de parásitos gastroin-
testinales en monos churuco (Lagothrix lagothricha) de individuos cautivos y silvestres, así como el cambio en la prevalencia
de parásitos en cuatro individuos durante un proceso de reintroducción. Para lograr este objetivo, utilizamos una técnica de
otación fecal para analizar las muestras colectadas. En cautiverio, el 95 % de las muestras examinadas estaban infectadas
con al menos un parásito, mientras que solo el 77 % de las muestras de primates silvestres mostraron infección, lo que indica
una mayor prevalencia en individuos en cautiverio frente a los silvestres. En general, los monos churuco salvajes y en cau-
tiverio compartieron muchos grupos de parásitos (Strongylidae, Oxyuridae y Entamoebidae) y se encontró una tendencia
de menor prevalencia después de la liberación de los individuos. Nuestros datos mostraron una diferencia consistente entre
individuos cautivos y reintroducidos, lo que sugiere que variables relacionadas con la dieta, hacinamiento y la presencia
humana pueden ser los factores más importantes que explican las comunidades de parásitos.
Palabras clave: conservación exsitu, churucos, nematodos, parásitos intestinales
Introduction
Primates are one of the most important taxonomic groups
in terms of conservation challenges, due to the danger of
extinction most of them face (Chinchilla et al., 2005; Es-
trada et al., 2017). Non-human primates are particularly
susceptible to parasitic infections because they can get in-
fected from other animal parasites, in spite of not being the
primary host (Johnson-Delaney, 2009). In addition, pri-
mates are vulnerable to parasitic infections due to the social
structure, which facilitates their transmission (Freeland,
1983). Habitat fragmentation and population size can
also compromise the population’s health and increase the
prevalence and richness of parasites (Gillespie and Chap-
man, 2008; Püttker et al., 2008). at is the reason why
the prevalence of parasites usually increases in smaller areas
where the possibility of re-infection is higher caused by an
unusual increase in primate crowding (Müller, 2007). is
is the scenario in zoos and rescue centers, where high popu-
lation densities and poor sanitation favor high prevalence
of parasites (Guerrero et al., 2012).
Information about gastrointestinal parasites in Old-World
primates is well known (Gillespie et al., 2005; Opara et
al., 2010; Petrezelkova et al., 2010), on the contrary, in
South America information gaps remain and an enormous
Neotropical Primates 25(1), December 2019 39
sampling eort is needed (Hopkins and Nunn 2007).
Woolly monkeys (Lagothrix lagothricha) are among the less
well-known species and to our knowledge, in Colombia
there are no studies describing gastrointestinal parasites
either from wild or captive populations. ese primates
are critically endangered according to IUCN (2008) due
to hunting pressure and habitat fragmentation that have
reduced the natural populations of this species to local
extinction in some areas (Stevenson and Aldana, 2008).
In this context, the aim of this study is to provide a rst
characterization of gastrointestinal parasite communities in
Colombian woolly monkeys (Lagothrix lagothricha) from
captive and wild individuals, and to characterize the para-
site community in four reintroduced individuals. We rst
evaluated if there were dierences in the prevalence of gas-
trointestinal parasites between captive and wild individuals
to evaluate if they shared the same parasites. en, we com-
pared these results with parasites found in reintroduced
individuals into the wild, to assess the potential parasite
loss or gain after release. We expected a higher density of
zoonotic parasites in captive individuals, given their prox-
imity to humans and their limited home range. Similarly,
we expected a higher prevalence of parasites in captive pri-
mates compared to released ones as a result of changes in
population density and diet.
Methods
Study Sites
Fecal samples from captive primates were collected between
June and November 2015 in two dierent enclosure sites
in Colombia. e rst site was Fundación Bioandina lo-
cated at Mesitas, Cundinamarca (4° 34’36.603’’N, 74° 27’
3.944’’W). is captivity site is located at an altitude of 990
m a.s.l. with a mean annual precipitation of 1,561 mm, and
temperature ranges between 17.3 – 26.8 °C. (Fig. 1).
Here we found ve individuals, two adult females, one
adult male, one sub-adult female and one juvenile female
belonging to two subspecies (Lagothrix lagothicha lugens
and Lagothrix lagothricha lagothricha). e individuals
were found in two small enclosures located side by side per-
mitting contact between them. e other site was Pereira`s
Centro de Atención y Valoración (CAV), Risaralda (4°
48’ 17.176’’N, 75° 47’ 1.687’’W). is captivity site is
located at an altitude of 1,411 m a.s.l. with a mean annual
precipitation of 2,441 mm. Temperature ranges between
14.7 – 26.8 °C (Fig. 1). Here we found four individuals,
two adult males, one adult female, and one juvenile female,
also from both subspecies. All the individuals were located
in a big enclosure enriched with sticks and planks to en-
courage their locomotion.
Samples from wild individuals were obtained between Sep-
tember 2010 to April 2013 from two groups of wild woolly
monkeys (L. l. lugens) inhabiting a pristine forest in Parque
Nacional Natural Cueva de Los Guacharos (PNNCG),
Huila, Colombia (1° 33’ 0’’ N, 76° 7’ 59.998’’ W). is
National Park is located in a montane forest with an ex-
tension of 9,000 hectares with a mean altitude of 2,000
m a.s.l. and a mean annual precipitation of 3,100 mm;
temperature ranges between 12 – 20 °C (Fig. 1). Here we
found two habituated woolly monkey groups varying in
size from 18 to 27 individuals.
Figure 1. Map showing the dierent study sites where primates
were sampled. e shape of the gures corresponds to the three
dierent conditions of the sampled individuals.
Regarding reintroduced primates, fecal samples from two
captive individuals were taken between March and July
2017 from a captivity site at Teruel’s CAV, Huila (2° 49’
53.93’’N, 75° 50’ 0.775’’W). is captivity site is lo-
cated at an altitude of 910 m a.s.l. with a mean annual
precipitation of 1635 mm; temperature ranges between
19.1 – 30.3 °C (Fig. 1). e individuals shared a big en-
riched enclosure (260 m3) with 10 other primates. ey
were fed twice a day with a mixture of fruits and veg-
etables that does not correspond to their diet in natural
habitats. Individuals were released in August 2017 in
a biological corridor located at El Pensil, Huila (1° 45’
43.949’’N, 76° 17’ 11.68’’W). is forest is located at a
mean altitude of 1,850m a.s.l. with a mean annual pre-
cipitation of 2,284 mm, and temperature ranges between
12 – 20 °C (Fig. 1). Fecal samples were collected from the
moment of release through March 2018. e other two
individuals were sampled in captivity at Teruel between
March of 2018 and November of the same year and re-
leased in a Biological Reserve located in San Martín, Meta
(3° 31’ 6.24’’N, 73° 24’ 11.88’’ W). is release site is
Neotropical Primates 25(1), December 201940
located at a mean altitude of 280 m a.s.l. and a mean
annual precipitation of 2,513 mm; temperature ranges
25 – 28 °C (Fig. 1). Fecal samples were obtained from the
time of release through April 2019.
Sample collection
Fecal samples were collected immediately after defeca-
tion and to avoid environmental contamination, only
2 grams of primate feces not in direct contact with the
ground were sampled in 15 ml Falcon tubes lled with
10 % formaldehyde. Tubes were shaken to maximize the
contact surface between the sample and formaldehyde.
For each sample, study site, date, time, individual name
and sex were recorded. e samples were kept at room
temperature until transport to Laboratorio de Ecología
de Bosques Tropicales y Primatología (LEBTYP) at Uni-
versidad de Los Andes, Colombia where they were stored
until processing.
Sample processing
Samples were processed at Centro de Investigaciones en
Microbiología y Parasitología Tropical (CIMPAT) at Uni-
versidad de los Andes, Colombia. For parasite identica-
tion, we followed the fecal otation method suggested by
Gillespie (2006), using a saline solution calibrated with
a pycnometer at a specic gravity of 1.28. One gram of
each preserved sample was placed in a 15 ml Falcon tube
lled 2/3 with distilled water and the sample was homog-
enized. en the sample was manually centrifuged for
10 minutes, the supernatant was discarded, and the fecal
matter was re-suspended with the saline solution lling
the tube to form an inverted meniscus where a cover slip
was placed. After centrifuging manually for 10 minutes,
the cover slip was removed and analyzed under a micro-
scope using 4x, 10x and 40x magnication. Eggs, cysts
and larvae were counted and measured with a microm-
eter. We used a drop of dilute Lugol’s iodine solution
(20 %) to facilitate the identication of protozoan cysts.
Photos of representative individuals were taken.
Data analysis
Information of parasite prevalence was dened as the num-
ber of samples infected with one parasite group divided by
the total number of samples taken in each study site. We
performed Chi-square analysis between the prevalence of
each group of parasites to identify the dierence in parasite
communities between study sites.
Results
A total of 185 samples were collected and analyzed. From
these, 43 belonged to wild woolly monkeys, 41 to captive
and 101 to reintroduced (56 taken when still in captivity and
28 after release into the wild at Pensil and 17 at San Martín).
A great variety of gastrointestinal parasites was found: six
Nematode families (Trichostrongylidae, Oxyuridae, Ancy-
lostomatidae, Ascarididae, Strongylidae and Trichinellidae),
eggs belonging to the class Cestoda and Trematoda, and one
protist belonging to the family Entamoebidae (Fig. 2).
In captive individuals at Mesitas and Pereira, we found that
95 % of the samples had at least one parasite individual (egg,
cyst or larvae) and 90 % had polyparasitism. We identied
ve groups of parasites: four members of the phylum Nema-
toda (Trichostrongylidae, Strongylidae, Trichinellidae and
Oxyuridae) and one protist of the family Entamoebidae.
Families with higher prevalence were Oxyuridae (83 % of
samples in Mesitas), and Trichstrongylidae (80 % in Mesi-
tas and 88 % in Pereira).
We found signicant dierences between samples taken
from primates in captivity sites (X2 = 76.1, df = 5, p < 0.01)
due to the fact that Pereira was the only study site where
family Trichinellidae was recorded. When prevalence of
parasitic families between the two captivity sites was com-
pared, we only found signicant dierences in the Oxyruri-
dae, for which Mesitas had a greater prevalence (X2 = 9.96,
df = 1, p < 0.05) (Fig. 3).
Figure 2. Gastrointestinal parasites found in captive and/or wild woolly monkeys. (A) Trichostrongylidae, (B) Oxyuridae,
(C) Ancylostomatidae, (D) Ascarididae, egg without cortex (E) Ascarididae, (F) Strongylidae, (G) Trichinellidae, (H) Trema-
toda, (I) Cestoda, (J) Entamoebidae.
Neotropical Primates 25(1), December 2019 41
Figure 3. Prevalence of gastrointestinal parasites in woolly mon-
keys in each captive site. Mesitas (n = 24), Pereira (n = 17).
Regarding wild woolly monkeys at PNNCG, we found
that 77 % of the samples analyzed had at least one parasite
individual. We identied ve groups of parasites: a protist
from the family Entamoebidae, three nematode families
(Oxyuridae, Ascarididae and Strongylidae) and one Ces-
tode. We found that 46 % of the samples had Helminths
and 42 % Protists.
When we evaluated the samples of the reintroduced indi-
viduals, we found eight groups of parasites, ve helminths
(Trichostrongylidae, Oxyuridae, Ascarididae, Ancylostoma-
tidae and Strongylidae), one protist (Entamoebidae), one
Trematode and one Cestode. In both reintroduction sites,
we found signicant dierences between captive and released
individuals (Pensil: X2 = 57.8, df = 8, p <0.01 and San Mar-
tín: X2 = 69, df = 8, p < 0.01) where a prevalence reduction
was shown in almost all parasite groups. Based on this result
we separated the samples in captive and released categories
for further analysis. We found an evident reduction of posi-
tive samples for almost all nematodes (X2 = 31.692, df = 8,
p < 0.01) including families Trichostrongylidae, Oxyuridae,
Ancylostomatidae and Ascarididae (Fig. 4).
Figure 4. Prevalence of gastrointestinal parasites in woolly monkeys in captive
(n = 56) and released (n = 45) individuals.
We observed that captive individuals had a higher prevalence
of nematodes than wild and released ones but no dierences
in the prevalence of protists and cestodes were found. Also,
we found that trematodes were present in captive and re-
leased individuals but not in the wild (Table 1).
Table 1. Prevalence (positive samples/total samples (*100)) of
gastrointestinal parasites in captive individuals in Teruel, wild in-
dividuals at PNNCG and released individuals at Pensil and San
Martín.
Captive
(n = 56)
Wild
(n = 43)
Released
(n = 45)
Nematodes 91 % 46 % 45 %
Protists 43 % 42 % 37 %
Trematodes 4 % 0 % 2 %
Cestodes 4 % 2 % 7 %
Discussion
For the rst time, gastrointestinal parasites infecting cap-
tive and wild Colombian woolly monkeys were studied. As
expected, many of the parasite families found have been
reported in the same primate genus (Michaud et al., 2003;
Larrañaga and Shanee, 2012; Pinto et al., 2013) but we
found four new parasite records for these primates: Ent-
amoebidae, Trichostrongylidae, Trematoda and Cestoda.
We found dierences between sites where primates were
held in captivity since the family Oxyuridae had a higher
prevalence in Mesitas compared to Pereira. is can be
explained by the fact that these parasites are transmitted
mainly by contact between individuals, and overcrowding
in captivity can promote this behavior facilitating their
transmission (González-Hernández et al., 2014). All para-
sites present in Mesitas and Pereira have been commonly
reported in captivity sites or near urban areas in dierent
primate species (Hasegawa et al., 2004; Soto-Calderón et
Neotropical Primates 25(1), December 201942
al., 2016) and have been reported in humans, which may
suggest possible zoonotic infections (Yamashita, 1963; Le-
gesse and Erko, 2004). Parasites found in captivity were
similar to the ones found in the wild at PNNCG. ree
of the ve parasite families found there (Strongylidae, Oxy-
uridae and Entamoebidae) were found in wild woolly mon-
keys with the exception of Trichinellidae and members of
the Trichostrongylidae family that only appeared in captiv-
ity. Ascarididae and Cestoda were the parasites found in
the wild that were absent in captivity.
As for the reintroduced individuals, we found a tendency
to reduction in parasite prevalence after being released.
ese dierences between sites can be associated to higher
rates of infection in the captivity sites due to overcrowding,
since primates share the enclosure with other 10 individu-
als. e higher prevalence of family Trichostrongylidae,
Oxyuridae, Ancylostomatidae and Ascarididae may be
because these parasites are geohelminths (Bethony et al.,
2006; Botero and Restrepo, 2015) and infect the primates
when they come into contact with the oor. e presence
of members of the Ascarididae family supports this idea,
since these parasites need a maturation time in the oor
before being infective (CDC, 2010). On the contrary, re-
leased individuals have better chances to explore higher for-
est strata and avoid contact with these parasites. e higher
prevalence of Oxyuridae may be explained by the reasons
we mentioned before that these parasites are transmitted
mainly by contact between individuals. A similar situation
has been reported in spider monkeys, where the number
of grooming interactions was positively correlated to the
presence of Strongyloides and Trichostrongylus (Rimbach et
al., 2015). Fewer encounters with conspecics can then
reduce the prevalence of parasites in released individuals
when compared to those in captivity.
Another factor that may be inuencing dierences in
parasite prevalence is primate diet. Many authors have
reported a negative relation between the consumption of
some plants and parasitic infections (Human et al. 1997;
Stoner and González-Di Pierro 2006). Many of the plant
families that primates consume in the wild and were not
consumed in captivity belong to the families Moraceae,
Rubiaceae, Araceae and Lauraceae, which have been found
to have deworming eects (Waller et al. 2001; MacIntosh
and Human 2010). ese plant families are consumed
by woolly monkeys in high and low lands (Stevenson et
al. 1994 and Ramirez et al. 2014), perhaps a switch on
the diet in reintroduced individuals promoted a reduction
in some parasite prevalence’s similar to the ones in wild
individuals.
Our data showed a consistent dierence between study
sites suggesting that diet, overcrowding and human pres-
ence may be the most important factors explaining parasite
communities in woolly monkeys in Colombia. We do not
consider environmental variables to be playing an impor-
tant role, since captivity sites were dierent among them,
but similar in parasite communities; the same tendency was
found in wild and released individuals. Due to the fact that
some parasites were found in captive and released individu-
als, but not in the wild ones, we support the idea of restor-
ing parasite-host balance before releasing the individuals as
Armstrong and Seddon proposed (2008). To achieve this,
it is convenient to reduce the number of individuals in an
enclosure and limit the contact of the individuals with the
ground to reduce infection rates and zoonotic infections.
Additionally, it may be useful to provide the primates with
deworming plants, mainly those common in the diet of
wild woolly monkeys prior to reintroduction.
Acknowledgments
We would like to thank Camila Orozco, Tatiana Novoa and
Santiago Yamaga for their help with sample collection. To
all members of LEBTYP and CIMPAT for their support
and collaboration. To Fundación Bioandina and Pereira´s
CAV. To Cindy and Alvaro, members of the Teruel´s CAV
for their help with the health of the individuals. To Cor-
poración del Alto Magdalena (CAM) and CORMACARE-
NA for providing us with a place to carry out the rehabilita-
tion and reintroduction of the primates and the constant
interest toward the project. is project was funded by
Fundación Alejandro Ángel Escobar, Colciencias (Project
code: 120465843684) and a teaching assistantship from
the Faculty of Sciences at Universidad de los Andes.
References
Armstrong, D. P. and Seddon, P. J. 2008. Directions in re-
introduction biology. Trends Ecol. Evol. 23: 20–25.
Bethony, J., Brooker, S., Albonico, M., Geiger, S. M., Lou-
kas, A., Diemert, D., and Hotez, P. J. 2006. Soil-
transmitted helminth infections: ascariasis, trichuriasis,
and hookworm. Lancet 367: 1521–1532.
Botero, D. and Restrepo, M., 2012. Parasitosis humanas.
Quinta Ed. Corporación para Investigaciones Biológicas,
Medellín.
Centers for Disease Control and Prevention. 2010.
Website: https://www.cdc.gov/dpdx/ascariasis/index.
html. Accessed 19 January 2019.
Chinchilla, M., Guerrero, O., Gutierrez–Ezpeleta, G., San-
chez, R and Rodrıguez, B. 2005. Parásitos intestinales en
monos congo Alouatta palliata (Primates: Cebidae) de
Costa Rica. Rev. Biol. Trop. 53: 437–44
Day, T. D., Waas, J. R., O’Connor, C. E., Carey, P. W.,
Matthews, L. R., and Pearson, A. J. 1997. Leptospiro-
sis in brushtail possums: is Leptospira interrogans serovar
balcanica environmentally transmitted? J. Wildl. Dis. 33:
254–260.
Estrada, A., Garber, P. A., Rylands, A. B., Roos, C., Fer-
nandez-Duque, E., Di Fiore, A., and Rovero, F. 2017.
Impending extinction crisis of the world’s primates: Why
primates matter.Sci. Adv. 3: 1–16.
Freeland, W.J. 1983. Parasites and the coexistence of ani-
mal host species. Am. Nat. 2: 223–236.
Neotropical Primates 25(1), December 2019 43
Gillespie, T. R., Greiner, E. C., and Chapman, C. A. 2005.
Gastrointestinal parasites of the colobus monkeys of
Uganda. J. Parasitol. 91: 569–573.
Gillespie, T. R., and Chapman, C. A. 2008. Forest frag-
mentation, the decline of an endangered primate, and
changes in host–parasite interactions relative to an un-
fragmented forest.Am. J. Primatol.70: 222–230.
Gillespie, T. R. 2006. Noninvasive assessment of gastroin-
testinal parasite infections in free-ranging primates. Int. J.
Primatol. 27: 1129–1143.
González-Hernández, M., Rangel-Negrín, A., Schoof, V.
A., Chapman, C. A., Canales- Espinosa, D., and Dias,
P. A. D. 2014. Transmission patterns of pinworms in two
sympatric congeneric primate species. Int. J. Primatol.
35: 445–462.
Guerrero, M. F., Serrano-Martínez, E. E., Tantaleán, V. M.,
Quispe, H. M., and Casas, V. G. 2012. Identicación de
parásitos gastrointestinales en primates no humanos del
Zoológico Parque Natural de Pucallpa, Perú. Rev. Inves-
tig. Vet. Perú 23: 469–476.
Hasegawa, H., Ikeda, Y., de Jesús Díaz-Aquino, J., and
Fukui, D. 2004. Redescription of two pinworms from
the black-handed spider monkey, Ateles geoffroyi, with
reestablishment of Oxyuronema and Buckleyenterobius
(Nematoda: Oxyuroidea).Comp. Parasitol.71: 166–175.
Hopkins, M. E. and Nunn, C. L. 2007. A global gap analy-
sis of infectious agents in wild primates.Divers. Distrib.
13: 561–572.
Human, M. A. 1997. Current evidence for selfmedica-
tion in primates: a multidisciplinary perspective. Am. J.
Phys. Anthropol. 104: 171–200.
IUCN. 2008. Stevenson, P. R, Link A. Lagothrix lugens.
IUCN Red List of reatened Species. Website: http://
www.iucnredlist.org/details/39926/0. Accessed 17 Janu-
ary 2019.
Johnson-Delaney, C. A. 2009. Parasites of captive nonhu-
man primates. Vet. Clin. North Am. Exot. 12: 563–581.
Larrañaga, J. S. and Shanee, S. 2012. Parasitos Gastrointes-
tinales en el Mono Choro Cola Amarilla (Oreonax flavi-
cauda) y el Mono Nocturno Andino (Aotus miconax) en
Amazonas, Peru.Neotrop. Primates. 19: 38–42.
Legesse, M. and Erko, B. 2004. Zoonotic intestinal parasites
in Papio anubis (baboon) and Cercopithecus aethiops (vervet)
from four localities in Ethiopia.Acta Trop. 90: 231–236.
MacIntosh, A. J. and Human, M. A. 2010. Topic 3: To-
ward understanding the role of diet in host–parasite in-
teractions: e case for Japanese Macaques. e Japanese
Macaques. pp. 323–344. Springer, Tokyo.
Michaud, C., Tantalean, M., Ique, C., Montoya, E. and
Gozalo, A. 2003. A survey for helminth parasites in fe-
ral New World nonhuman primate populations and its
comparison with parasitological data from man in the
region. J. Med. Primatol. 32: 341–345.
Müller, B. 2007. Determinants of the diversity of intestinal
parasite communities in sympatric New World Primates
(Saguinus mystax, Saguinus fuscicollis, Callicebus cupreus).
Doctoral esis. Tierärztliche Hochschule Hannover,
Hannover, Germany
Opara, M. N., Osuji, C. T. and Opara, J. A. 2010. Gastro-
intestinal parasitism in captive animals at the Zoological
Garden, Nekede Owerri, Southeast Nigeria. Ostrich. 1:
21–28.
Petrželková, K. J., Hasegawa, H., Appleton, C. C., Hu-
man, M. A., Archer, C. E., Moscovice, L. R. and Kaur, T.
2010. Gastrointestinal parasites of the chimpanzee popu-
lation introduced onto Rubondo Island National Park,
Tanzania.Am. J. Primatol. 72: 307–316.
Pinto, H. A., Ferreira Junior, F. C., Mati, V. L. T. and Melo,
A. L. D. 2013. Trypanoxyuris (Paraoxyuronema) lagothri-
cis (Nematoda: Oxyuridae) in Lagothrix cana (Primates:
Atelidae) from Brazil.Rev. Bras. Parasitol. V. 22: 307–311.
Püttker, T., MeyerLucht, Y. and Sommer, S. 2008. Ef-
fects of fragmentation on parasite burden (nematodes) of
generalist and specialist small mammal species in second-
ary forest fragments of the coastal Atlantic Forest, Bra-
zil.Ecol. Res. 23: 207–215.
Ramírez, M. A., Galvis, N. F., Vargas, S. A., Léon, J. J.,
Cifuentes, E. F. and Stevenson, P. R. 2014. Seed disper-
sal by woolly monkeys in Cueva de los Guácharos Na-
tional Park (Colombia): an Amazonian primate dispers-
ing montane plants. High altitude primates. pp. 103–114.
Springer, New York, NY.
Rimbach, R., Bisanzio, D., Galvis, N., Link, A., Di Fiore,
A. and Gillespie, T. R. 2015. Brown spider monkeys
(Ateles hybridus): A model for dierentiating the role of
social networks and physical contact on parasite trans-
mission dynamics. Philos. T. R. Soc. B. 370, doi:10.1098/
rstb.2014.0110.
SotoCalderón, I. D., AcevedoGarcés, Y. A., ÁlvarezCar-
dona, J., HernándezCastro, C. and GarcíaMontoya, G.
M. 2016. Physiological and parasitological implications
of living in a city: the case of the whitefooted tamarin
(Saguinus leucopus).Am. J. Primatol. 78: 1272–1281.
Stevenson, P. R. and Aldana, A. M. 2008. Potential eects
of Ateline extinction and forest fragmentation on plant
diversity and composition in the western Orinoco Basin,
Colombia. Int. J. Primatol. 29: 365–377.
Stoner, K. E. and González-Di Pierro, A. 2006. Intestinal
parasitic infections in Alouatta pigra in tropical rainforest
in Lacandona, Chiapas, Mexico: Implications for behav-
ioral ecology and conservation. In: New Perspectives in
the Study of Mesoamerican Primates: Distribution, Ecology,
Behavior and Conservation, Estrada, A, Garber, P, Pavelka
M. S. M and Luecka, L. (eds), pp. 215–240. Springer
Press, New York.
Waller, P. J., Bernes, G., amsborg, S. M., Sukura, A.,
Richter, S. H., Ingebrigtsen, K. and Höglund, J. 2001.
Plants as de-worming agents of livestock in the Nordic
countries: historical perspective, popular beliefs and pros-
pects for the future. Acta Vet. Scand. 42: 31–44.
Yamashita, J. 1963. Ecological relationships between para-
sites and primates.Primates. 4: 1–96.
Neotropical Primates 25(1), December 201944
S A
FUR RUBBING BEHAVIOUR IN FREE RANG
ING BENI TITI MONKEYS (PLECTUROCEBUS
MODESTUS) IN BOLIVIA
Jesús Martínez
Freddy Zenteno-Ruiz
Laura Moya
Pamela Carvajal
Robert Wallace
Introduction
Fur rubbing is a mammalian behaviour in which a foreign
substance is vigorously rubbed over some parts of the body
with hands or feet (Baker, 1996; Human, 1997; Paukner
and Suomi 2012). is behaviour has been observed in
Neotropical primate species using distinct substances such
as plant parts or insects, and has been related to distinct
functions. Health benets of fur rubbing were inferred as
protection against mosquito blooms in rainy months and
for healing wounds from fur rubbing observed in white-
faced capuchin monkeys (Cebus capucinus), as insecticid-
al – repellent and fungistatic properties were found in one
of those plant species used (Piper tuberculatum; Human,
1997; Palacios et al., 2009; Bazán-Calderón et al., 2011).
Repellent functions were also suggested for plants used in
fur rubbing by robust capuchins, Sapajus apella (Paukner
and Suomi, 2008).
e repellent functions of fur rubbing seem valid when
substances are spread over most of the individual’s body as
was observed in white-faced capuchin monkeys (C. capuci-
nus; Baker, 1996). Nevertheless, Campbell (2000) related
extensive fur rubbing behavior as a part of social interac-
tion in spider monkeys (Ateles geoffroyi), when they applied
foreign substances on some parts of their bodies. Potential
changes in olfactory cues between individuals after applying
pungent substances to fur could increase aliative intra-
group interactions. However, after unexpected aggressive
interactions were observed in captive capuchin monkeys
(Sapajus apella) after fur rubbing behavior, Paukner and
Suomi (2008, 2012) hypothesized that the medicinal pur-
poses of fur rubbing could be more relevant than group
cohesion ones.
Fur rubbing has also been observed in some titi monkey
species. Individuals of Cheracebus torquatus rubbed fur
from throat to chest with a small ball of wadded uniden-
tied leaves wetted with saliva (Deer, 2010). Similar
behaviour was observed in Plecturocebus donacophilus us-
ing leaves of Piper tuberculatum (Ryan, 2011), a plant
with insecticidal and fungicidal properties (Palacios et al.,
2009; Bazán-Calderón et al., 2011). Recently, important
eorts have been made to increase natural history knowl-
edge and promote conservation actions for Plecturocebus
modestus, an Endangered titi monkey species endemic to
Bolivia (Veiga et al., 2008; Martinez and Wallace, 2010,
2016; Wallace et al., 2013). Here we report fur rubbing
using plants observed in individuals of two groups of P.
modestus, during a behavioral study of the species. We
provide details regarding plant species used, individu-
als involved, and seasonal variations in the frequency of
fur rubbing, as well as attempt to elucidate the probable
function of this behaviour.
Methods
We conducted our study at San Miguel cattle ranch locat-
ed in the southwestern portion of the Beni Department,
Bolivia (13°57’5.49”S, 66°50’5.07”W). is site, selected
according to available distributional information for Plec-
turocebus modestus (Felton et al., 2006; Martinez and Wal-
lace, 2007; Wallace et al., 2013), is in the Llanos de Moxos
ecosystem characterized by a landscape dominated by a
grassland matrix where forest patches are immersed (Han-
agarth, 1993). We selected two groups of P. modestus to
be observed. e Maramacho group had four individuals
(adult pair, one juvenile and one infant) inhabiting an area
of large forest patches (>10 ha), and the Corral group had
two adult individuals occurring in an area of small forest
patches.
We sampled the occurrence of unusual behaviours such as
fur rubbing by means of ad libitum sampling (Altmann,
1974), registering the duration of each fur rubbing event.
We observed the focal groups all day from sunrise to sunset
for 10 days per month, during 12 months (July 2010 – June
2011) covering dry and wet seasons. We calculated abso-
lute frequencies and time accumulated in fur rubbing for
each focal group and individual. Plant species used in fur
rubbing were collected and voucher specimens were identi-
ed at the Bolivian Herbarium in La Paz.
Results
In all our observations, fur rubbing consisted of an individ-
ual harvesting leaves of a plant that were then chewed for
a short time, before the monkey rubbed the chewed plant
mixture against its throat and chest with repeated energetic
vertical movements. Titi monkeys used both hands for
this task and chewed the leaves several times while they sat
upright on branches, looking ahead. Although the behav-
ioural display was similar between focal groups, the plant
species used varied. Individuals of the Maramacho group
used leaves of the herb Piper callosum (Piperaceae, collec-
tion number FZR-17816), while the Corral group used
leaves of the vine Tynanthus schumannianus (Bignoniaceae,
collection number FZR-17817). Leaves of both plant spe-
cies had a mint smell and were dropped after fur rubbing.
ey were never eaten.
Neotropical Primates 25(1), December 2019 45
Most of the fur rubbing observed was performed by the
Corral group in the small forest patches (18 events, 73
minutes, on 8 days), and both adult individuals per-
formed this behaviour (Table 1). Fur rubbing was less
frequent in the Maramacho group (3 events, 7 minutes,
on 2 days) where only the adult male and juvenile female
performed fur rubbing.
Table 1. Accumulated time and frequency of fur rubbing for each individual of focal groups of Plecturocebus modestus (rows in bold cor-
respond to total time for each group).
Group Individual Age Sex Time accumulated [min]
(number of events)
Total Rain Dry
CORRAL Mandingo Adult Male 38(9) 31(7) 7(2)
Natusha Adult Female 35(9) 35(9) 0(0)
73(18) 66(16) 7(2)
MARAMACHO Timoteo Adult Male 4(2) 4(2) 0(0)
Lita Juvenile Female 3(1) 3(1) 0(0)
7(3) 7(3) 0(0)
Total 80(21) 73(19) 7(2)
Observation time (hours)
CORRAL 1143.8 582.8 561.0
MARAMACHO 1235.7 619.0 616.7
e adult male of the Maramacho group performed fur
rubbing alone one time (15 % of the fur rubbing group
time), and once just before the juvenile female (85 % of
the accumulated group time). For the Corral group, most
of the fur rubbing was performed by the adult pair simul-
taneously (5 of 8 days, 84.9 % of accumulated group fur
rubbing time), on two days the male fur rubbed alone
(9.6 % of fur rubbing time), and on one day the female
fur rubbed alone (5.5 % of fur rubbing time). Titi mon-
keys performed fur rubbing separately, without any kind of
body contact between them, even in those cases when two
individuals were engaged in this activity in close proxim-
ity. Fur rubbing was observed almost exclusively in the wet
season except two events involving the adult male of Corral
group (9.6 % of accumulated group time, Table 1).
No special situations were observed on the days when the
individuals of Maramacho group performed fur rubbing.
On two of the days when individuals of the Corral group
performed fur rubbing, we observed the adult male groom-
ing the adult female, and on one day he tasted the female’s
urine. However, grooming was commonly observed in this
group (37 % of observation days) and although only three
events of urine testing were observed during the study,
none of these observations occurred just after fur rubbing;
they occurred over a half an hour later.
Discussion
Plant species observed in fur rubbing by individuals of
Plecturocebus modestus are used in traditional medicine by
Amazonian people. Brazilian and Bolivian people prepare
a tea or poultice with leaves and stem pieces of Piper callo-
sum to treat digestive and diuretic illnesses, and fungistatic,
insecticidal, and antilarval properties found in this plant
suggest its use as repellent (Souto et al., 2012; Silva et al.,
2017; Bolivian Herbarium database). Similarly, tea made
with fruits and stem pieces of Tynanthus schumannianus
is traditionally used for treatment of diarrhea in Bolivia,
while active compounds for treatment of malaria were also
found in fruits of this vine with no apparent use as repel-
lent (Muñoz et al., 2000; Cansian et al., 2015). is plant
is used also to treat conjunctivitis and as women’s perfume
(Bolivian Herbarium database). As Beni titi monkeys did
not ingest the plants used in fur rubbing, some external
function such as repellent seems feasible for P. callosum.
Several primate species have sternal glands whose secretions
are used for scent marking (Ewer, 1968). Spider monkey
(Ateles geoffroyi) fur rubbing was related to scent mark-
ing, rubbing the chest against a substrate that seemed to
stimulate secretions of sternal glands (Campbell, 2000).
As scent marking shares diverse types of information about
an individual (such as identity, condition, and social rank),
fur rubbing could be related to social interactions through
chemical communication (NRC, 1998). Scent marking us-
ing the sternal gland was reported for Plecturocebus moloch
and Cheracebus torquatus, rubbing their chest on branches,
although with no clear function (Moynihan, 1966; Kinzey,
1981). Chest rubbing seemed to help re-establish friendly
relationships between individuals of captive C. torquatus af-
ter prolonged separation (Fernandez-Duque et al., 1997).
e fact that we did not observe any scent marking be-
haviour nor prolonged separations of groups’ individuals
Neotropical Primates 25(1), December 201946
linked to fur rubbing, discards the scent marking function
for fur rubbing in our groups of Plecturocebus modestus.
Capuchins and owl monkeys engage in social fur rubbing,
with the participation of several individuals, using highly
available rubbing materials such as mud, ants, or plant
leaves, while solitary fur rubbing occurred with less abun-
dant materials such as owers or millipedes (Lynch et al.,
2012). e same authors describe dierent levels of con-
tact between individuals, such as rubbing on each other,
or individuals rubbing their body against another whom
already applied the rubbing substance. In our study, indi-
viduals performed fur rubbing with plants separately. Ad-
ditionally, despite some coincidence of fur rubbing with
grooming, there was not a direct relationship between the
two behaviours that could suggest some social context for
our fur rubbing observations.
Chemical communication could also help reproductive
success, as was observed in sifakas (Propithecus verreauxi).
Males of this species with stained chests caused by sternal
gland secretions had higher copulation rates than males
with clean chests (Dall’Olio et al., 2012). e only link we
could report between fur rubbing and mating was when
the Corral group male drank female’s urine on the same
day, but considerably later than the fur rubbing event. e
assessment of females’ fertility by male individuals based on
drinking their urine has been reported for other mammals
including the owl monkey Aotus nancymaae (Wolovich and
Evans, 2007). Nevertheless, one isolated observation does
not provide strong evidence for a link between mating be-
havior and fur rubbing.
Repellent functions, as well as usefulness against bacterial
or fungal skin infections, were attributed to fur rubbing
when substances were applied to almost the entire body,
and especially during rainy season when risks of insects’
bites and infections are higher (Human, 1997). is was
observed in capuchin monkeys such as Cebus capucinus
(Baker 1996), Sapajus cay (Giudice and Pavé, 2007), and
S. apella, as well as distinct species of Aotus owl monkeys
(Zito et al., 2003). In our case, the titi monkeys rubbed
their throat and chest in a similar way as reported for Ch-
eracebus torquatus (Deer, 2010), Plecturocebus donacophi-
lus (Ryan, 2011), and P. oenanthe (Huashuayo-Llamocca
and Heymann, 2017). e dense and long hair of titi mon-
keys, including P. modestus (Lönnberg, 1939; Martinez et
al., 2013), would help prevent access to skin for biting in-
sects, except for ventral zones with shorter and less dense
hair, probably more vulnerable to insect bites. e marked
occurrence of our fur rubbing observations during the wet
season corresponds with the period of higher risk of in-
sect bites due to increase of insect abundances (Human,
1997). Moreover, our focal groups occurred in ecotones of
forest and savannahs with higher insect diversity than sin-
gle habitats, including mosquito species that can be vectors
of tropical diseases (ongsripong et al., 2013). It is likely
that a high abundance of mosquitos or other biting insects
could be promoting the need of a repellent. erefore, our
observations of P. modestus treating their most vulnerable
body areas with plant substances during the riskiest insect
bite months suggest repellent as the most likely function of
fur rubbing for this species.
We presented data on an uncommon behaviour observed
in wild individuals of Plecturocebus modestus. Although we
did not determine a conclusive function of fur rubbing, we
provide valuable considerations for further research on the
ecology of this endemic and threatened primate.
Acknowledgements
We would like to thank the Wildlife Conservation Society,
the Gordon and Betty Moore Foundation, Primate Con-
servation Inc., Margot Marsh Biodiversity Foundation, the
BP Conservation Leadership Program and, the Conserva-
tion International Primate Action Fund for their contin-
ued nancial support. anks to the National Director-
ate for the Protection of Biodiversity for help in acquiring
necessary research permits, to the Bolivian Herbarium for
providing access to reference plant collections, as well as
the collaboration of the Municipality of Santa Rosa del
Yacuma, and especially the Nogales cattle ranches for access
to the study sites. Finally, we acknowledge the wonderful
support of our eld assistants Edson (Kayo) Gonzales and
Eduardo (Lalo) Fernandez, as well as Vilma Hidalgo and
volunteers who helped during eldwork.
Jesús Martínez, Wildlife Conservation Society, Casilla
3-35181 SM., San Miguel, La Paz, Bolivia. E-mail: < jmarti-
nez@wcs.org>, Freddy Zenteno-Ruiz, Wildlife Conserva-
tion Society, Casilla 3-35181 SM., San Miguel, La Paz,
Bolivia and Herbario Nacional de Bolivia, Instituto de
Ecología, Cota Calle 27 – Campus Universitario, Casilla
10077 La Paz, Bolivia, Laura Moya, Herbario Nacional
de Bolivia, Instituto de Ecología, Cota Calle 27 – Cam-
pus Universitario, Casilla 10077 La Paz, Bolivia, Pamela
Carvajal, Wildlife Conservation Society, Casilla 3-35181
SM., San Miguel, La Paz, Bolivia and, Robert Wallace,
Wildlife Conservation Society, Casilla 3-35181 SM., San
Miguel, La Paz, Bolivia, Wildlife Conservation Society,
185th Street and Southern Boulevard, Bronx, New York,
10460, U.S.A.
References
Altmann, J. 1974. Observational study of behaviour: sam-
pling methods. Behaviour 49:227-265.
Baker, M. 1996. Fur rubbing: use of medicinal plants by
capuchin monkeys (Cebus capucinus). Am. J. Primatol.
38:263–270.
Bazán-Calderón, J., Ventura-Flores, R., Kato, M. J., Rojas-
Idrogo, C., and Delgado-Paredes, G. E. 2011. Actividad
insecticida de Piper tuberculatum Jacq. sobre Aedes aegypti
L. (Diptera: Culicidae) y Anopheles pseudopunctipennis
Tehobal (Diptera: Culicidae). An. Biol. 33:135–147.
Neotropical Primates 25(1), December 2019 47
Campbell, C. J. 2000. Fur rubbing behavior in free-rang-
ing black-handed spider monkeys (Ateles geoffroyi) in
Panama. Am. J. Primatol. 51: 205–208.
Cansian, F. C., Merino, F. J. Z., Dias, J. F. G., Zanin,
S. M. W., Miguel, O. G., and Miguel, M. D. 2015.
Chemical view and studies related to species from ge-
nus Tynanthus (Bignoniaceae). Braz. J. Pharm. Sci. 51:
515–523.
Dall’Olio, S., Norscia, I., Antonacci, D., and Palagi, E.
2012. Sexual signalling in Propithecus verreauxi: male
“chest badge” and female mate choice. PLoS ONE. 7(5):
e37332 [doi:10.1371/journal.pone.0037332].
Deer, T. 2010. Historia natural de los primates colom-
bianos (2 edición). Universidad Nacional de Colombia.
Bogotá.
Ewer, R. F. 1968. Ethology of mammals. Springer
Science+Business Media, LCC. New York.
Felton, A., Felton, A. M., Wallace, R. B., and Gómez,
H. 2006. Identication, distribution and behavioral
observations of the titi monkeys Callicebus modestus
Lönnberg, 1939 and Callicebus olallae Lönnberg, 1939.
Primate Conserv. 20: 41–46.
Fernandez-Duque, E., Mason, W. A., and Mendoza, S.
P. 1997. Eects of duration of separation on responses
to mates and strangers in the monogamous titi monkey
(Callicebus moloch). Am. J. Primatol. 43: 225–237.
Giudice, A. M., and Pavé, R. 2007. Cebus paraguayanus
in zoos: the spontaneous expression of species-specic
behaviors. Neotrop. Primates. 41: 65–71.
Hanagarth, W. 1993. Acerca de la geología de las sabanas de
Beni en el norte de Bolivia. Instituto de Ecología. La Paz.
Huashuayo-Llamocca, R., and Heymann, E. W. 2017.
Fur-rubbing with Piper leaves in the San Martin titi
monkey, Callicebus oenanthe. Primate Biol. 4: 127–130.
Human, M. A. 1997. Current evidence of self-medica-
tion in primates: a multidisciplinary perspective. Yearb.
Phys. Anthropol. 40: 171–200.
Kinzey, W. G. 1981. e titi monkeys, genus Callicebus. In:
Ecology and Behavior of Neotropical Primates, Vol. 1, A. F.
Coimbra-Filho, and R. A. Mittermeier (eds.), pp.240–-
276. Academia Brasileira de Ciencias, Rio de Janeiro.
Lönnberg, E. (1939). Notes on some members of the ge-
nus Callicebus. Arkiv för zoology. 31: 1–18.
Lynch-Alfaro, J. W., Matthews, L., Boyette, A. H., Mac-
Farlan, S. J., Phillips, K. A., Falótico, T., Ottoni, E.,
Verderane, M., Izar, P., Schulte, M., Melin, A., Fedigan,
L., Janson, C., and Alfaro, M. E. 2012. Anointing vari-
ation across wild capuchin populations: a review of ma-
terial preferences, bout frequency and anointing social-
ity in Cebus and Sapajus. Am. J. Primatol. 74: 299–314.
Martinez, J, and Wallace, R. B. 2007. Further notes on
the distribution of endemic Bolivian titi monkeys, Cal-
licebus modestus and Callicebus olallae. Neotrop. Pri-
mates. 14: 47–54.
Martinez J, Wallace RB. 2010. Pitheciidae. In: Distribu-
ción, Ecología y Conservación de los Mamíferos Medianos
y Grandes de Bolivia, R. B. Wallace, H. Gómez, Z. R.
Porcel, and D. I. Rumiz (eds.), pp.305–330. Centro de
Ecología Difusión Simón I. Patiño, Santa Cruz de la
Sierra.
Martinez, J., Wallace, R. B., De la Torre, P., López-Strauss,
H., and Aranibar, H. 2013. Two new specimens for the
Bolivian titi monkeys, Callicebus olallae and Callicebus
modestus. Neotrop. Primates. 20: 39–44.
Martinez, J., and Wallace, R. B. 2016. Plecturocebus
modestus. In: All the world’s primates, N. Rowe, and M.
Myers (eds.), pp.197. Pogonias Press, Charlestown.
Moynihan, M. 1966. Communication in the titi monkey,
Callicebus. J. Zool. 150: 77–127.
Muñoz, V., Sauvain, M., Bourdy, G., Callapa, J., Rojas,
I., Vargas, L., Tae, A., and Deharo, E. 2000. e search
for natural bioactive compounds trough a multidisci-
plinary approach in Bolivia. Part II. Antimalarial activ-
ity of some plants used by Mosetene indians. J Ethno-
pharmacol. 69: 139–155.
National Research Council (NRC). 1998. e psychologi-
cal well-being of nonhuman primates. National Academy
Press. Washington.
Palacios, Z. G. F., Delgado, G. E., Moreno, M. C., Kato,
M. J., and Rojas, C. 2009. Actividad antifúngica in vi-
tro de extractos crudos de Piper tuberculatum. Rev. Peru.
Biol. 16: 209–214.
Paukner, A., and Suomi, S. J. 2008. e eects of fur
rubbing on the social behavior of tufted capuchin mon-
keys. Am. J. Primatol.70: 1007–1012.
Paukner, A., and Suomi, S. J. 2012. Social after-eects of
fur rubbing in tufted capuchins (Cebus apella): increas-
es in antagonism and decreases in aliation. Primates.
53:297–301.
Ryan, -. 2011. Fur rubbing in Callicebus: A personal
account. In: Titi tales: our stories of a small South
American monkey. Website: http://tititales.blogspot.
com/2011/03/fur-rubbing-in-callicebus-personal.html.
Accessed 15 October 2017.
Silva, R. J. F, de Aguiar-Dias, A. C. A, Faial, K. C. F,
and de Mendonça, M. S. 2017. Morphoanatomical and
physicochemical prole of Piper callosum: valuable as-
sessment for its quality control. Rev. Bras. Farmacogn.
27: 20–33.
Souto, R. N. P., Harada, A. Y., Andrade, E. H. A., and
Maia, J. G. S. 2012. Insecticidal activity of Piper es-
sential oils from the Amazon against the re ant Sole-
nopsis saevissima (Smith) (Hymenoptera: Formicidae).
Neotrop. Entomol. 41: 510–517.
ongsripong, P., Green, A., Kittayapong, P., Kapan,
D., Wilcox, B., and Bennett, S. 2013. Mosquito vec-
tor diversity across habitats in Central ailand en-
demic for dengue and other arthropod- borne diseases.
PLoS Negl. Trop. Dis. 7: e2507 [doi:10.1371/journal.
pntd.0002507].
Veiga, L. M., Wallace, R. B., and Martinez, J. 2008. Cal-
licebus modestus. In: IUCN, editors. IUCN Red List of
reatened Species. Version 2013.1. Website: http.//
www.iucnredlist.org. Accessed 25September 2017.
Neotropical Primates 25(1), December 201948
Wallace, R. B., Martinez, J., López-Strauss, H., Barreta,
J., Reinaga, A., and López, L. 2013. Conservation chal-
lenges facing two threatened endemic titi monkeys in
a naturally fragmented Bolivian forest. In: Primates in
fragments: complexity and resilience, L. K. Marsh, and
C. A. Chapman (eds.), pp.493–501. Springer Science,
New York.
Wolovich, C. K., and Evans, S. 2007. Sociosexual behav-
ior and chemical communication of Aotus nancymaae.
Int. J. Primatol. 28: 1299–1313.
Zito, M., Evans, S., and Weldon, P. J. 2003. Owl mon-
keys (Aotus spp.) self-anoint with plants and millipedes.
Folia Primatol. 74: 159–161.
GEOGRAPHICAL AND ALTITUDINAL RANGE
EXTENSION OF WHITEBELLIED SPIDER MON
KEYS ATELES BELZEBUTH IN THE NORTH
ERN ANDES OF COLOMBIA
Victoria Andrea Barrera
Camila Valdés Cardona
Luisa Mesa
Sebastian Nossa
Andrés Link
Introduction
e geographic distribution of white-bellied spider mon-
keys (Ateles belzebuth) has been debated extensively, and
there is no consensus on the historical continuity or dis-
continuity of its wild populations. Currently, white-bellied
spider monkeys are known to have a disjunct distribution
located across three regions: [1] the western piedmont of
the Eastern Andes and the lowland rainforests of Colom-
bia, [2] the forests in western Amazonia in Ecuador and
Peru, as well as from [3] southern Venezuela and north-
western Brazil (Fig. 1). As mentioned by the IUCN Red
List Assessment: “e distribution of this species is not well
known and dees easy description” (Link et al., 2019).
In Colombia, white-bellied spider monkeys are present
in the lowland rainforests of Tinigua and Macarena Na-
tional Parks, especially near the piedmont of the Eastern
Andes. Some populations also occur in Guaviare and
Caquetá departments, and a few “anecdotal” records have
been documented in south-eastern Colombia. Nonethe-
less, Deer (2003) proposed that this handful of records in
south-eastern Colombia actually correspond to isolated in-
dividuals, including two spider monkeys that were hunted
by local persons given its rarity in the region. ese spider
monkeys are not present across a broad area of the Ama-
zonian rainforests in Colombia (e.g. Amazonas depart-
ment), nor are they found in northern Ecuador, north of
the Cuyabeno River. us, based on reliable records, it
seems that populations of white-bellied spider monkeys are
divided into at least three disjoint populations (Fig. 1). e
biogeographical, ecological and even anthropological driv-
ers of this discontinuous distribution are still unknown.
Figure 1. Geographical distribution of Ateles belzebuth (IUCN
2019). Shadow denotes reported populations and grey symbol
denotes the northern population newly registered in this study.
e white-bellied spider monkey is classied as Endan-
gered by the IUCN Red List (Link et al., 2019) mainly
due to the loss of habitat and the estimated reduction of its
populations during the last decades. e demographic dy-
namics of white-bellied spider monkeys have been studied
in the Ecuadorian and Colombian Amazon (Shimooka et
al., 2008; Link et al. 2018) and it is clear that they have one
of the slowest development cycles amongst living primates,
with extended periods of infancy and sexual immaturity
(Link et al., 2018). It has been proposed that their slow
life history variables partly account for their high vulner-
ability to anthropogenic threats (Michalski & Peres, 2005).
White-bellied spider monkeys also have long periods of
development. Females begin reproducing only when they
are approximately 7 – 9 years, most often have singletons
(but see Link et al 2006), and have inter-birth intervals
of approximately 30 – 36 months (Shimooka et al., 2008;
Link et al., 2018). Spider monkeys also prefer undisturbed
forests where they use large areas (160 – 400 hectares) to
search for food, especially ripe eshy fruits (Di Fiore et al.,
2008). Spider monkeys’ large body size makes them pre-
ferred hunting items for many indigenous and local com-
munities, posing a strong threat on their wild populations
(Franzen, 2008).
Here, we report on a previously unknown population of
white-bellied spider monkeys living in the highland forests
in the Eastern slope of the Eastern Andes in Colombia,
in the departments of Casanare and Boyacá. is popula-
tion accounts for the northern-most record of white-bellied
spider monkeys in the Andes Piedmont in Colombia, and
is present in highland forests that extend its altitudinal
range to over 1,800 m. a.s.l. Given that in the Colom-
bian Andes during the last centuries there has been a dra-
matic transformation of natural forests into agricultural
elds and pastures for cattle ranching (Etter and van Wyn-
gaarden, 2000; Armenteras et al., 2011), it is possible to
Neotropical Primates 25(1), December 2019 49
speculate on the historical presence of a large and continu-
ous population that might have been connected to those
extant populations in northwestern Amazonia through a
lowland and highland forest corridor west of the natural
“Colombian and Venezuelan Llanos” savannas. We discuss
the implications of these new records in light of the urgent
need of conservation for these endangered primates in the
Neotropics.
Methods
Study area.
e forests where the initial sightings of white-bellied spi-
der monkeys took place in 2014 are located in the Eastern
slope of the Eastern Andes cordillera, in the municipal-
ity of El Yopal - Corregimiento El Morro, vereda Marro-
quín - (5° 29.938’N, 72° 26.818’W) (Fig. 2), in Casanare
Department. In 2018, we found other groups of white-
bellied spider monkeys in forest fragments in the same
broader region, specically in the municipality of La Paya
– veredas Guayabal de la Peña, La Unión and Milagros - (5°
35.626’N, 72° 21.218’W), in the department of Boyacá.
e two localities are roughly 15 km apart.
According to Holdridge (1979) the area is considered as
a premontane very humid forest and is characterized by
steep mountains that oscillate between 1,100 and 2,200 m.
a.s.l. Precipitation patterns are unimodal, with a rainy sea-
son from April through November, and a dry season from
December through March. Annual rainfall ranges between
2,000 – 4,500 mm and average temperature oscillates be-
tween 12°C – 18°C (IGAC, 1999). e landscape is com-
prised by a matrix of pastures devoted to cattle ranching,
subsistence agricultural plots and remnants of secondary
and primary forests. Most forests have been selectively
logged for timber but otherwise remain intact, although
deforestation takes place in the broader region; between
2014 -2016, 114 ha of primary and secondary forests were
cleared in the Paya alone (Pinza, unpublished data). How-
ever, since 2018, a payment for ecosystem services (PES)
strategy is being implemented through Voluntary Conser-
vation Agreements, where the owners of the forests receive
monetary incentives from an oil company that operates
down at the basin, as an environmental compensation, to
preserve the forest for at least three years.
Characterization of the population of white-bellied spider
monkeys in Casanare and Boyacá
We began to collect systematic data on the population of
white-bellied spider monkeys at Yopal in 2018 and at Paya
in 2019 (Fig. 2), as part of a regional on-going initiative
to protect and conserve Ateles belzebuth in the premon-
tane forests of the north-eastern Andes. We conducted
population surveys at El Yopal in order to estimate primate
population densities following the line transect methods
proposed by Peres (1993) and Buckland et al. (1993). At
Paya, we conducted ad libitum surveys in the forests during
January and February in 2019 and conducted line transect
surveys from April to September of the same year. For ev-
ery visual observation of white-bellied spider monkeys we
recorded the time of day, the number of individuals with
age and sex categories whenever possible, and the location
using a hand-held Garmin GPSMAP 64s Topo COL 100K
GPS Handheld Receiver with 2.6-Inches Blacklit Display.
Additionally, we conducted semi-structured interviews
with locals in order to obtain information on the presence
or absence of white-bellied spider monkeys in the dier-
ent forest fragments in the broader region. We also asked
for more detailed information (whenever possible) on the
number of groups/subgroups present, specic behaviors
and vocalizations, or other information about the species.
Figure 2. Records of Ateles belzebuth at Paya, Boyacá. Circles de-
note records from ad libitum surveys from January to February
2019; Triangles denote records from line transect surveys from
April to September 2019.
Results
During the initial surveys (July to October 2018) at the
municipality of Yopal we were unable to visually record the
presence of Ateles belzebuth, however we were able to record
several long-distance vocalizations, thus conrming their
presence in the area. Moreover, the interviewees conrmed
the presence of white-bellied spider monkeys in the adja-
cent forest fragments, and from the information gathered
during these interviews we could infer the presence of at
least two subgroups of around six individuals in dier-
ent parts of the forest as well as solitary females traveling
through the fragments, as expected given the high degree
of ssion-fusion dynamics described for the genus Ateles
(Symingon, 1990; Aureli and Schaner, 2008).
On the other hand, at Paya (January to March and April to
September 2019) we obtained 56 sightings of subgroups of
Ateles belzebuth in 170 ha of continuous forest (Appendix 1).
e subgroups ranged in size from 1 to 9 individuals with a
mean subgroup size of 3.8 individuals (SD = 2.5) (Appendix
1). is matches the information given by the peasants, who
had seen groups between 2 and 5 individuals of Ateles belze-
buth in both fragments, and closely resembles the average
Neotropical Primates 25(1), December 201950
subgroup size of other populations of white-bellied spider
monkeys in lowland forests (Link & Di Fiore, 2013).
In both localities, locals described two vocalizations: a long-
distance call and a “barking” or “repeated bark” alarm call,
previously described for several species of spider monkeys
(Eisenberg, 1976; León & Link, 2013). rough hearing
long-distance vocalizations, we were able to conrm the
presence of Ateles belzebuth at Yopal, and to locate the sub-
groups during the ad libitum and transect surveys at Paya.
Discussion
e distribution of white bellied spider monkeys has been
a matter of debate, given the current discontinuity between
populations found on the eastern slope of the eastern An-
des cordillera and in the Amazon rainforests (Link et al.,
2019). is study adds to this debate by documenting the
northernmost populations of Ateles belzebuth in the Andes,
and extending the distribution of this taxon for approxi-
mately 130 km from the locations of specimens collected
in 1920´s and 1950´s in the departments of Cundinamarca
and Meta, respectively (Fig. 2). Also, these records expand
the altitudinal range for white-bellied spider monkeys from
1,300 m. a.s.l. (Hernandez-Camacho & Cooper, 1976) to
1,800 m. a.s.l. is geographical and altitudinal expansion
poses an additional question about the continuity of these
recently recorded populations with those in northwestern
Amazonia in Colombia, and adds to the complexity of its
current geographical distribution.
e biogeography of spider monkeys (Ateles spp.) has
been largely explained by the separation of major clades
due to riverine and mountain barriers (Collins & Dubach
2000; Morales-Jiménez et al. 2015). Nonetheless, these
northern populations of white-bellied spider monkeys
are currently located about 200 km south of records of
brown spider monkeys (Ateles hybridus) with no evident
geographical barriers between them. In the 1960´s there
is a record of Ateles hybridus in Cucuta, Norte de Santand-
er department, Colombia (see Deer, in press), and cur-
rently there is a population of brown spider monkeys at
Caparó, in Venezuela (Aliaga-Samanez et al., 2017) (Fig
3). us, populations of both taxa might be currently
in a process of range expansion (and have not reached
a contact zone), or might have occupied these areas and
have been locally extirpated elsewhere except for limited
current residual populations.
e status of white-bellied spider monkeys in the north-
ern Andes of Colombia is largely unknown and eorts
should be made to better understand the size of this high-
land population, in order to plan successful conservation
strategies. Mountain forests in Colombian Andes have
been heavily degraded during the last centuries (Etter and
van Wyngaarden, 2000), and the broader region where
white bellied spider monkeys have been recently record-
ed in the Andes has high levels of forest fragmentation.
us, understanding how common or rare is the presence
of Ateles belzebuth in these forest fragments might drive
conservation strategies focused on a few fragments or,
in restoring connectivity between isolated populations,
amongst other conservation actions. Studies on the ecol-
ogy and behavior of Ateles belzebuth in highland forests
are urgently needed to better understand the ecological
exibility of these endangered primates, as most of the
information on the species has been recorded on popu-
lations in lowland Amazonian forests (Stevenson et al.,
2000; Link et al., 2018).
Figure 3. Records of Ateles belzebuth (1, 2, 5, 6) and A. hybridus
(3,4) in Colombia and Venezuela. Circles (5, 6) show this study
data at Casanare and Boyacá; Triangles show literature reports of
nearest populations of A. hybridus and, Squares show literature re-
ports of A. belzebuth. 1. Mambita, Cundinamarca, [N 4°45.08112´,
W-73°19.6705´], 1923, AMNH76784, AMNH62815. 2. Vil-
lavicencio, Acacías, Meta, [N3°59.2285´, W-73°45.6075´], 1956,
FMNH85816. 3. Caparó, Venezuela, [N7° 25.3´, W-70°59.7166´],
2014, direct observation, 4. Cúcuta, rio del Oro,[N7° 53.4963´,
W-72° 30.102´], 1965, ICN1033.
In conclusion, the record of a new population of white-
bellied spider monkeys living in the highland forests of the
northern Andes of Colombia creates the need to prioritize
urgent conservation actions to study and better understand
spider monkey evolutionary history and behavioral ex-
ibility, that allows them to adapt to highland ecosystems.
Ateles may well represent some of the most important seed
dispersers (see Link & Di Fiore, 2006; Dew et al., 2008)
for these mountain forests, and may be playing a crucial
role in the maintenance of the structure and composition
of these threatened ecosystems (Link & di Fiore, 2006).
Finally, given the high vulnerability of spider monkeys to
anthropogenic pressure, spider monkeys can be used as
agship species; focusing conservation eorts on their wild
population can drive indirect conservation of a large bio-
diverse ecosystem in the global biodiversity Hotspot of the
Northern Andes in the Neotropics.
Neotropical Primates 25(1), December 2019 51
Appendix. Visual records of Ateles belzebuth at Paya, Boyacá, January to September 2019.
Date Coordinates Altitude (m) Group size
21/01/2019 N5° 36.262’ W-72° 20.907’ 1425 3
22/01/2019 N5° 36.373’ W-72° 20.998’ 1610 3
23/01/2019 N5° 36.282’ W-72° 20.940’ 1361 7
24/01/2019 N5° 36.232’ W-72° 20.910’ 1329 3
25/01/2019 N5° 36.228’ W-72° 20.853’ 1355 4
26/01/2019 N5° 36.268’ W-72° 21.050’ 1460 6
28/01/2019 N5° 35.635’ W-72° 20.962’ 1218 5
29/01/2019 N5° 36.113’ W-72° 20.897’ 1311 3
31/01/2019 N5° 36.295’ W-72° 20.908’ 1466 2
1/02/2019 N5° 36.297’ W -72° 20.898’ 1460 1
29/04/19 N5° 36.606’ W -72°21’036’ 1836 4
29/04/19 N5° 36’606’ W -72°21’029’ 1833 1
29/04/19 N5° 36’560’ W -72°21’016’ 1794 1
14/05/19 N5° 36.413’ W -72° 20.882’ 1547 3
17/05/19 N5° 36.005’ W -72° 20.624’ 1576 3
17/05/19 N5° 36.005’ W -72° 20.624’ 1576 3
17/05/19 N5° 36.005’ W -72° 20.624’ 1576 3
17/05/19 N5° 36.005’ W -72° 20.624’ 1576 3
21/05/19 N5° 35.780’ W -72° 21.297’ 1453 2
21/05/19 N5° 35.969’ W -72° 21.336’ 1608 2
24/05/19 N5° 36.335’ W -72° 21.180’ 1734 4
28/05/19 N5° 36.049’ W -72° 21.277’ 1593 1
28/05/19 N5° 36.190’ W -72° 21.220’ 1602 3
6/06/19 N5° 36.325’ W -72° 21.180’ 1690 1
15/06/19 N5° 35.379’ W -72° 21.560’ 1635 4
26/06/19 N5° 35.313’ W -72° 21.574’ 1611 1
2/07/19 N5° 36.203’ W -72° 21.197’ 1658 6
16/07/19 N5°59174° W -72°.35986° 1388 2
17/07/19 N5° 35.903’ W -72° 21.491’ 1690 8
17/07/19 N5° 35.804’ W -72° 21.584’ 1740 1
17/07/19 N5° 35.806’ W -72° 21.596’ 1759 1
23/07/19 N5° 35.338’ W -72° 21.648’ 1508 2
30/07/19 N5° 35.885’ W -72° 21.466’ 1668 8
30/07/19 N5° 35.867’ W -72° 21.502’ 1693 9
31/07/19 N5° 35.867’ W -72° 21.490’ 1687 3
31/07/19 N5° 35.905’ W -72° 21.474’ 1687 9
4/08/19 N5° 35.866’ W -72° 21.503’ 1694 7
26/08/19 N5° 35.831’ W -72° 21.029’ 1275 1
26/08/19 N5° 36.061’ W -72° 21.203’ 1548 1
26/08/19 N5° 35.902’ W -72° 21.469’ 1684 4
29/08/19 N5° 35.669’ W -72° 21.567’ 1734 6
29/08/19 N5° 35.588’ W -72° 21.477’ 1641 3
Neotropical Primates 25(1), December 201952
Date Coordinates Altitude (m) Group size
30/08/19 N5° 35.480’ W -72° 21.521’ 1579 1
30/08/19 N5° 35.481’ W -72° 21.521’ 1579 5
30/08/19 N5° 35550’ W -72°21.582’ 1683 5
3/09/19 N5° 35.906’ W -72° 21.489’ 1699 1
3/09/19 N5° 35.767’ W -72° 21.024’ 1254 3
4/09/19 N5° 35.562’ W -72° 21.574’ 1723 7
5/09/19 N5° 35.528’ W -72° 21.562’ 1684 9
6/09/19 N5° 35.484’ W -72° 21.565’ 1670 9
6/09/19 N5° 35.734’ W -72° 21.555’ 1774 3
13/09/19 N5° 35.338’ W -72° 21.604’ 1617 6
13/09/19 N5° 35.690’ W -72° 21.564’ 1749 3
Acknowledgements
We are grateful to the families Hernández, Fernández, Cor-
redor-Cachay, and Cachay-Rodriguez for their hospitality
and for allowing us into their properties to carry out the
surveys; to Rubiel Fernández, Miguel Garcés, Beyer Cata-
ño, Próspero Cachay, Solis Cepeda and Rosario Cachay for
their assistance with the eld work; to all the community
from Guayabal de La Peña and La Unión for welcoming
us in their territory; and to the Asociación de Becarios de
Casanare (ABC) for the management of the project. We
also thank Hugo López-Arévalo and Pablo Stevenson for
their advice and Pedro Martinez for the maps. Equion En-
ergía Limited and ABC nanced this research.
References
Armenteras, D., Rodríguez, N., Retana, J. and Morales,
M. 2011. Understanding deforestation in montane and
lowland forests of the Colombian Andes. Reg Environ
Chang. 11(3): 693–705.
Aureli, F. and Schaner, C. 2008. Social interactions, social
relationships and the social system of spider monkeys. In:
Spider Monkeys: Behavior, Ecology, and Evolution of the
genus Ateles, Campbell, C. J. (ed.), pp. 236–265. Cam-
bridge University Press, New York.
Buckland, S. T., Anderson, D. R., Burnham, K. P. and
Laake, J. L. 1993 Distance Sampling: Estimating Abun-
dance of Biological Populations. Chapman and Hall,
London.
Collins, A. and Dubac, J. 2000. Biogeographic and eco-
logical forces responsible for speciation in Ateles. Int. J.
Primatol. 21: 421–444
Deer, T. R. 2003. Primates de Colombia. Conservación In-
ternacional, Bogotá D. C.
Dew, J. L. 2008. Spider monkeys as seed dispersers. In: Spi-
der Monkeys: Behavior, Ecology, and Evolution of the genus
Ateles, Campbell, C. J. (ed.), pp.155–182. Cambridge
University Press, New York.
Di Fiore, A., Link, A. and Dew, L. 2008. Diets of wild spi-
der monkeys. In: Spider Monkeys: Behavior, Ecology, and
Evolution of the genus Ateles, Campbell, C. J. (ed.), pp.
81–138. Cambridge University Press, New York.
Eisenberg, J. F. 1976. Communication Mechanisms and
Social Integration in the Black Spider Monkey, Ateles fus-
ciceps robustus, and Related Species. Smithson. Contrib.
Zool. 213: 1–108.
Etter, A. and van Wyngaarden, W. 2000. Patterns of land-
scape transformation in Colombia, with emphasis in the
Andean region. Ambio. 29(7): 432–439
Franzen, M. 2006. Evaluating the sustainability of hunt-
ing: a comparison of harvest proles across three Hua-
orani communities. Environ. Conserv. 33 (1): 36–45.
Hernández-Camacho, J. and Cooper, R. W. 1976. e
nonhuman primates of Colombia. In: R. W. orington,
Jr. and P. G. Heltne (eds.), Neotropical Primates: Field
Studies and Conservation, pp. 35–69. National Academy
of Sciences, Washington, D. C., USA.
Holdridge, L. R. 1979. Ecología basada en zonas de vida.
Instituto Interamericano de Ciencias Agrícolas, San José.
IGAC. 1999. Casanare, características geográficas. Instituto
Geográco Agustín Codazzi (IGAC), Bogotá D.C.
León, J. y Link, A. 2013. Repertorio vocal de los monos
araña café (Ateles hybridus). En: Primates Colombianos en
Peligro de Extinción, Deer, T. R., Stevenson, P. R., Bue-
no, M. L. y Guzmán-Caro, D. L. (eds.), pp. 281–293.
Asociación Primatológica Colombiana, Bogotá D. C.
Link, A., Palma, A. C., Velez, A. and de Luna, A.G. 2006.
Costs of twins in free-ranging white-bellied spider mon-
keys (Ateles belzebuth belzebuth) at Tinigua National
Park, Colombia. Primates. 47: 131–139.
Link, A. and Di Fiore, A. 2006. Seed dispersal by spider
monkeys and its importance in the maintenance of neo-
tropical rain-forest diversity. J. Trop. Ecol. 22: 235–246.
Link, A., Milich, K. and Di Fiore, A. 2018. Demography
and life history of a group of white-bellied spider mon-
keys (Ateles belzebuth) in western Amazonia. Am. J. Pri-
matol. e22899
Neotropical Primates 25(1), December 2019 53
Link, A., Muniz, C., Rylands, A. B., Mourthé, Í., Cornejo,
F. M., Urbani, B., Mittermeier, R. A., Stevenson, P. R.,
Palacios, E., Boubli, J., Shanee, S., de la Torre, S. and
Moscoso, P.2019.Ateles belzebuth.e IUCN Red List
of reatened Species2019: e.T2276A17928557.http://
dx.doi.org/10.2305/IUCN.UK.20192.RLTS.
T2276A17928557.en. Downloaded on 22 September
2019.
Michalski, F. and Peres, C. A. 2005. Anthropogenic deter-
minants of primate and carnivore local extinctions in a
fragmented forest landscape of southern Amazonia. Biol.
Conserv. 124: 383–396.
Morales-Jiménez, A. L., Disotell, T., Di Fiore, A. 2015.
Revisiting the phylogenetic relationships, biogeography,
and taxonomy of spider monkeys (genus Ateles) in light
of new molecular data.Mol. Phylogen. Evol.82: 467–483.
Peres, C. A. 1993. Structure and spatial organization of an
Amazonian terra firme forest primate community. J. Trop.
Ecol. 9: 259–276.
Shimooka, Y., Campbell, C.J., Di Fiore, A., Felton, A. M.,
Izawa, K., Link, A., Nishimura, A., Ramos-Fernández,
G. y Wallace, R. B. 2008. Demography and group com-
position of Ateles. In: Spider Monkeys: Behavior, Ecology,
and Evolution of the genus Ateles, Campbell, C. J. (ed.),
pp.329–348. Cambridge University Press, New York.
Stevenson, P. R., Quiñones, M. J. and Ahumada, J. A.
2000. Inuence of Fruit Availability on Ecological Over-
lap among Four Neotropical Primates at Tinigua Nation-
al Park, Colombia. Biotropica. 32(3): 533–544.
Symington, M. M. 1990. Fission-fusion social organiza-
tion in Ateles and Pan. Int. J. Primatol. 11(1): 47–61.
PRIMER REGISTRO DE PITHECIA MILLERI
ALLEN, 1914 EN LA BAJA BOTA CAUCANA,
CORREGIMIENTO DE MIRAFLOR, MUNICIPIO
DE PIAMONTE, CAUCA
Laura Suárez
Hugo Mantilla-Meluk
Introducción
Los monos voladores o sakis, comprenden las especies de
menor tamaño entre los Pitheciines y son considerados
habitantes típicos de los bosques de varzea, igapó y tierra
rme en la Amazonía (Rylands, 1988; Rylands y Mitter-
meier, 2009). Pithecia milleri, descrita como una especie
separada de P. monachus en 1914 por Allen, fue remitida a
subespecie de P. monachus por Hershkovitz (1987), crite-
rio aceptado para las poblaciones de Colombia por Deer
(2004); siendo elevada de nuevo al estatus especíco por
Marsh (2014). Es poca la información que en la actuali-
dad existe sobre esta especie, considerada a la fecha en la
categoría Datos Decientes (DD) por la Unión Internacio-
nal para la Conservación de la Naturaleza (Marsh, 2015);
dicho desconocimiento, sumado a la degradación por de-
forestación de los ambientes que ocupa en la porción de
su distribución en Colombia, son las principales amenazas
para este taxón. Según García et al., (2017) Pithecia milleri
se distribuye en Colombia entre los 200 y 1,070 m.s.n.m.,
sobre el anco oriental de la Cordillera Oriental, en el Pi-
edemonte Andino-Amazónico, con límite norte en San
Vicente del Caguán, en el departamento del Caquetá, cu-
briendo las cuencas del río Caguán hasta su desembocadura
en el río Caquetá; y al sur, a través del interuvio de los ríos
Caquetá y Putumayo, hasta el límite de los departamentos
del Putumayo y Amazonas en la población de Guaquirá.
A pesar de que la presencia de la especie fue sugerida para
la Bota Caucana por García et al., (2017), a la fecha no se
cuenta con registros de P. milleri para el departamento del
Cauca.
Observaciones y discusión
En el marco del desarrollo de las actividades de campo del
proyecto Densidad Poblacional y Estructura de grupo de
Plecturocebus caquetensis en la Baja Bota Caucana, bajo -
nanciación de la Primate Society of Great Britain (PSGB),
se reportan los primeros registros de mico volador (P. mil-
leri) para el municipio de Piamonte, departamento del
Cauca, en la Baja Bota Caucana (Fig. 1), correspondientes
a tres avistamientos independientes: i) observación de
un individuo solitario, el día 17 de septiembre de 2018
a las 7:07 horas, en el fragmento de bosque La Floresta,
ubicado en el Resguardo Indígena Inga “La Floresta-
La Española” corregimiento de Miraor, municipio de
Piamonte, en un bosque de tierra rme de Piedemonte
a 302 m.s.n.m. (dosel denso: 15 –20 m) (1° 1’22.38”N,
76°26’29.77”O).
El individuo observado se encontraba posado sobre un
árbol de Yarumo negro (Cecropia angustifolia) de 15 m.
Al observar al investigador realizó despliegues agonísticos,
emitiendo gruñidos y balanceando su cuerpo de un lado
al otro en repetidas ocasiones, para luego huir rápidam-
ente saltando en el estrato medio del bosque. De acu-
erdo al patrón de distribución y coloración del pelaje de
la especie, y las características registradas para este indi-
viduo, consideramos que el individuo observado era una
hembra; presentaba extremidades y cola con pelos largos
negruzcos con puntas blanquecinas y manos con pelos
blanquecinos, en contraste con lo reportado por Allen
(1914) para los machos: puntas de los pelos en extremi-
dades y cola de color amarillento pálido, y de color blanco
amarillento en sus manos, ii) observación de un individuo
solitario el día 26 de septiembre de 2018 a las 7:44 horas,
en el fragmento de bosque La Floresta, 294 m.s.n.m. (1°
1’23.66”N, 76°26’31.40”O). Este individuo fue obser-
vado posado sobre un árbol (no identicado) de 12 m;
al observar al investigador emite gruñidos y emprende la
huida rápidamente. Quizá, este individuo sea el mismo
reportado para el primer avistamiento ya que se encon-
traba a unos 60m de distancia del primer punto de ob-
servación reportado y era una hembra, iii) observación de
dos parejas de sakis, realizadas el día 8 de octubre de 2018
Neotropical Primates 25(1), December 201954
a las 13:30 horas en un corredor de bosque que conecta el
fragmento de bosque La Floresta y un segundo fragmento
sin nombre (1° 0’47.41”N, 76°26’11.80”O). Las parejas
de P. milleri se avistaron posadas sobre árboles de aproxi-
madamente 20m de altura, distanciados 30m entre sí. El
reporte corresponde a una comunicación del señor Nixon
Palacios, dueño del predio y habitante de la localidad de
Miraor por más de 40 años. En sus palabras describe los
monos como “una especie rara, nunca vista en la zona, de
pelaje denso, negruzco y con canas”.
Estos registros en conjunto conrman la distribución
de P. milleri para el área de la Bota Caucana, Departa-
mento del Cauca, sugerida por García et al. (2017). Se
llama la atención sobre la necesidad de realizar expedi-
ciones e investigaciones en los límites de su distribución,
pues la carencia de información, sumada a la creciente
deforestación, exigen la formulación pronta de estrategias
para la conservación de la especie.
deseo de contribuir y apoyar iniciativas de conservación en
la Baja Bota Caucana, permitiendo el acceso a sus bosques.
Referencias
Allen, J. A. 1914. New South American monkeys. Bull.
Am. Mus. Nat. His. 33: 647–655.
Deer, T. R. 2004. Primates of Colombia. Conservation In-
ternational, Washington DC.
García, V. J., Paéz, A., Palacios, E. 2017. Aportes al con-
ocimiento de la distribución del mico Volador Pithecia
milleri (Allen, 1914) en el occidente Amazónico colom-
biano. Neotrop. Primates 23(2): 59–66.
Hershkovitz, P. 1987. e taxonomy of South American
sakis, genus Pithecia (Cebidae, Platyrrhini): a preliminary
report and critical review with the description of a new
species and a new subspecies. Am. J. Primatol. 12: 387–46.
Marsh, L. K. 2014. A Taxonomic revision of the Saki mon-
keys, Pithecia Desmarest, 1804. Neotrop. Primates. 21(1):
1–163.
Marsh, L. K. and Veiga, L. M. 2015. Pithecia milleri. e
IUCN Red List of reatened Species 2015. Website:
http://dx.doi.org/10.2305/IUCN.UK.2015-1. RLTS.
T17407A70609259. Consultado el 22 de noviembre de
2018.
Rylands, A. B. and Keuroghlian, A. 1988. Primate popula-
tions in continuous forest and forest fragments in central
Amazonia, Acta Amaz. 18: 291–307
Rylands, A. B. and Mittermeier, R. A. 2009. e diver-
sity of the New World primates (Platyrrhini). In: South
American Primates: Comparative Perspectives in the
Study of Behavior, Ecology, and Conservation. In: P. A.
Garber, A. Estrada, J. C. Bicca-Marques, E. W. Heymann
and K. B. Strier (eds.), pp.23–54. Springer, New York.
EVIDENCE OF OPOSSUM (DIDELPHIS SP.) PRE-
DATION BY WHITE-FRONTED CAPUCHINS
(CEBUS YURACUS)
IN THE COPALLÍN PRIVATE
CONSERVATION AREA, AMAZONAS, PERÚ
Karen Pedersen
Sam Shanee
Christian Miguel Olivera Tarifeño
Introduction
Capuchin monkeys (Genera Cebus and Sapajus) are om-
nivorous and known to opportunistically prey on small
vertebrates including frogs, lizards, adult birds, eggs, nest-
lings, bats, squirrels, coatis and mice (Izawa, 1978; Fedigan
1990; Milano and Monteiro-Filho, 2009). However, there
are a few reports of Capuchins feeding on larger mamma-
lian preys. e white-faced capuchins (Cebus capucinus)
have been observed feeding on coati pups (Newcomer and
De Farcy, 1985; Fedingan, 1990; Perry and Rose, 1994),
Ka’apor capuchins (Cebus kaapori) have been observed feed-
ing on a young titi monkey (Sampaio and Ferrari, 2005),
Figura 1. Primer registro de Pithecia milleri (estrella negra), para
la Baja Bota Caucana (área en gris), y registros de la especie so-
portados por datos museológicos (puntos grises) y observaciones
en campo (puntos en blanco). Modicado de García et al., 2017.
Laura Suárez Ramírez, Programa de Biología, Facultad de
Ciencias Básicas y Tecnológicas, Universidad del Quindío,
Armenia y Hugo Mantilla Meluk, Centro de Estudios de
Alta Montaña de la Universidad del Quindío, Armenia.
Agradecimientos
A la Primate Society of Great Britain (PSGB) por el apoyo
nanciero. A Conservación Internacional Colombia y su
Alianza Naturamazonas, por su apoyo y alojamiento en el
Centro de Capacitación Agro-Forestal Guayuyaco. A los
biólogos Javier García Villalba y Erwin Palacios por sus
aportes acerca de la especie. A Catherine Meneses por sus
recomendaciones en la elaboración del mapa. Agradecemos
en especial al Resguardo Indígena Inga de La Floresta- La Es-
pañola, a Nixon Palacios, Alonso Cuellar y su esposa, por su
Neotropical Primates 25(1), December 2019 55
and black striped capuchins (Sapajus libidinosus) have been
observed preying on snakes (Falótico et al., 2018). Milano
and Monteiro-Filho (2009) reported Azaras’s capuchins (Sa-
pajus cay) chasing a mammal the size of an opossum, though
conclusive identication was impossible before the monkey
and prey animal were lost from sight. e black-horned ca-
puchin (Sapajus nigritus) was observed attempting to con-
sume a brown-eared woolly opossum (Caluromys lanatus)
that had been run over; this occurred in Mata Santa Tereza,
Brazil, a semi urban area where capuchins are accustomed
to receiving food on the ground from local people which
may alter their behavior (Palmeira and Pianca, 2012). Here
we present an observation of a white-fronted capuchin (Ce-
bus yuracus) preying on an opossum in the Copallín Private
Conservation Area in Amazonas, northern Peru.
Methods
We placed four camera stations of three camera traps (Bush-
nell Aggressor No Glow Trail Cameras) each on the Las
Higueras trail in the Copallín Private Conservation Area (S
05°37’16”, W 78°16’46”), bordering the Santuario Nacio-
nal Cordillera de Colán (Fig. 1). Each camera was set fac-
ing animal trails at a height of ~ 40 cm above the ground.
Cameras were congured to take one photo followed by 30
seconds of video. We set the cameras on the 13th and 14th
of March, 2018 and they were taken down on the 14th and
15th of May, 2018. Once collected, the photos and videos
from each trap were transferred to a hard drive for analy-
ses and storage (Sanderson and Harris, 2013). e camera
which recorded the predation event was set at an altitude
of 2,413 m above sea level and recorded for 1,466 hours
(62 camera days).
Results and discussion
On 2nd of April 2018 at 16:32, the camera of inter-
est captured one photo of a capuchin (Cebus yuracus) on
the ground and then 30 seconds of video of the capuchin
clutching a dead Didelphis sp. to its underbelly and disap-
pearing onto an animal trail (Fig. 2). is is the rst and
only time we have seen monkeys on our terrestrial camera
traps despite sampling for almost a year.
ough vertebrate predation is well documented in Old
World primates (Hausfater, 1976; Busse, 1977; Morris
and Goodall, 1977; McGrew et al., 1978; Anderson, et
al., 1983; McGrew 1983; Takahata et al.,1984; Boesch
and Boesch, 1989; Wrangham and Riss, 1990; Alp,
1993; Basabose, and Yamagiwa, 1997; Wrangham, 1999;
Surbeck, and Hohmann, 2008; Fowler and Hohmann,
2010), it has been much less studied in the New World
primates (Izawa, K. 1978; Newcomer and De Farcy 1985;
Perry and Rose, 1994; Sampaio and Ferrari 2005; Milano
and Monteiro-Filho, 2009; Sanderson and Harris 2013;
Falótico et al., 2018). Capuchins are well known to hunt
but this is the rst record we are aware of that documents
mammal predation in Cebus yuracus, and the rst con-
rmed report of a capuchin predating on an opossum.
Additionally, there are very few records of capuchins prey-
ing on opossums, in the literature. e one observation
we were able to nd was unconrmed but probable (Mi-
lano and Monteiro-Filho, 2009) and one attempt (Pal-
meira and Pianca, 2012). While there are few in-depth
studies of Neotropical opossums (Didelphis), the Virginia
opossum (Didelphis virginiana), the northern and central
American species, has been extensively studied and found
to be surprisingly resistant to rabies and ticks, however
they are great sources for a number of other diseases and
parasites, and therefore may be risky to consume (Tardieu
et al., 2017).
We do not know how the opossum died. It could have been
killed by the capuchin in a tree and fallen to the ground,
or have already been on the ground, and dead, nearly dead
or killed there. e capuchin did leave the relative safety
of the canopy to the ground to retrieve its body, or kill the
opossum, indicating that it is a high enough quality food
to be worth the risk of coming down from the trees to the
forest oor.
Acknowledgements
We would like to thank Marlon Yordano Hoyos Cerna of
the Santuario Nacional Cordillera de Colán and Gabriel
Garcia Mendoza Nature and Culture International, for
their help with identication, the hardworking park guards
from both the Copallín Private Conservation Area, and
Santuario Nacional Cordillera de Colán, for help in identi-
cation, and, the Peace Corps USAID for nancing grant
number SP-16-527-009.
Figure 1. Location of our eld site in the Andes of Northern Perú,
department of Amazonas, districts of Copallína and Cajaruro.
e black star indicates the location of the camera trap which
captured the image of the capuchin and the opossum.
Neotropical Primates 25(1), December 201956
Karen Pedersen, Copallín Private Conservation Area,
Peace Corps, # 321 Jr. Garcilazo de la Vega Copallín, Ama-
zonas, Perú, E-mail: <pedersen.6@wright.edu>, Sam Sha-
nee, Asociación Neotropical Primate Conservation Perú,
#1187 Av. Belaunde, Yambrasbamba, Amazonas, Perú,
and, Christian Miguel Olivera Tarifeño, Santuario Na-
cional Cordillera de Colán Jr. Ciro Alegría # 788 Bagua
Grande, Amazonas, Perú.
References
Alp, R., 1993. Meat eating and ant dipping by wild chim-
panzees in Sierra Leone. Primates 34: 463–468.
Anderson, J. R., Williamson, E. A., and Carter, J. 1983.
Chimpanzees of Sapo Forest, Liberia: density, nests, tools
and meat-eating.Primates24: 594–601.
Basabose, K., and Yamagiwa, J. 1997. Predation on mam-
mals by chimpanzees in the montane forest of Kahuzi,
Zaire.Primates38: 45–55.
Boubli, J. P., Rylands, A. B., Farias, I. P., Alfaro, M. E., and
Alfaro, J. L. 2012. Cebus Phylogenetic Relationships: A
Preliminary Reassessment of the Diversity of the Untuft-
ed Capuchin Monkeys. Am. J. Primatol. 74: 381–393.
Busse, C. D. 1977. Chimpanzee predation as a possible
factor in the evolution of red colobus monkey social or-
ganization. Evolution 31: 907–911.
Boesch, C., and Boesch, H. 1989. Hunting behavior of
wild chimpanzees in the Tai National Park.Am. J. Phys.
Anthropol.78: 547–573.
Falótico, T., Verderane, M. P., Mendonça-Furtado, O., Sp-
agnoletti, N., Ottoni, E. B., Visalberghi, E., and Izar, P.
2018. Food or threat? Wild capuchin monkeys (Sapajus
libidinosus) as both predators and prey of snakes. Primates
59: 99–106.
Fedigan, L. M. 1990. Vertebrate predation in Cebus capuci-
nus: meat eating in a Neotropical monkey. Folia Primatol.
54: 196–205.
Fowler, A., and Hohmann, G. 2010. Cannibalism in wild
bonobos (Pan paniscus) at Lui Kotale. Am. J. Prima-
tol.72: 509–514.
Hausfater, G. 1976. Predatory behavior of yellow ba-
boons.Behaviour56: 44–67.
Izawa, K. 1978. Frog-eating behavior of wild black-capped
capuchin (Cebus apella). Primates 19: 633–642.
Keesing, F., Brunner, J., Duerr, S., Killilea, M., LoGiudice,
K., Schmidt, K., Young H. and Ostfeld, R. S. 2009. Hosts
as ecological traps for the vector of Lyme disease.Proc
R. Soc. Lond. B. Biol. Sci.276: 3911–3919.
McGrew, W. C. Tutin, C. E. G., Baldwin, P. J., Sharman
M. J., and Whiten, A. 1978. Primates preying upon ver-
tebrates: new records from West Africa (Pan troglodytes
verus, Papio papio, Cercopithecus sabaeus). Carnivore 1:
41–45.
McGrew, W. C. 1983. Animal foods in the diets of wild
chimpanzees (Pan troglodytes): Why cross-cultural varia-
tion?J. Ethol.1: 46–61.
Figure 2. Video stills from the video of the capuchin clutching a dead Didelphis sp. to its
underbelly. e opossum’s feet, and hairless tail as well as part of its body can be seen. e
arrows point to the opossum.
Neotropical Primates 25(1), December 2019 57
Milano, M. Z., and Monteiro-Filho, E. L. A. 2009. Pre-
dation on small mammals by capuchin monkeys, Cebus
cay.Neotrop. Primates16: 78–80.
Morris, K., and Goodall, J. 1977. Competition for meat
between chimpanzees and baboons of the Gombe Na-
tional Park. Folia Primatol. 28: 109–121.
Newcomer, M. W., and De Farcy, D. D. 1985. White-
faced capuchin (Cebus capucinus) predation on a nestling
coati (Nasua narica).J. Mammal.66: 185–186.
Palmeira, F. B. L. and Pianca, C. C., 2012. Predation At-
tempt on a Roadkilled Brown-Eared Woolly Opossum
(Caluromys lanatus) by a Black-Horned Capuchin (Sapa-
jus nigritus).Neotrop. Primates19:36–38.
Perry, S., and Rose, L. 1994. Begging and transfer of coati
meat by white-faced capuchin monkeys, Cebus capucinus.
Primates 35: 409–415.
Sanderson, J., and Harris, G. 2013. Automatic data orga-
nization, storage, and analysis of camera trap pictures.J.
Ind. Nat. Hist.1: 11–19.
Sampaio, D. T., and Ferrari, S. F. 2005. Predation of an in-
fant titi monkey (Callicebus moloch) by a tufted capuchin
(Cebus apella).Folia Primatol.76: 113–115.
Surbeck, M., and Hohmann, G. 2008. Primate hunting
by bonobos at LuiKotale, Salonga National Park.Curr.
Biol.18: 906–907.
Takahata, Y., Hasegawa, T., and Nishida, T. 1984. Chim-
panzee predation in the Mahale Mountains from August
1979 to May 1982.Int. J. Primatol.5: 213–233.
Tardieu, L., Adogwa, A. O., and Garcia, G. W. 2017. Di-
delphis species, neo-tropical animals with the potential
for intensive production: Part 1 Review of taxonomy,
natural history, general biology, animal behavior, and nu-
trition.Trop. Agric.94: 157–174.
Wrangham, R. W., and Riss, E. V. Z. B. 1990. Rates of
predation on mammals by Gombe chimpanzees, 1972–
1975.Primates31: 157–-170.
Wrangham, R. W. 1999. Evolution of coalitionary killing.
Am. J. Phys. Anthropol. 110: 1–30.
AMPLIACIÓN DEL ÁREA DE DISTRIBUCIÓN
DEL MONO MAICERO CACHÓN SAPAJUS
APELLA: NUEVO REGISTRO EN EL PARQUE
NACIONAL NATURAL LAS HERMOSASGVC,
TOLIMA, COLOMBIA
Pablo Paya
Jesús-A Sánchez-C
Carolina Guzmán-V
Germán Rodríguez-P
Néstor Roncancio-D
Introducción
Producto de los cambios sociopolíticos que se han dado
en Colombia en los últimos años, se ha podido ingresar a
zonas que incluyen porciones del sistema de áreas protegi-
das, donde antes no era posible, y avanzar con la gestión
de generar información primaria, e implementar sus planes
de monitoreo y portafolios de investigación. Esto ha per-
mitido explorar cientícamente áreas que estuvieron veta-
das por décadas y conocer más detalladamente aspectos de
la ecología de algunas especies, e incluso descubrir algu-
nas nuevas para la ciencia (Vieira-U y Karremans, 2018;
Vieira-U y Moreno, 2018), conocimiento clave para revisar
las prioridades de conservación y orientar el manejo ambi-
ental de los territorios (Nichols y Williams, 2006; Pullin y
Knight, 2005).
En el marco de la implementación del plan de monitoreo
del oso andino (Tremarctos ornatus) y la danta de páramo
(Tapirus pinchaque), y obedeciendo al diseño de muestreo
denido para ellos, el equipo del PNN Las Hermosas – Glo-
ria Valencia de Castaño ingresó a esta área protegida por el
sector del departamento del Tolima, municipio de Chapar-
ral, para hacer recorridos en donde históricamente el acceso
había estado restringido.
Observación
El 15 de mayo de 2018 se registraron cuatro individuos
de Mono maicero cachón (Sapajus apella, Asociación Pri-
matológica Colombiana, 2016) (Sinónimos: Cebus apella
en Deer, 2010; Sapajus macrocephalus en De la Torre
et al., 2018), en el límite del área protegida, en el muni-
cipio de Chaparral, departamento de Tolima (3.75975N,
-75.68392W) a 2,370 metros de elevación (Fig. 1).
Figura 1. Área de estudio y sitio de registro de Sapajus apella en el
PNN Las Hermosas – Gloria Valencia de Castaño
Neotropical Primates 25(1), December 201958
Discusión
Sapajus apella está categorizada como especie de preocu-
pación menor (LC) pero se considera que su población
está disminuyendo (De la Torre, 2018), y con la tenden-
cia actual de deforestación podría perder cerca del 21 %
de su hábitat a 2030 (Carretero-P y Stevenson, 2018). En
Colombia la especie tenía una extensión de ocurrencia es-
timada de aproximadamente 521,362 km2, que abarcaba
toda la Amazonía y parte de la Orinoquia colombiana,
excepto en algunas zonas al oriente, en el departamento
del Vichada, penetrando también en el alto valle del río
Magdalena hasta el departamento de Huila (Deer, 2010;
Carretero-P y Stevenson, 2018). Su distribución dentro
de áreas protegidas representa 21.9 %, correspondiendo el
17.3 % a áreas del Sistema de Parques Nacionales Natura-
les y 4.6 % a otras guras de protección. Las coberturas
vegetales dentro de su área de distribución estimada son
bosque denso en un 78 %, pastos limpios en un 7.61 % y
vegetación secundaria o en transición en un 2.32 % (Car-
retero-P y Stevenson, 2018). Con este registro se amplía la
distribución de la especie cerca de 100 kilómetros al norte
sobre la cuenca del río Magdalena, más allá de áreas de
bosque seco hoy en situación de alta reducción y fragmen-
tación (IDEAM, 2012). Es probable que, la población en
el PNN Las Hermosas-Gloría Valencia de Castaño (GVC)
sea una población aislada en un hábitat marginal, dado que
en general los primates Neotropicales tienden a preferir zo-
nas bajas más cálidas (Deer, 2010).
Sapajus apella es tal vez la especie de primate con la mayor
área de distribución en el país y la tercera con más estu-
dios documentados. A pesar de ello, aún hay vacíos de
información en aspectos tan elementales como su distri-
bución (Guzmán-Caro et al., 2018), situación debida en
parte probablemente a la dicultad de tener un muestreo
representativo dada la extensión de ocurrencia de la espe-
cie. Este registro reeja que sigue siendo necesario obtener
conocimiento adicional clave para planear, implementar y
monitorear la gestión para la conservación de los primates
en Colombia (Guzmán-Caro et al., 2018) y en particular
de las áreas protegidas, que permitan hacer el manejo alin-
eado a un proceso de toma estructurada de decisiones (Pos-
singham et al., 2001).
Agradecimientos
Los autores agradecen a todo el equipo del Parque Nacio-
nal Natural Las Hermosas – GVC quienes acompañaron
las labores de campo en el marco de las cuales se obtuvo
este registro. Igualmente, a Isagen por el apoyo nanciero
y la articulación técnica con Parques Nacionales Naturales,
que el marco de las alianzas público privadas, permitió la
implementación del programa de monitoreo del PNN Las
Hermosas-GVC.
Pablo Paya, Jesús-A Sánchez-C., Carolina Guzmán-
V, Germán Rodríguez-P, Parque Nacional Natural Las
Hermosas-Gloría Valencia de Castaño, Parques Nacionales
Naturales de Colombia y Néstor Roncancio-D, Dirección
Territorial Andes Occidentales, Parques Nacionales Natu-
rales de Colombia.
Referencias
Asociación Primatológica Colombiana. 2016. Lista de pri-
mates colombianos de la Asociación Primatológica Co-
lombiana. www.asoprimatologicacolombiana.org. Con-
sultado el 23 de diciembre de 2018.
Carretero-P, X. y Stevenson, P. 2018. Modelo de distri-
bución de Sapajus apella ID PRI–729. Laboratorio de
Biogeografía Aplicada. Instituto Alexander von Hum-
boldt. http://biomodelos.humboldt.org.co/species/
visor?species_id=932.
De la Torre, S., Boubli, J., Calouro, A. M., Heymann, E.
W., Lynch Alfaro, J., Martins, A. B., Mollinedo, J., Mos-
coso, P., Ravetta, A., Shanee, S. y Urbani, B. 2018.Sapa-
jus macrocephalus.
Guzmán-Caro, D. C., Vargas, S. A., Cárdenas, S., Castro,
J. D. y Stevenson P. R., 2018. Estudio y conservación de
primates en Colombia: avances, retos y el papel del Siste-
ma de Parques Nacionales Naturales. En: La primatología
en Latinoamérica 2 – A primatologia na America Latina
2. Tomo I Argentina-Colombia, B. Urbani, Kowalewski
M., Cunha R., De la Torre S. y L. Cortés-Ortiz (ed.),
pp. 283–294. Ediciones IVIC. Instituto Venezolano de
Investigaciones Cientícas (IVIC). Caracas, Venezuela.
[IDEAM] Instituto de Hidrología, Meteorología y Estudios
Ambientales. 2012. Leyenda Nacional de Coberturas de la
Tierra. Metodología CORINE Land Cover adaptada para
Colombia Escala 1:100.000. Bogotá, D. C., Colombia.
Nichols, J. D. y Williams, B. K. 2006. Monitoring for
Conservation. Trends Ecol. Evol. 21 (12): 668–673.
Possingham, H., Andelman, S. J., Noon, B. R., Trombu-
lak, S. y Pulliam, H. R. 2001. Making smart conservation
decisions. En: Conservation Biology: Research Priorities for
the Next Decade Soule M. E y G. H Orians (eds.), pp.
225–244. Island Press. Washington.
Pullin, A. S. y Knight, T. M. 2005. Assessing Conservation
Management’s Evidence Base: Survey of Management-
Plan Compilers in the United Kingdom y Australia.
Cons. Biol. 19: 1989–1996.
e IUCN Red List of reatened Species 2018:
e.T42696A70613972. http://dx.doi.org/10.2305/
IUCN.UK.2018-.RLTS.T42696A70613972.en. Des-
cargado el 22 de diciembre de 2018.
Vieira-U, S. y Karremans, A. P., 2018. La Specklinia
(Orquidaceae) con señuelo, una asombrosa nueva especie
de los Andes occidentales en Colombia. Orquideología 35
(2): 164–172
Vieira-U, S. y Moreno, J. S. 2018. Dos nuevas especies de
Lepanthes (Orquidiaceae: Pleurothallidinae) del Parque
Nacional Natural Tatamá en Colombia. Orquideología 35
(2):176–195
Neotropical Primates 25(1), December 2019 59
N
AN UPDATE ON THE COIBA HOWLER MONKEY,
COIBA ISLAND, PANAMÁ
After visiting Coiba Island in the Gulf of Chiriqui in 1999,
and in 2001 as eld assistant of Liliana Cortés-Ortiz in her
research on the phylogeny of the genus Alouatta, I found
that I had left a piece of myself there. Its mystique—a cruel
and fearsome island, a hideout for pirates, and later a peni-
tentiary—was augmented by my fascination of its beauty,
spectacular wildlife, and almost untouched forest, and it
was inspirational for my early career as a primatologist in
Panama. I felt I was Jim Hawkins, visiting the Treasure
Island of Robert Louis Stevenson. Leaving the island in
2001, I resolved to return someday as a Panamanian prima-
tologist, to study the population and ecology of the howler
monkeys and capuchins there. When I returned from Coiba
in 1999, I become interested in the Coiba howler monkey,
and reviewed the literature concerning the island and its
wildlife, visiting the libraries of University of Panama and
the Smithsonian Tropical Research Institute. I did my rst
publication about Coiba primates as “e kun-kun howler;
an endemic primate at extinction risk”, published in 2002
in a special edition about Coiba, “Coiba; an unpublished
world”, in the magazine Icaro of the National Association for
Conservation (ANCON). is article was read by Alvaro
Espinel, who showed it to Anthony Rylands, who helped
me with my rst scientic note in Neotropical Primates Jour-
nal, also in 2002. I briey described the geography and
biodiversity of Coiba and the smaller island of Jicarón, ex-
plaining that Coiba Island passed from the status of high
security prison (since 1919), incorporated a scientic station
(1996), and eventually become a national park (2005), also
recognized as Natural Heritage of Humanity, awarded by the
United Nations Educational, Scientic and Cultural Orga-
nization (UNESCO). Having achieved my Masters’ degree
in Primate Conservation from Oxford Brookes University,
UK (2008), I returned to Panama and created an NGO
called the Fundación Pro-Conservación de los Primates
Panameños (FCPP) (fcprimatespanama. org), and in 2010
began the rst primate population survey on Coiba Island.
In 2010 I invited Timothy Bearder as volunteer of my proj-
ect from Oxford BBC Radio Station and he made a lm,
a brief documentary, which he donated (https://www.you-
tube.com/watch?v=EvldLq-Tsn4). e project “Population
and Conservation Status of Azuero Peninsula and Coiba En-
demic Primates” was supported by the Ruord Foundation
(2011), and fullled my wish to study the Coiba howlers
and capuchins.
Recently, our eorts to conserve the primates and the bio-
logical diversity of Coiba have been greatly helped with the
formal creation of a eld station there, the “Estación Cientí-
ca Coiba AIP” created by Panama’s National Science and
Technology Secretary (SENACYT), with the FCPP being
part of the committee as associate investigators with the
project “Population ecology and genetic characterization
of two subspecies of primates endemic to Coiba Island and
the Azuero peninsula, Republic of Panama”, in collabora-
tion with Edgardo Díaz-Ferguson, an expert geneticist, and
Coiba AIP’s director (Panamá, SENACYT, 2019). New ob-
servations have been carried out in Coiba Island also for ar-
boreal and volant mammals using the Orion Camera System
(OCS) (Méndez-Carvajal, 2014). OCS consists of an array
of canopy camera traps at 12 m high level that will allow
us to understand activity patterns, interactions with arboreal
mammals, and habitat use. Other studies being led by FCPP
include research on bats and on the mammalian diversity in
the forest understory of Coiba. e capuchin monkeys of
Coiba have been studied to understand their dierent tech-
niques of survival. A recently published description of their
feeding behavior included descriptions of their use of tools
(Méndez-Carvajal and Valdes-Díaz, 2017).
As we know more about Coiba, however, its exuberance
and beauty are drawing increasing attention from tourists,
a trend which is potentially detrimental. By 2014, FCPP
advised the government the problem that cows and buf-
falos were causing negative impact in the understory and
increasing the hematophagous bats density. e Panama-
nian government nally achieved the removal of the feral
cows and bualos from the island. Being Coiba Island an
important point for shing and tourism, the activities has
subsequently increased, and is now being promoted by
the Panamanian Government. e building of an airport
on Coiba Island has been polemic, with local people from
Santa Catalina beach, Banco beach and Montijo Gulf,
arguing strongly against it. Tourism and development
are now putting the Coiba howler monkey at increasing
risk, resulting in an IUCN Red List assessment that places
it as Endangered. New research is availing Coiba with
more arguments for its conservation, with such as Carlos
Ramos from the University of Panama, and her student
Yohanny Pineda, studying population genetics aspects of
Coiba and Azuero monkeys, Pedro González (Biology
student) from the University of Panama (CRU-Coclé),
Karol Gutiérrez (Chemistry student) from the Autono-
mous University of Chiriqui (UNACHI), Margie Tejada
and Kimberly McIntosh (Parasitology students), Yohanni
Pineda (Genetics student) from the University of Panama
linked to FCPP-Coiba AIP (Del Moral, 2018), helping
to study and protect the Coiba howler monkeys, and its
habitat. An update of Coiba research “Long-term moni-
toring of the Coiba howler monkey Alouatta coibensis
coibensis and other mammals from Coiba Island, Coiba
National Park, Republic of Panama”, was presented re-
cently during the IV Ruord Small Grant Conference
South America Science for the Conservation of the East-
ern Tropical Pacic Region, on January 21 to 26, 2019, in
the Galapagos Islands, Ecuador. We continue monitoring
and studying Coiba for the conservation of its biodiver-
sity, and now endangered howler monkeys.
Neotropical Primates 25(1), December 201960
Pedro G. Méndez-Carvajal, Fundación Pro-Conservación
de los Primates Panameños (FCPP) (FCPP), 0816-05855,
Panama. mendezp@fcprimatespanama.org. Professor, De-
partment of Physiology and Animal Behavior, Biology
School, University of Panama, and Associate Investigator
of the Coiba Island Scientic Station (Coiba AIP).
References
Cortés-Ortiz, L., Bermingham, E., Rico, C., Rodriguez-Lu-
na, E., Sampaio, I. and Ruiz-Garcia, M. 2003. Molecular
systematics and biogeography of the Neotropical monkey
genus, Alouatta. Mol. Phylogenet. Evol. 26: 64–81.
Del Morral, T. 2018. Las riquezas naturales de Coiba. Ima-
gina 8: 40-41.
Froehlich J.W. and Froehlich P.H. 1986. Dermatoglyphics
and subspecic systematics of mantled howler monkeys
(Alouatta palliata). In: Current Perspectives in Primate Bi-
ology, D.M. Taub and F.A. King (eds.), pp.107–121. Van
Nostrand Reinhold, New York.
Froehlich, J.W. and Froehlich P.H. 1987. e status of
Panama’s endemic howling monkeys. Primate Conserv.
(8): 58–62.
Méndez-Carvajal, P.G. 2002a. El Kun-kun howler; an en-
demic primate in extinction risk. Icaro 7: 28-30.
Méndez-Carvajal, P.G. 2002b. Coiba Island, Panama. Neo-
trop. Primates 10(3): 162.
Méndez-Carvajal, P.G. & Serio-Silva, J.C. 2011. Daybreak
and bark analysis for two species of howler monkeys Al-
ouatta coibensis and Alouatta palliata: Atelidae, Republic
of Panamá. In: Perspectivas en Primatología Mexicana
(Ed.): Lilia Gama Campillo, Gilberto Pozo Montuy, Wil-
frido M. Contreras Sanchez, y Stefan L. Arriaga Weiss.
164–183pp.
Méndez-Carvajal, P.G. 2012. Population Study of Coiba
Howler Monkeys (Alouatta coibensis coibensis) and Coiba
Capuchin Monkeys (Cebus capucinus imitator), Coiba
Island National Park, Republic of Panama. J. Prima-
tol. 1:104. URL: http://dro.dur.ac.uk/15650/1/15650.
pdf?DDD5+kgvh67+d700tmt
Méndez-Carvajal, P. G. 2014. e Orion Camera System,
a new method for deploying camera traps in tree canopy
to study arboreal primates and other mammals: a case
study in Panama.
Revista Mesoamericana, 18(1): 9–23. URL: https://
www.rufford.org/files/Mesoamericana%2018(1)%20
Volumen%2018(1)%20Agosto%20de%202014%20
nn.pdf
Méndez-Carvajal, P.G. & Valdes-Díaz, S. 2017. Use of
anvils and other feeding behaviour observed in Cebus im-
itator, Coiba Island, Panama. Tecnociencia 19(1): 5–18.
URL:http://www.repositorio.up.ac.pa/635/1/Tecnocien-
cia%20Articulo%201%20Pedro%20Mendez.pdf
Milton, K. and Mittermeier, R. A. 1977. A brief survey
of the primates of Coiba Island, Panama. Primates 18:
931–936.
Panamá, SENACYT. 2019. La Estación Cientica Coiba
AIP presentó su plan estratégico. Secretaría Nacional de
Ciencia, Tecnología e Innovación (SENACYT), Panamá.
URL: <https://www.senacyt.gob.pa/la-estacion-cienti-
ca-coiba-aip-presento-su-plan-estrategico/>. Accessed 30
January 2019.
Ruord Foundation. 2011. Pedro Guillermo Méndez-
Carvajal. URL: https://www.ruord.org/rsg/projects/
pedro_guillermo_m%C3%A9ndezcarvajal. Accessed 30
January 2019.
ACTIVITIES OF THE MESOAMERICAN PRIMA
TOLOGY THEMATIC GROUP GITPRIMATES
MESO IN THE MESOAMERICAN SOCIETY FOR
THE BIOLOGY AND CONSERVATION SMBC
e VI Mesoamerican Primate Symposium was held at
the Sheraton Hotel in Panama City, Republic of Pan-
amá, as part of the program of the XXII Congreso de la
Sociedad Mesoamericana para la Biología y la Conserva-
ción, 21−25 November 2018. Seven of the eight Meso-
american countries were represented at this event, held
since 2012 to promote the exchange of information and
encourage collaboration among primatologists from the
region to improve and inspire new eorts from national
primatologists to conserve our primate species. e meet-
ings organized to date were in Panama (2012 and 2018),
Belize (2016), and Costa Rica (2017), all organized by
the Fundación Pro-Conservación de los Primates Pan-
ameños (FCPP) and its director Pedro Mendez-Carvajal,
who is also the coordinator of GIT Primates Meso. e
attendance was up compared to previous meetings due
to the huge support received from anonymous donors
besides the regular supporters (see Acknowledgements).
e Symposia are attracting attention in South America
and Caribbean side, and we welcome people from those
regions. ere were 14 participating primatologists who
presented papers on ethology (Pedro Méndez-Carvajal,
Pedro González), parasitology and zoonosis (Adela Palma,
Enos Juárez), plant chemistry and the howler diet (Karol
Gutiérrez), social hierarchy (Juan José Fernández-Cas-
tro), distribution (Danilo Chiari), conservation (Daniela
Solano-Rojas, Melissa Rodriguez, Jarinton García, Luz
Loría, Roger Morales, and Mynor Sandoval). e Meso-
american region and the Mesoamerican corridor are un-
der threat from the narco-deforestation, putting the last
Panamanian spider monkeys (Ateles geoffroyi panamensis)
at risk, according to the 2018 report of Primates in Peril:
e World’s 25 Most Endangered Primates. Eorts to pro-
tect the corridor have taken the lives of several conser-
vationists. e symposium included a session concern-
ing the importance of art as a tool for conservation. e
rst non-human primate mural in acrylic was presented
by Victor Aleksander Martínez, a Panamanian artist from
the University of Panama, creating a link between visual
Neotropical Primates 25(1), December 2019 61
power, cultural importance, and conservation. In our
opening and ending sessions, we reected on the loss of
Robert Horwich and his huge contribution in Mesoamer-
ica for the conservation of non-human primates, working
with the local communities, particularly in Belize, and
also on the legacy of the celebrated Honduran Berta Cá-
ceres, who fought so hard for wildlife conservation. Our
message is that conservation cannot be blind. As local
scientists and primatologists, we feel that conservationists
and scientists need to have more support from IUCN and
other organizations that promote conservation, a reality
that we face year by year. We need to have a backup when
a conservationist is under threat. is same argument
was pronounced by the author as the representative from
FCPP and GIT Primates Meso in the last Congress of the
International Primatological Society (IPS) held in Nairo-
bi, Kenya, in 2018. e improvement of primate studies
in Mesoamerica need to be promoted and for this reason,
we set up a new annual course in January 2018, “Moni-
toring Systems in Primates and Bats,” at the Chucanti
Natural Reserve, Maje Mountain Chain, Panama. e
course is an initiative of the FCPP, supported by Adopta
Bosque Panama (led by Guido Berguido), to train young
biologists and students in related elds interested in learn-
ing basic techniques to carry out population surveys for
primates and bats as arboreal and volant seed dispersers.
Due to the lack of updated scientic information on the
Mesoamerican primates, GIT Primates Meso and FCPP
opened a webpage (https://primatesmesoamerica.org) to
integrate new leaders and facilitate communication, not
only between primatologists but also others who may
be interested. Proceedings of the Mesoamerican Primate
Symposium can be found at https://fcprimatespanama.
org/noticias.html.
Acknowledgements
e Mesoamerican Primates Symposia have been made
possible by the support of Primate Action Fund (PAF) of
Conservation International and (currently) Global Wildlife
Conservation, the Margot Marsh Biodiversity Foundation,
Primate Conservation, Inc., and the Environment Minis-
try of Panama, and most by especially Emilio Sempris and
Yamil Sánchez. My special thanks to Durham University,
Durham, UK, and to Katharine Milton and Jackie Willis
for personal donations for the past symposia in Belize and
Costa Rica.
Pedro G. Méndez-Carvajal, Fundación Pro-Conservación
de los Primates Panameños (FCPP), 0816-05855, Panama.
E-mail: <mendezp@fcprimatespanama.org>, Professor,
Department of Physiology and Animal Behavior, School of
Biology, University of Panamá, and Associate Researcher,
Coiba Island Scientic Station (Coiba AIP).
O
FILOMENO ENCARNACIÓN: 1945-2019
Si en algún momento alguien va a escribir una histo-
ria de la primatología en el Perú, el nombre Filome-
prominente. Aunque no fue primatólogo por entrena-
miento sino botánico, sus actividades desarrolladas
como integrante del Proyecto Peruano de Primatología
(PPP), muchas en compañía de Rolando Aquino, han
sido extremamente importantes para avanzar y ampliar
los conocimientos acerca de los primates del Perú. El
tomo “Primates of Peru – Primates del Perú”, publica-
do como edición bilingüe en la revista Primate Report,
sigue siendo una referencia importante, no obstante los
muchos cambios taxonómicos y la cantidad de conoci-
miento generada desde su publicación en 1994. Fue au-
tor y co-autor de varias publicaciones sobre primates,
la Amazonía peruana.
Filomeno siempre tomaba una perspectiva conservacio-
-
llando actividades pertinentes. Durante el 2° simposio
“Primatología en el Perú” en Iquitos en noviembre 2013,
Filomeno – junto con Rolando Aquino – fue condecora-
do con el “Premio Philip Hershkovitz” por su eminente
contribución al desarollo de la primatología peruana y
nombrado miembro honorario de la Sociedad Latinoa-
mericana de Primatología.
Filomeno fue amigo mío desde que nos encontramos
-
producción y Conservación de Primates del Instituto
Veterinario de Investigaciones Tropicales y de Altura
(IVITA) en Iquitos. Estoy eternamente agradecido con
él por el enorme apoyo que recibí a largo de los años para
desarollar mis actividades primatológicas en el Perú, y
sobretodo por apoyar el desarollo de la Estación Bioló-
gica Quebrada Blanco. Siempre le recordaré con mucho
cariño y respeto, y le voy a extrañar. Estoy convencido
que este sentimiento es compartido por la comunidad
Neotropical Primates 25(1), December 201962
primatológica del Perú y allende de Latinoamérica. Fi-
lomeno falleció el 12 agosto de 2019; le sobreviven su
esposa Yolanda y su hija Myrcia.
Eckhard W. Heymann, Verhaltensökologie & Sozio-
biologie, Deutsches Primatenzentrum – Leibniz-Institut
für Primatenforschung, Kellnerweg 4, 37077 Göttingen,
Alemania. E-mail: eheyman@gwdg.de
Publicaciones científicas de Filomeno Encarnación
Cajañaupa
1. Aquino, R., Cornejo, F. M., Cortés Ortiz, L., Encar-
nación, F., Heymann, E. W., Marsh, L. K., Mitter-
meier, R. A., Rylands, A. B. and Vermeer, J. 2015.
Monkeys of Peru. Pocket identification guide – Primates
de Perú. Guía de identificación de bolsillo. Conserva-
tion International, Arlington.
structure of Aotus nancymai (Cebidae: Primates) in
Peruvian Amazon lowland forest. American Journal
of Primatology 11:1–7.
and use of sleeping sites in Aotus (Cebidae: Prima-
tes) in the Amazon lowlands of Peru. American Jour-
nal of Primatology 11:310–331.
-
tion densities and geographic distribution of night
monkeys (Aotus nancymai and Aotus vociferans) (Ce-
bidae: Primates) in northeastern Peru. American Jour-
nal of Primatology
5. Aquino, R. y Encarnación, F. 1994. Primates of Peru
- Los Primates del Perú. Primate Report 40:1–127.
6. Aquino, R. y Encarnación, F. 1996. Distribución
Saguinus tripartitus en la Amazonía del
Perú. Neotropical Primates 4:1–4.
7. Aquino, R. y Encarnación, F. 1999. Observaciones
preliminares sobre la dieta de Cacajao calvus ucayalii
en el nor-oriente peruano. Neotropical Primates 7:1–5.
Supplemental notes on population parameters of nor-
theastern Peruvian night monkeys, genus Aotus (Ce-
bidae). American Journal of Primatology 21:215–221.
9. Aquino, R., Puertas, P. y Encarnación, F. 1992.
Evaluación post-captura de Aotus vociferans y Aotus
nancymaae en bosques de la Amazonía peruana. Folia
Amazonica 4:141–151.
Las Mimosoídeas del Arborétum Jenaro Herrera
(provincia de Requena, departamento de Loreto,
Perú). Candollea 36:301–333.
11. Castro, N., Encarnación, F., Valverde, L., Uga-
moto, M. y Maruyama, E. 1990. Censo de prima-
tes no humanos en el sur oriente peruano: Iberia y
Iñapari (Departamento de Madre de Dios), Junio
(ed) La Primatología en el Perú - Investigaciones Pri-
matológicas (1973-1985). Imprenta Propaceb, Lima,
12. Descailleaux, J., Fujita, R., Rodríguez, L. A., Aqui-
no, R. y Encarnación, F. (1990) Rearreglos cromo-
sómicos y variabilidad cariotípica del género Aotus
(Cebidae: Platyrrhini). In: Castro-Rodríguez NE
(ed) La Primatología en el Perú Investigaciones Pri-
matológicas (1973-1985). Imprenta Propaceb, Lima,
pp 572–577.
Saimiri sciureus, Linnaeus, „fraile“ (Primates: Cebi-
dae) a nuevas fuentes alimenticias en la Amazonía
peruana. Boletín del Proyecto Primates 3:1–26.
forestales comunes en el Perú. Proyecto PNUD/
7. Mi-
nisterio de Agriculrtura, Lima, 149 p.
-
getación de la Amazonía peruana: estado actual de
los estudios, medio natural y ensayo de una clave
de determinación de las formaciones vegetales en la
llanura amazónica. Candollea 40:237–252.
16. Encarnación, F. 1993. El bosque y las formaciones
vegetales en la llanura amazónica del Perú. Alma
Máter 6:95–114.
17. Encarnación, F. 1990. Técnicas y sistemas de atrape
o captura de primates en la Amazonía peruana. In:
Castro-Rodríguez NE (ed) La Primatología en el Perú
Investigaciones Primatológicas (1973-1985). Imprenta
Propaceb, Lima, pp 152–157.
y vegetación de la Isla Iquitos y Padre Isla (Lore-
to, Perú): su relación con el manejo semiextensivo
de Saguinus mystax, Saimiri sciureus y Aotus. In: Cas-
tro-Rodríguez NE (ed) La Primatología en el Perú
Investigaciones Primatológicas (1973-1985). Imprenta
19. Encarnación, F. y Castro, N. 1990. Informe prelimi-
nar sobre censo de primates no humanos en el sur
oriente peruano: Iberia y Iñapar1.i (Departamento
Neotropical Primates 25(1), December 2019 63
Castro-Rodríguez NE (ed) La Primatología en el Perú
- Investigaciones Primatológicas (1973-1985). Imprenta
Propaceb, Lima, pp 57–67.
20. Encarnación, F., Castro, N. y de Rham, P. 1990.
Observaciones sobre primates no humanos en el
río Yuvineto (río Putumayo), Loreto, Perú. In: Cas-
tro-Rodríguez NE (ed) La Primatología en el Perú
Investigaciones Primatológicas (1973-1985). Imprenta
the Tumbes Reserved Zone. Primate Conservation
mass of wild Callimico goeldii. Folia Primatologica
23. Encarnación, F. y Ique, C. 2000. Sistemas agro-
foretales y manejo de Saguinus mystax en de la isla
inundable estacional, río Amazonas, Perú. In: San
Martín F, García P M (eds) La Primatología en el Perú
2, Lima, pp 153–174.
24. Encarnación, F., Moya, L., Aquino, R., Tapia, J. y
Soini, P. 2000. Situación y estado actual de las espe-
cies de primates no humanos en el Perú. In: Estrada
A, Rodríguez-Luna E, López-Wilchis R, Coates-Es-
trada R (eds) Estudios primatológicos en México. Uni-
versidad Veracruzana, Xalapa.
25. Encarnación, F., Moya, L., Soini, P. y Tapia, J. 1990.
La captura de Callitrichidae (Saguinus y Cebuella) en
la Amazonía peruana. In: DGFF/IVITA/OPS (ed) La
Primatología en el Perú Investigaciones Primatológicas
(1973-1985). Imprenta Propacep, Lima, pp 45–56.
Las meliáceas del Arborétum Jenaro Herrera (Pro-
vincia de Requena, Departamento de Loreto, Perú).
Candollea 39:693–713.
-
ráceas del Arborétum Jenaro Herrera (provincia de
Requena, departamento de Loreto, Perú). Candollea
36:335–347.
del Arborétum Jenaro Herrera (provincia de Requena,
departamento de Loreto, Perú). Candollea 37:1–15.
29. Garber, P. A., Encarnación, F., Moya, L. and Pruetz,
J. D. 1993. Demographic and reproductive patterns
in moustached tamarin monkeys (Saguinus mystax):
implications for reconstructing platyrrhine mating
systems. American Journal of Primatology 29:235–254.
30. Gozalo, A., Moya, L., Ique, C., Moro, J. and En-
carnación, F. 1991. Breeding the moustached ta-
marin (Saguinus mystax) on islands. In: Ehara A
(ed) Primatology Today. Elsevier Science Publishers,
pp 401–402.
30. Harada Hamel, M. L., Schneider, H., Encarnación,
F., Montoya, E. and Villavicencio, E. 1990. ABO
blood groups in two species of Peruvian night
monkeys (Aotus nancymai and Aotus vociferans). Revis-
ta Brasileira de Genetica 13:97–105.
31. Heltne, P. G. and Encarnación, F. 1990. Evaluación
de recursos primates en Madre de Dios, Perú: esta-
do corriente de primates y estrategias para investi-
gación y manejo en el futuro. In: Castro-Rodríguez
NE (ed) La Primatología en el Perú Investigaciones Pri-
matológicas (1973-1985). Imprenta Propaceb, Lima,
32. Heymann, E. W., Encarnación, F. and Canaquín, J.
E. (2002) Primates of the Río Curaray, northern Pe-
ruvian Amazon. International Journal of Primatology
23:191–201.
33. Heymann, E. W., Encarnación, F. and Soini, P. 2002.
Notes on the diagnostic characters and geographic
distribution of the “yellow-handed” titi monkey,
Callicebus lucifer, in Peru. Neotropical Primates
10:124–126.
34. Inga, H. and Encarnación, F. 2012. Ecología de
poblaciones naturales de ‘‘camu camu’’(Myrciaria
dubia Mc Vaugh) en los lagos Sahua y Supay, in-
mediaciones de Jenaro Herrera, Río Ucayali. Xilema
25:29–36.
35. Josse, C., Navarro, G., Encarnación, F., Tovar, A.,
Comer, P., Ferreira, W. A. S., Rodríguez, F., Saito,
J., Sanjurjo, J., Dyson, J., Rubin de Celis, E., Zárate,
R., Chang, J., Ahuite, M., Vargas, C., Paredes, F.,
Castro, W., Maco, J. and Reátegui, F. 2007. Ecolo-
gical systems of the Amazon Basin of Peru and Bolivia.
Classification and mapping. NatureServe, Arlington.
36. Montoya, E., Málaga, C., Villavicencio, E., Encar-
nación, F., Moro, J., Aquino, R. y Tapia, J. 1990.
Reproducción de Aotus nancymai en cautiverio. In:
Castro-Rodríguez NE (ed) La Primatología en el Perú
Investigaciones Primatológicas (1973-1985). Imprenta
37. Moya, L., Encarnación F. and Moro, J. 2000. Eva-
luación preliminar de las Islas de Panguana y de
Muyuy en el río Amazonas, para la introducción de
Saguinus labiatus. In: San Martín F, García P M (eds)
La Primatología en el Perú 2
Neotropical Primates 25(1), December 201964
2000. Liberación de los “pichico pecho anaranjado”
(Saguinus labiatus) en la Isla de Muyuy. In: San Mar-
tín F, García P M (eds) La Primatología en el Perú 2,
Lima, pp 109–120.
39. Puertas, P., Encarnación, F., Aquino, R. y García, J.
E. 1995. Análisis poblacional del pichico pecho ana-
ranjado, Saguinus labiatus, en el sur oriente peruano.
Neotropical Primates 3:4–7.
40. Puertas, P., Aquino, R. y Encarnación, F. 1992. Uso
de alimentos y competición entre el mono nocturno
Aotus vociferans y otros mamíferos, Loreto, Perú. Fo-
lia Amazónica 4:135–144.
41. Puertas, P. E., Aquino, R. and Encarnación, F. 1995.
Sharing of sleeping sites between Aotus vociferans
with other mammals in the Peruvian Amazon. Pri-
mates
42. Rylands, A. B., Matauschek, C., Aquino, R., Encar-
nación, F., de la Torre, S., Heymann, E. W. and Mit-
termeier, R. A. 2011. The range of the golden-mantle
tamarin, Saguinus tripartitus
distributions and sympatry of four tamarin species
in Colombia, Ecuador, and northern Peru. Primates
52:25–39.
43. Sampaio, M. I. C., Schneider, M. P. C., Barroso, C.
M. L., Silva, B. T. F., Schneider, H., Encarnación,
F., Montoya, E. and Salzano, F. M. 1991. Carbonic
anhydrase II in New World monkeys. International
Journal of Primatology
44. Schneider, H., Harada, M. L., Encarnación, F. and
Montoya, E. 1993. Comparison of ABO blood
groups from two species of Peruvian squirrel
monkeys (Saimiri sciureus macrodon, Saimiri bolivien-
sis peruviensis) with a natural population of S. b. pe-
ruviensis-S. s. macrodon hybrids. Revista Brasileira de
Genetica 16:661–-669.
45. Schneider, M. P. C., Sampaio, M. I. C., Schneider,
H., Encarnación, F., Montoya, E., Pissinatti, A.,
Coimbra-Filho, A. and Salzano, F. M. 1994. Com-
genera of New World monkeys. Revista Brasileira de
Genetica 17:321–329.
46. Schneider, H., Schneider, M. P. C., Sampaio, M.
I. C., Montoya, E., Tapia, J., Encarnación, F., An-
selmo, N. P. and Salzano, F. M. 1993. Divergence
three species of the Callicebus moloch group. Ameri-
can Journal of Physical Anthropology 90:345–350.
47. Schneider, M. P. C., Schneider, H., Sampaio, M. I.
C., Carvalho-Filho, N. M., Encarnación, F., Monto-
ya, E. and Salzano, F. M. 1995. Biochemical diversi-
ty and genetic distances in the Pitheciinae subfamily
(Primates, Platyrrhini). Primates 36:129–134.
-
sultados preliminares de la crianza de Saguinus mys-
tax (Primates: Callitrichidae) en un galpón de repro-
ducción al aire libre. Folia Amazónica 3:139–146.
49. Silva, B. T. F., Sampaio, M. I. C., Schneider, H.,
Schneider, M. P. C., Montoya, E., Encarnación, F.
and Salzano, F. M. 1992. Natural hybridization be-
tween Saimiri taxa in the Peruvian Amazonia. Pri-
mates 33:107–113.
50. Silva, B. T. F., Sampaio, M. I. C., Schneider, H.,
Schneider, M. P. C., Montoya, E., Encarnación, F.,
Protein electrophoretic variability in Saimiri and the
question of its species status. American Journal of Pri-
matology
51. Soini, P., de Soini, M., Aquino, R., Encarnación, F.,
Moya, L. y Tapia, J. 1990. Aspectos biológicos de
las especies de los géneros Saguinus y Cebuella. In:
Castro-Rodríguez NE (ed) La Primatología en el Perú
Investigaciones Primatológicas (1973-1985). Imprenta
Propaceb, Lima, pp 36–44.
Catálogo de los nombres vernáculos de los árboles
del Arborétum Jenaro Herrera y alrededores (pro-
vincia de Requena, departamento de Loreto, Perú).
Candollea 40:595–629.
Las combretáceas y rizoforáceas del Arborétum Je-
naro Herrera (provincia de Requena, departamento
de Loreto, Perú). Candollea
54. Tapia, J., Encarnación, F., Aquino, R., Moya, L. y
Soini, P. 1990. Censos poblacionales y sacas pe-
riodicas de primates en la Amazonía peruana. In:
DGFF/IVITA/OPS (ed) La Primatología en el Perú
-Investigaciones Primatológicas (1973-1985). Imprenta
Propacep, Lima, pp 325–341.
Neotropical Primates 25(1), December 2019 65
HORACIO SCHNEIDER (1948-2018)
Professor Horacio Schneider, best known for his work on the
phylogeny of New World monkeys, was a relentless advocate
for the advancement of science in the Amazon. In publish-
ing over 150 research articles, supervising over 50 graduate
students and holding along the years various administrative
positions at the Federal University of Pará (UFPA), Schnei-
der helped shape policy and establish excellence in biodiver-
sity research in Northern Brazil. With his death on Septem-
ber 27, at 70, the Amazon lost one of its champions.
Born in the city of São Paulo in 1948, Schneider entered
UFPA in 1969 to study medicine. Inuenced by the research
of Francisco Mauro Salzano and eodosius Dobzhansky,
Schneider’s interests quickly shifted to biology and he be-
came a voluntary student researcher for Manuel Ayres, study-
ing immune system diversity in indigenous populations.
He pursued both his Masters and PhD degrees at the Federal
University of Rio Grande do Sul, under the supervision of
the prominent Brazilian geneticist Francisco Mauro Salzano.
In 1984, in his doctoral work, Schneider used protein elec-
trophoresis to study protein polymorphisms in bualoes.
By the late 80’s, assessment of variation at the DNA level
was the dominant method used to measure genetic dier-
ences for generation of phylogenetic trees. In 1990, Schnei-
der joined the laboratory of Luigi Luca Cavalli-Sforza at
Stanford University, where he learned and later applied
molecular phylogenetics to unravel evolutionary relation-
ships in primates.
Upon his return to UFPA in 1992, Schneider had a collab-
orative grant with Morris Goodman at Wayne State Uni-
versity, on the broad theme of molecular systematics stud-
ies in primates. e collaboration lasted nearly a decade,
resulting in ve PhD theses and numerous publications,
including the rst New World primate phylogeny based on
DNA variation in 1993.
In 1998, Schneider threw himself into a new challenge: to
establish a Biology Research Center in Bragança, a small
town in the northeast coast of the State of Pará. During
the early 2000’s, his group was supported by research fund-
ing from the Millenium Institute program of the Brazilian
Government, as well as from a collaborative partnership
between Germany and Brazil (jointly coordinated with Ul-
rich Saint-Paul, University of Bremen), to conduct research
on mangrove dynamics and management (MADAM). is
represented a new avenue of investigation and his inter-
ests in phylogenetics and biogeography greatly expanded
to include a myriad of Amazonian invertebrate and verte-
brate species. In 2005, Schneider was a visiting researcher
at the University of Nebraska, Lincoln, where he worked
with Guillermo Ortí studying phylogenetic relationships in
Amazonian cichlids.
Schneider held multiple administrative roles in his career,
yet he is mostly known for his role as Vice Rector of the
UFPA from 2009 to 2017, where he helped spearhead the
expansion of infrastructure on UFPA campuses across the
State via the federal funding program known as REUNI.
Schneider was president of the Brazilian Society of Pri-
matology from 1991 to 1994 and also largely respected
among the Brazilian community of geneticists for being
twice elected as president of the Brazilian Society of Genet-
ics (2000 to 2002 and 2006 to 2008).
Over his career, Professor Schneider received numerous
academic awards and distinctions, including some of the
highest honors granted by Brazilian institutions. He was a
full member of the Brazilian National Academy of Sciences
since 2002 and received in 2002 the title of Commander
of the Order of Scientic Merit (medal given in person by
president Fernando Henrique Cardoso) and was later pro-
moted in 2010 to the Grã-Cruz class. He was also a mem-
ber of the advisory committee on Genetics at e Brazilian
Council of Research and Development (CNPq).
In 1989, the journal Nature published an article entitled
“An Amazon University for Amazonia”, where it described
the Schneider research team’s eort as “quite heroic”, high-
lighting the diculties surrounding research in the Amazon,
describing how “e laboratory roof sometimes leaks, the
water and electricity supply are unreliable and 90 percent of
their electrophoretic reagents have to be imported. e Uni-
versity is too poor to aord journal subscriptions”. e ar-
ticle also underscored the enthusiasm of the research group:
“the team is great in spirit”. His resilience in face of adversity
was a hallmark of his academic career and personal life.
On a more personal level, Professor Schneider was an elegant
softspoken man with an everpresent smile, a witty sense of
humor, and a fondness for music and poetry. He was a car-
ing husband, father and grandfather, and an inspiration to
his students and collaborators throughout the years. He also
possessed an unabating and contagious optimism, a charac-
ter trait much needed in times such as these. In his passing,
science in the Amazon lost one of its most powerful voices. A
tree fell in the forest and was heard by everyone.
is obituary by Igor Schneider was rst published
in Genetics and Molecular Biology, 41, 4, iii-iv (2018).
Neotropical Primates 25(1), December 201966
Horacio Schnider’s primate-related publication list
(journal articles and book chapters)
1. Schneider, M. P. C., Sampaio, M. I. D., and Schnei-
Cebus apella from the
Amazonian region. Animal Blood Groups and Bio-
chemical Genetics 13(2): 109–113.
2. Schneider, H., Corvelo, T. C. O., and Hamel, M. L. H.
Ce-
bus apella). Revista Brasileira de Genetica
3. Schneider, H., Hamel, M. L. H., and Corvelo, T. C.
of black-handed tamarins (Saguinus midas niger).
American Journal of Physical Anthropology 72(1): 39–
42. DOI: 10.1002/Ajpa.1330720105
4. Hamel, M. L. H., Schneider, H., Matayoshi, T., Na-
-
vary antigens in a population of capuchin monkeys
(Cebus apella paraguayanus) from Paraguay. Revista
Brasileira De Genetica 11(2): 317–327.
5. Schneider, H., Sampaio, I., Barroso, C. M. L., Sil-
va, B. T. F., Warzbort, R., Matayoshi, T., Howlin,
Genetic variability in a natural population of Cebus
apella paraguayanus (Cebidae, Primatas). Brazilian
Journal of Genetics
6. Schneider, M. P. C., Sampaio, M. I. D., Schneider,
natural populations of the Brazilian night monkey
(Aotus infulatus). International Journal of Primatology
10(4): 363-374. DOI: 10.1007/Bf02737422
7. Harada M. L. H., Schneider, H., Encarnacion, F.,
Montoya, E., and Villavicencio, E. 1990. ABO blood
groups in 2 species of Peruvian night monkeys (Ao-
tus nancymai and Aotus vociferans). Revista Brasileira de
Genetica 13(1): 97–105.
H. 1990. ABO blood groups in a natural population
of Chiropotes satanas. Revista Brasileira de Genetica
13(1): 107–113.
9. Rocha, R. M., Harada-Hamel, M. L., and Schneider,
H. 1990. ABO blood groups in natural populations
of Callitrichidae (Platyrrhini, Primates). Revista
Brasileira de Genetica 13(3): 531–537.
Schneider, M. P. C., and Salzano, F. M. 1990. Chro-
mosome and protein variation in red howler mon-
keys. Revista Brasileira de Genetica
11. Schneider, H., Sampaio, M. I. C., Schneider, M. P.
C., Ayres, J. M., Barroso, C. M. L., Hamel, A. R.,
Silva, B. T. F., and Salzano, F. M. 1991. Coat color
and biochemical variation in Amazonian wild popu-
lations of Alouatta belzebul. American Journal of Physi-
cal Anthropology
12. Sampaio, M. I. C., Schneider, M. P. C., Barroso, C.
M. L., Silva, B. T. F., Schneider, H., Encarnacion,
F., Montoya, E., and Salzano, F. M. 1991. Carbonic
anhydrase II In New World monkeys. International
Journal of Primatology
DOI: 10.1007/Bf02547619
13. Sampaio, I., Schneider, H., Barroso, C. M. L., Silva,
B. T. F., Schneider, M. P. C., Encarnación, F., Mon-
toya, E., and Salzano, F. M. 1991. Genetic variants
of carbonic anhydrase II in New World Monkeys. In:
Carbonic Anhydrase. F. Botrè, G. Gros, and B. T. Sto-
rey (eds.), pp.130–133. VCH Publishers, New York.
14. Sampaio, M. I. C., Barroso, C. M. L., Silva, B. T.
F., Seuanez, H., Matayoshi, T., Howlin, E., Nassazi,
N., Nagle, C., and Schneider, H. 1991. Genetic vari-
ability in Cebus appella paraguayanus: Biochemical
analysis of seven loci and variation in Glyoxalase I
(E.C.4.4.1.5). Primates 32(1): 105–109.
15. Schneider, H., and Harada, M. L. 1991. ABO blood
groups in squirrel monkeys (Saimiri boliviensis bolivi-
ensis). Revista Brasileira de Genetica
16. Schneider, H. 1992. A contribuição dos polimorf-
ismos bioquímicos ao estudo da microevolução no
gênero Callicebus. Brazilian Journal of Genetics 15:
229–233.
17. Silva, B. T. F., Sampaio, M. I. C., Schneider, H.,
Schneider, M. P. C., Montoya, E., Encarnacion, F.,
and Salzano, F. M. 1992. Natural hybridization be-
tween Saimiri taxa in the Peruvian Amazonia. Pri-
mates
H., and Schneider, M. P. C. 1992. Protein variation,
-
mosets (Genus Callithrix Erxleben, 1777). Primates
19. Melo, A. C. A., Sampaio, M. I. C., Schneider, M. P.
C., and Schneider, H. 1992. Biochemical diversity
and genetic distance in two species of the Genus Sa-
guinus. Primates 33(2): 217–225.
Neotropical Primates 25(1), December 2019 67
20. Rocha, R. M., Harada, M. L., and Schneider, H.
1992. ABO blood groups in Cebidae (Platyrrhini,
Primates) from the Rio Jamari Region. Primates
21. Schneider, H., Schneider, M. P. C., Sampaio, I.,
Harada, M. L., Stanhope, M., Czelusniak, J., and
Goodman, M. 1993. Molecular phylogeny of the
New World monkeys (Platyrrhini, Primates). Mo-
lecular Phylogenetics And Evolution 2(3): 225–242.
DOI: 10.1006/Mpev.1993.1022
22. Silva, B. T. F., Sampaio, M. I. C., Schneider, H.,
Schneider, M. P. C., Montoya, E., Encarnacion, F.,
Callegari-Jacques, S. M., and Salzano, F. M. 1993.
Protein electrophoretic variability in Saimiri and the
question of its species status. American Journal of Pri-
matology
DOI: 10.1002/Ajp.1350290304
23. Schneider, H., Schneider, M. P. C., Sampaio, M.
I. C., Montoya, E., Tapia, J., Encarnacion, F., An-
selmo, N. P., and Salzano, F. M. 1993. Divergence
three species of the Callicebus moloch group. Ameri-
can Journal of Physical Anthropology 90(3): 345–350.
24. Sampaio, M. I. D., Schneider, M. P. C., and Schnei-
der, H. 1993. Contribution of genetic distances
studies to the taxonomy of Ateles, particularly Ateles
paniscus paniscus and Ateles paniscus chamek. Interna-
tional Journal of Primatology
25. Schneider, H., Harada, M. L., Encarnacion, F.,
and Montoya, E. 1993. Comparison of ABO blood
groups from two species of Peruvian squirrel mon-
keys (Saimiri sciureus macrodon, Saimiri boliviensis
peruviensis) with a natural population of S. b. peruvi-
ensis-S. s. macrodon hybrids. Revista Brasileira de Ge-
netica 16(3): 661–669.
26. Schneider, M. P. C., Sampaio, M. I. D., Schneider,
H., Encarnacion, F., Montoya, E., Pissinatti, A., Co-
imbra, A., and Salzano, F. M. 1994. Comparative
study of lactate dehydrogenase in 15 genera of New
World monkeys. Revista Brasileira de Genetica 17(3):
321-329.
27. Harada, M. L., Schneider, H., Schneider, M. P. C.,
Sampaio, I., Czelusniak, J., and Goodman, M. 1995.
DNA evidence on the phylogenetic systematics of
New World Monkeys: Support for the sister group-
ing of Cebus and Saimiri from two unlinked nuclear
genes. Molecular Phylogenetics and Evolution 4(3):
331–349. DOI: 10.1006/Mpev.1995.1029
M. P. C., Czelusniak, J., and Goodman, M. 1995.
Evidence on primate phylogeny from epsilon-globin
Journal of Mo-
lecular Evolution 40(1): 30–55.
DOI: 10.1007/Bf00166594
29. Meireles, C. M. M., Schneider, M. P. C., Sampaio,
M. I. C., Schneider, H., Slightom, J. L., Chiu, C. H.,
Neiswanger, K., Gumucio, D. L., Czelusniak, J.,
and Goodman, M. 1995. Fate of a redundant gam-
ma-globin gene in the atelid clade of New World
monkeys: Implications concerning fetal globin gene
expression. Proceedings of the National Academy of Sci-
ences of the United States of America 92(7): 2607–2611.
DOI: 10.1073/Pnas.92.7.2607
30. Schneider, M. P. C., Schneider, H., Sampaio, M. I.
C., Carvalho Filho, N. M., Encarnacion, F. Montoya,
E., and Salzano, F. M. 1995. Biochemical diversity
and genetic distances in the Pitheciinae subfamily
(Primates, Platyrrhini). Primates 36(1): 129–134.
31. Schneider, H., and Rosenberger, A. L. 1996. Mol-
ecules, morphology, and platyrrhine systematics.
In: Adaptive Radiations of Neotropical Primates, M. A.
Norconk, A. L. Rosenberger, and P. A. Garber (eds.),
pp.3–19. Springer, New York.
32. Schneider, H., Sampaio, I., Harada, M. L., Barroso,
C. M. L., Schneider, M. P. C., Czelusniak, J., and
Goodman, M. 1996. Molecular phylogeny of the
New World monkeys (Platyrrhini, primates) based
on two unlinked nuclear genes: IRBP intron 1 and
epsilon-globin sequences. American Journal of Physi-
cal Anthropology 100(2):153–79.
33. Schneider, H., Schneider, M. P. C., Sampaio, I.
1996. Systematics of the Platyrrhines. In: Systemat-
ics of the Platyrrhines, S. F. Ferrari, and H. Schneider
(eds.), pp.1–364. Editora da Universidade Federal
do Pará, Belém.
34. Chiu, C. H., Schneider, H., Schneider, M. P. C.,
Sampaio, I., Meireles, C., Slightom, J. L., Gumucio,
D. L., and Goodman, M. 1996. Reduction of two
functional gamma-globin genes to one: An evolu-
tionary trend in New World monkeys (infraorder
Platyrrhini). Proceedings of the National Academy of
Sciences of the United States of America 93(13): 6510–
6515. DOI: 10.1073/pnas.93.13.6510
35. Johnson, R. M., Buck, S., Chiu, C. H., Schneider,
H., Sampaio, I., Gage, D. A., Shen, T. L., Schneider,
M. P. C., Muniz, J. A., Gumucio, D. L., and Good-
man, M. 1996. Fetal globin expression in new world
Neotropical Primates 25(1), December 201968
44. Meireles, C., Sampaio, I., Schneider, H., Ferrari, S.
F., Coimbra, A. F., Pissinatti, A., and Schneider, M.
P. C. 1997. A comparative study of eleven protein
systems in tamarins, genus Saguinus (Platyrrhini,
Callitrichinae). Brazilian Journal of Genetics 20(1):
45. Goodman, M., Porter, C. A., Czelusniak, J., Page,
S. L., Schneider, H., Shoshani, J., Gunnell, G., and
-
cation of primates based on DNA evidence comple-
mented by fossil evidence. Molecular Phylogenetics
and Evolution
46. Boissinot, S., Tan, Y., Shyue, S. K., Schneider, H.,
Sampaio, I., Neiswanger, K., Hewett-Emmett, D.,
linked triallelic color vision systems in New World
monkeys. Proceedings of the National Academy of Sci-
ences of the United States of America 95(23): 13749–
13754. DOI: 10.1073/pnas.95.23.13749
47. Figueiredo, W. M. B., Carvalho-Filho, N. M.,
DNA sequences and the taxonomic status of Alouat-
ta seniculus populations in north eastern Amazonia.
Neotropical Primates 6(6): 73–77.
-
paio, I., Schneider, M. P., Abee, C. R., Williams,
L., Hewett-Emmett, D., Sperling, H. G., Cowing, J.
Molecular genetics of spectral tuning in New World
monkey color vision. Journal of Molecular Evolution
46(6): 697–702. DOI: 10.1007/PL00006350
49. Meireles, C. M., Czelusniak, J., Sampaio, I., Schnei-
der, H., Ferrari, S. F., Coimbra, A. F., Pissinatti, A.,
Muniz, J. A. P. C., Ferreira, H. S., and Schneider, M.
taxonomic implications in Callitrichini (Primates,
Platyrrhini). Biochemical Genetics
50. Chaves, R., Sampaio, I., Schneider, M. P., Schnei-
der, H., Page, S. L., and Goodman, M. 1999. The
place of Callimico goeldii in the callitrichine phylo-
genetic tree: Evidence from von Willebrand factor
gene intron II sequences. Molecular Phylogenetics and
Evolution 13(2): 392–404.
51. Porter, C. A., Czelusniak, J., Schneider, H., Schnei-
der, M. P. C., Sampaio, I., and Goodman, M. 1999.
-
silon-globin gene support the relationship of Cal-
licebus with the Pitheciins. American Journal of
monkeys. Journal of Biological Chemistry 271(25):
36. Sampaio, I., Schneider, M. P. C., and Schneider,
H. 1996. Taxonomy of the Alouatta seniculus group:
Biochemical and chromosome data. Primates 37(1):
37. Sampaio, I., Schneider, H., Barroso, C. M. L., and
Schneider, M. P. C. 1996. Polymorphism of the
phosphogluconate dehydrogenase (PGD) in New
World monkeys: taxonomic implications. Genetics
and Molecular Biology
H., Schneider, M. P. C., Sampaio, I., and Goodman,
M. 1997. Phylogeny and evolution of selected pri-
mates as determined by sequences of the epsilon-
International
Journal of Primatology
39. Tagliaro, C. H., Schneider, M. P. C., Schneider, H.,
Sampaio, I. C., and Stanhope, M. J. 1997. Marmoset
phylogenetics, conservation perspectives, and evo-
lution of the mtDNA control region. Molecular Biol-
ogy and Evolution
40. Barroso, C. M. L., Schneider, H., Schneider, M. P.
C., Sampaio, I., Harada, M. L., Czelusniak, J., and
Goodman, M. 1997. Update on the phylogenetic
systematics of new world monkeys: Further DNA
evidence for placing the pygmy marmoset (Cebuella)
within the genus Callithrix. International Journal of
Primatology
41. Porter, C. A., Czelusniak, J., Schneider, H., Schnei-
der, M. P. C., Sampaio, I., and Goodman, M. 1997.
Sequences of the primate epsilon globin gene: im-
plications for systematics of the marmosets and
other New World primates. Gene 205(1–2): 59–71.
42. Chiu, C. H., Schneider, H., Slightom, J. L., Gu-
mucio, D. L., and Goodman, M. 1997. Dynamics
of regulatory evolution in primate beta globin gene
clusters: cis-mediated acquisition of simian gamma
fetal expression patterns. Gene 205(1–2): 47–57.
43. Boissinot, S., Zhou, Y. H., Qiu, L., Dulai, K. S.,
Neiswanger, K., Schneider, H., Sampaio, I., Hunt,
D. M., Hewett Emmett, D., and Li, W. H. 1997.Ori-
gin and molecular evolution of the X-linked dupli-
cate color vision genes in howler monkeys. Zoologi-
cal Studies 36(4):360–369.
Neotropical Primates 25(1), December 2019 69
Primatology
52. Rylands, A., Schneider, H., Langguth, A., Mitter-
meier, R., Groves, C., and Rodríguez Luna, E. 2000.
An assessment of the diversity of the New World
primates. Neotropical Primates
53. Schneider, H. 2000. The current status of the New
World monkey phylogeny. Anais da Academia
Brasileira de Ciencias 72(2): 165–172.
DOI: 10.1590/S0001-37652000000200005
54. Tagliaro, C. H., Schneider, M. P. C., Schneider,
H., Sampaio, I, and Stanhope, M. 2000. Molecular
studies of Callithrix pygmaea (Primates, Platyrrhini)
based on transferrin intronic and ND1 regions: im-
plications for taxonomy and conservation. Genetics
and Molecular Biology 23(4): 729–737.
DOI: 10.1590/S1415-47572000000400006
55. Vallinoto, M., Sena, L., Sampaio, I., Schneider, H.,
and Schneider, M. P. 2000. Mitochondrial DNA-like
sequence in the nuclear genome of Saguinus (Callit-
richinae, Primates): transfer estimation. Genetics and
Molecular Biology 23(1): 35–42.
DOI: 10.1590/S1415-47572000000100006
56. Schneider, H., Canavez, F. C., Sampaio, I., Moreira,
M. A. M., Tagliaro, C. H., and Seuanez, H. N. 2001.
Can molecular data place each neotropical monkey
in its own branch? Chromosoma
DOI: 10.1007/s004120000106
57. Sena, L., Vallinoto, M., Sampaio, I., Schneider,
H., Ferrari, S. F., and Schneider, M. P. C. 2002.
Mitochondrial COII gene sequences provide new
insights into the phylogeny of marmoset species
groups (Callitrichidae, primates). Folia Primatologica
73(5): 240–251. DOI: 10.1159/000067456
2002. ABO blood groups in the primate species of
Cebidae from the Amazon region. Journal of Medical
Primatology 31(3): 136–141.
59. Schneider, I., Schneider, H., Schneider, M. P., and
Silva, A. 2004. The prion protein and New World
primate phylogeny. Genetics and Molecular Biology
27(4): 505– 510.
DOI: 10.1590/S1415-47572004000400007
60. Tagliaro, C. H., Schneider, H., Sampaio, I., Schnei-
der, M. P. C., Vallinoto, M., and Stanhope, M. 2005.
Molecular phylogeny of the genus Saguinus (Platyr-
rhini, Primates) based on the ND1 mitochondrial
gene and implications for conservation. Genetics and
Molecular Biology
DOI: 10.1590/S1415-47572005000100009
61. Schneider, H., Sampaio, I., Vallinoto, M., Bernardi,
J. A. R., Rego, P. S., Araripe, J., and Tagliaro, C.
2005. The phylogeny of the Callitrichinae, with
special emphasis on the marmosets (including Cal-
libela), Callimico and new information on Brazilian
Saguinus. American Journal of Physical Anthropology
62. Vallinoto, M., Araripe, J., do Rego, P. S., Tagliaro,
C. H., Sampaio, I., and Schneider, H. 2006. Tocan-
Sagu-
inus niger populations. Genetics and Molecular Biology
29(2): 215–219.
DOI: 10.1590/S1415-47572006000200005
63. de Lima C, M. M., Sampaio, I., Vieira, R. S., and
Schneider, H. 2007. Spider monkey, muriqui and
woolly monkey relationships revisited. Primates
64. Araripe, J., Tagliaro, C. H., Rego, P. S., Sampaio,
-
lar phylogenetics of large-bodied tamarins, Saguinus
spp. (Primates, Platyrrhini). Zoologica Scripta 37(5):
65. Schneider, H., Bernardi, J. R., Cunha, D. B., Taglia-
ro, C. H., Ferrari, S. F., and Sampaio, I. 2009. Cal-
libella and Cebuella are Mico until proven otherwise.
American Journal of Primatology 71: 94.
66. da Cunha, D. B., Monteiro, E., Vallinoto, M., Sam-
paio, I., Ferrari, S. F., and Schneider, H. 2011. A mo-
lecular phylogeny of the tamarins (genus Saguinus)
containing Alu insertions. American Journal of Physi-
cal Anthropology
67 Schneider, H., Bernardi, J. A. R., da Cunha, D. B.,
Tagliaro, C. H., Vallinoto, M., Ferrari, S. F., and
Sampaio, I. 2012. A molecular analysis of the evo-
lutionary relationships in the Callitrichinae, with
emphasis on the position of the dwarf marmoset.
Zoologica Scripta 41(1): 1-10.
DOI: 10.1111/j.1463-6409.2011.00502.x
Harada, M.L., Silva, J. M. C., Bates, J. M., and Silva
Junior, J. S. E. 2013. A molecular phylogeography of
the uacaris (Cacajao). In: Evolutionary Biology and Con-
servation of Titis, Sakis and Uacaris. L. M. Veiga, A. A.
Barnet, S. F. Ferrari, and M. A. Norconk (eds.), pp.23–
30. Cambridge University Press, Cambridge, UK.
Neotropical Primates 25(1), December 201970
69. Schneider, H., and Sampaio, I. 2015. The systemat-
ics and evolution of New World primates - A review.
Molecular Phylogenetics and Evolution
DOI: 10.1016/j.ympev.2013.10.017
70. Martins, A. M. G., Jr., Amorim, N., Carneiro, J. C.,
Antunes de Mello A. P. R., Sampaio, I., and Schnei-
der, H. 2015. Alu elements and the phylogeny of
capuchin (Cebus and Sapajus) monkeys. American
Journal of Primatology
DOI: 10.1002/ajp.22352
71. Byrne, H., Rylands, A. B., Carneiro, J. C., Lynch-
Alfaro, J. W., Bertuol, F., da Silva, M. N. F., Mes-
sias, M., Groves, C. P., Mittermeier, R. A., Farias, I.,
Hrbek, T., Schneider, H., Sampaio, I., and Boubli,
J. P. 2016. Phylogenetic relationships of the New
World titi monkeys (Callicebus
taxonomy based on molecular evidence. Frontiers in
Zoology
72. Carneiro, J., De Sousa E Silva, J., Jr., Sampaio, I.,
Pissinatti, A., Hrbek, T., Messias, M. R., Rohe, F.,
Farias, I., Boubli, J., and Schneider, H. 2016. Phy-
logeny of the titi monkeys of the Callicebus moloch
group (Pitheciidae, Primates). American Journal of
Primatology
DOI: 10.1002/ajp.22559
73. Carneiro, J., da Silva Rodrigues-Filho, L. F., Schnei-
der, H., and Sampaio, I. 2016. Molecular data high-
light hybridization in squirrel monkeys (Saimiri,
Cebidae). Genetics and Molecular Biology 39(4): 539–
74. Boubli, J. P., da Silva, M. N. F., Rylands, A. B.,
Nash, S. D., Bertuol, F., Nunes, M., Mittermeier, R.
A., Byrne, H., Silva, F. E., Rohe, F., Sampaio, I.,
many pygmy marmoset (Cebuella -
cies are there? A taxonomic re-appraisal based on
new molecular evidence. Molecular Phylogenetics and
Evolution
DOI: 10.1016/j.ympev.2017.11.010
75. Martins-Junior, A. M. G., Carneiro, J. C., Sampaio,
-
netic relationships among Capuchin (Cebidae, Plat-
yrrhini) lineages: An old event of sympatry explains
the current distribution of Cebus and Sapajus. Genetics
and Molecular Biology 41(3): 699–712.
76. Byrne, H., Lynch Alfaro, J. W., Sampaio, I., Farias,
Titi monkey biogeography: Parallel Pleistocene
spread by and into a post-Pebas Western Amazon.
Zoologica Scripta 47(5): 499–517.
DOI: 10.1111/zsc.12300
77. Carneiro, J., Sampaio, I., De Sousa E Silva-Júnior,
J., Farias, I., Hrbek, T., Pissinatti, A., Silva, R., Mar-
tins-Junior, A., Boubli, J., Ferrari, S. F., and Schnei-
-
geographic history of the titi monkeys (Callicebus,
Pitheciidae) of eastern Brazil. Molecular Phylogenetics
and Evolution 124:10–15.
R P
BOOKS
e Promise of Contemporary Primatology, edited by Riley
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book argues for a contemporary primatology that recog-
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for collaborative exchange across the natural sciences, so-
cial sciences, and humanities. Content: 1) Introduction:
e promise of Contemporary Primatology; 2) Franz Boas,
American Anthropology, and the Biological-Sociocultural
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texts: e Emergence of Ethnoprimatology; 6) Beyond the
Divide: Fieldwork, Reexivity, and Multispecies worlds;
7) Primate Conservation in the Twenty-First Century,
and Beyond; 8) Conclusions: Reclaiming Primatology as
Anthropology.
Studying Primates: How to Design, Conduct and Report
Primatological Research. Setchell J. Cambridge University
Press. 360pp. ISBN: 978-1108434270. is accessible
guide for graduate students and post-doctoral researchers
explains how to develop a research question, formulate
testable hypotheses and predictions, design and conduct
a project and report the results. e focus is on research
integrity and ethics throughout, and the book provides
practical advice on overcoming common diculties re-
searchers face. Contents: 1) Asking the questions about
primates; 2) Ethics in primatology; 3) Keeping science
healthy: research integrity; 4) Inclusive science; 5) Under-
standing statistical evidence; 6) Communicating ideas in
writing; 7) Introduction to the primates; 8) Why study
primates?; 9) Identifying a research question; 10) Find-
ing out what we know; 11) Reading journal articles; 12)
Formulating hypothesis and predictions and designing a
study; 13) Observing and manipulating; 14) Choosing
measures; 15) Planning data analysis; 16) Sampling and
statistical power; 17) Checking feasibility and nalizing
your plans; 18) Writing research proposal; 19) Collect-
ing data; 20) Conducting eldwork; 21) Analysing and
Neotropical Primates 25(1), December 2019 71
interpreting data; 22) General guidance; 23) Submitting
to a peer-reviewed journal; 24) Presenting your work at a
conference; 25) Conclusions.
ARTICLES
Arakaki, P. R., Borges, P. A., Hidalgo, R., Teixeira, F., Bra-
ga, F., et al. 2019. Testicular volume and semen charac-
teristics in the endangered southern muriqui (Brachyteles
arachnoides). J. Med. Primatol. 48(4): 244–250.
Arakaki, P. R., Borges Salgado, P. A., Losano, J. D. A., Ro-
drigues Gonçalves D, do Valle R, Garcia Pereira, R. J.
and Nichi, M. 2019. Semen cryopreservation in golden
headed lion tamarin, Leontopithecus chrysomelas. Am. J.
Primatol. 81(12).
Aristizabal, J. F., Negrete-Yankelevich, S., Macías-Ordónez,
R., et al. 2019. Spatial aggregation of fruits explains food
selection in a Neotropical primate (Alouatta pigra). Sci.
Rep. 9: 19452.
Armstrong, A. R., Wunschmann, A., Rigatti, L. H., et al.
2019. Clostridium difficile Enterocolitis in a captive Geof-
froy’s Spider monkey (Ateles geoffroyi) and common Mar-
mosets (Callithrix jacchus). Vet. Pathol. 56(6): 959–963.
Back, J. P. and BiccaMarques, J. C. 2019. Supplemented
howler monkeys eat less wild fruits, but do not change
their activity budgets. Am. J. Primatol. 81(9).
Barreta Pinto, J., Martinez, J., Bernal, Y., Sánchez, R., et
al. 2019. Genetic dierentiation and diversity of the Bo-
livian endemic titi monkeys, Plecturocebus modestus and
Plecturocebus olallae. Primates 60(6):565–573.
Barreto, M. A., dos Santos, E., Cardoso, J., Noll, C. A.,
Moura, M., et al. 2019.Detection of antibodies against
Icoaraci, Ilhéus, and Saint Louis Encephalitis arboviruses
during yellow fever monitoring surveillance in nonhu-
man primates (Alouatta caraya) in southern Brazil. J.
Med. Primatol. 48(4): 211–217
Beran, M. J., French, K. and Smith, T. R. 2019. Limited
evidence of number-space mapping in Rhesus monkeys
(Macaca mulatta) and Capuchin conkeys (Sapajus apella).
J. Comp. Psychol. 133(4): 281–293.
Bergstrom, M. L., Hogan, J. D., Melin, A. D. and Fedi-
gan, L. M. 2019. e nutritional importance of inverte-
brates to female Cebus capucinus imitator in a highly sea-
sonal tropical dry forest. Am. J. Phys. Anthropol. 170(2):
207–216.
Bolt, L. M., Russell, D. G., Coggeshall, E. M. C., et al.
2019. Howling by the river: howler monkey (Alouatta
palliata) communication in an anthropogenically-altered
riparian forest in Costa Rica. Behavior 157(1): 77–100.
Bolt, L. M., Schreier, A. L., Russe, D. G., et al. 2019.
Howling on the edge: Mantled howler monkey (Alouatta
palliata) howling behaviour and anthropogenic edge ef-
fects in a fragmented tropical rainforest in Costa Rica.
Ethology 125(9): 593–602.
Bothwell, E. S., Mendoza, S. P., Ragen, B. J., et al. 2019. Do-
pamine D1-like receptors regulate agonistic components
of pair bond maintenance behaviors in male titi monkeys
(Callicebus cupreus). Psychoneuroendocrino. 106: 259–267.
Brown, C. J., Mtui, D., Oswald, B. P., Van Leuven, J. T.,
Vallender, E. J., SchultzDarken, N., Ross, C. N., Tardif,
S. D., Austad, S. N., Forney, L. J. 2019. Comparative
genomics of Bifidobacterium species isolated from mar-
mosets and humans. Am. J. Primatol. 81(10).
Busia, L., Schaner, C. M. and Aureli, F. 2019. Watch out!
Insecure relationships aect vigilance in wild spider mon-
keys (Ateles geoffroyi). Behav. Ecol. Sociobiol. 73(12).
Campbell Nekaris, K. A. I., Pereira, T. S., Allgas, N. and
Shanee, S. 2019. Occupancy modeling for the conser-
vation assessment of the Peruvian Night monkey (Aotus
miconax). Primate Conserv. (33): 13–20.
Chaves, P. B., Magnus, T., Jerusalinsky, L., Talebi, M., Stri-
er, K., Breves, P., Tabacow, F., Teixeira, R. H. F., Moreira,
L., Hack, R. O. E., et al. 2019. Phylogeographic evidence
for two species of muriqui (genus Brachyteles) positional
behavior and substrate use in wild adult bearded capuchin
monkeys (Sapajus libidinosus). Am. J. Primatol. 81(12).
Corewyn, L. C. 2019. Greeting behaviors in male Alouatta
palliata at La Pacica, Costa Rica. Int. J. Primatol. 40 (6):
630–646.
Erkenswick, G. A., Watsa, M., Gozalo, A. S., Dudaie, S.,
Bailey, L., Muranda, K. S., Kuziez, A. and Parker, P. G.
2019. A multiyear survey of helminths from wild saddle-
back (Leontocebus weddelli) and emperor (Saguinus im-
perator) tamarins. Am. J. Primatol. 81(12).
Fam, B. S. O., Reales, G., VargasPinilla, P., Paré, P., Vis-
cardi, L. H., Sortica, V. A., Felkl, A. B., Franco, A. O.,
Lucion, A. B., CostaNeto, C. M., Pissinatti, A., Salzano,
F. M., PaixãoCôrtes, V. R. and Bortolini, M. C. 2019.
AVPR1b variation and the emergence of adaptive phe-
notypes in Platyrrhini primates. Am. J. Primatol. 81(8).
Fernandes Junior, O., de Oliveira, G. E., Santos, F. M.,
et al. 2019. Behavioral activities and diet of Azaras’s ca-
puchin monkey, Sapajus cay (Illiger, 1815), in a forest
remnant of the Brazilian Cerrado. Stud. Neotrop. Fauna
E. DOI:10.1080/01650521.2019.1708228.
Ferraro, M. A. R., Molina, C. V., Gris, V. N., Kierul, M.
C. M., Galvão Bueno, M., et al. 2019. Early reversal of
ketamine/dexmedetomidine chemical immobilization by
atipamezole in goldenheaded lion tamarins (Leontopithe-
cus chrysomelas). J. Med. Primatol. 48(6): 351–356.
Firrman, J., Liu, L. S., Tanes, C., Bittinger, K., Mahalak,
K. and Rinaldi, W. 2019. Metagenomic assessment of the
Cebus apella gut microbiota. Am. J. Primatol. 81(10).
Garber, P. A., Caselli, C. B., McKenney, A. C., Abreu, F.,
De la Fuente, M. F., Araújo, A., Arruda, M. F., Souto,
A., Schiel, N. and BiccaMarques, J. C. 2019. Trait varia-
tion and trait stability in common marmosets (Callithrix
jacchus) inhabiting ecologically distinct habitats in north-
eastern Brazil. Am. J. Primatol. 81(7).
Garber, P. A., Mallott, E. K., Porter, L. M. and Gomez, A.
2019. e gut microbiome and metabolome of saddleback
tamarins (Leontocebus weddelli): insights into the foraging
ecology of a smallbodied primate. Am. J. Primatol. 81(10).
Neotropical Primates 25(1), December 201972
Gomes Almeida, T. T., Barros Monteiro, M. V., Guima-
raes, R. C., et al. 2019. Eect of gluten diet on blood
innate immune gene expressions and stool consistency in
Spix’s Saddleback Tamarin (Leontocebus fuscicollis) raised
in captivity. Mol. Biol. Rep. 46(4): 3617–3623.
Gusmão, A. C., Messias, M. R., Carneiro, J. C., Schnei-
der, H., de Alencar, T. B., et al. 2019. A new species of
Titi Monkey, Plecturocebus. Byrne et al., 2016 (Primates,
Pitheciidae), from Southwestern Amazonia, Brazil. Pri-
mate Conserv. (33): 21–35.
Hardin, A. M. 2019. Genetic correlations in the dental di-
mensions of Saguinus fuscicollis. Am. J. Phys. Anthropol.
169(3): 557–566.
Heimbauer, L. A., Johns, T. N. and Weiss, D. J. 2019. In-
ferential reasoning in the visual and auditory modalities
by Cotton-Top Tamarins (Saguinus oedipus). J. Comp.
Psychol. 133(4): 496–501.
Hogan, J. D., Jack, K. M., Campos, F. A., Kalbitzer, U.
and Fedigan, L. M. 2019. Group versus population level
demographics: an analysis of comparability using long
term data on wild whitefaced capuchin monkeys (Cebus
capucinus imitator). Am. J. Primatol. 81(7).
Kajokaite, K., Whalen, A., Panchanathan, K. and Perry, S.
2019. White-faced capuchin monkeys use both rank and
relationship quality to recruit allies. Anim. Behav. 154:
161–169.
Kawaguchi, Y., Kuroshima, H. and Fujita, K. 2019. Age
categorization of conspecic and heterospecic faces in
Capuchin Monkeys (Sapajus apella). J. Comp. Psychol.
133(4): 502–511.
Kawai, N., Nakagami, A., Yasue, M., et al. 2019. Common
Marmosets (Callithrix jacchus) evaluate third-party social
interactions of human actors but Japanese monkeys (Ma-
caca fuscata) do not. J. Comp. Psychol. 133(4): 488–495.
Kishimoto, R., Iwasaki, S. and Fujita, K. 2019. Do Capu-
chins (Sapajus apella) know how well they will remem-
ber? Analysis of delay length-dependency with memory
strategies. J. Comp. Psychol. 133(4): 340–350.
Lima, M., Mendes, S. L. and Strier, K. B. 2019. Habitat
use in a population of the Northern Muriqui (Brachyteles
hypoxanthus). Int. J. Primatol. 40: 470–495.
Mareike, C. A., Burrell, A. S., Orkin, J. D., et al. 2019. Dupli-
cation and parallel evolution of the pancreatic ribonuclease
gene (RNASE1) in folivorous non-colobine primates, the
howler monkeys (Alouatta spp.). Sci. Rep. 9: 20366.
Martinez, M. F., Santini, M. S., Kowalewski, M., et al.
2019. Phlebotominae in peri-domestic and forest envi-
ronments inhabited by Alouatta caraya in northeastern
Argentina. Med. Vet. Entomol. 33(3): 367–374.
Martins, E. M., Moura, A. C., Finkenwirth, C., et al. 2019.
Food sharing patterns in three species of Callitrichid
monkeys (Callithrix jacchus, Leontopithecus chrysomelas,
Saguinus midas): individual and species dierences. J.
Comp. Psychol. 133(4): 474–487.
McCoy, D. E., Frye, B. M., Kotler, J., Burkart, J. M., Burns,
M., Embury, A., Eyre, S., Galbusera, P., Hooper, J., Idoe,
A., López Goya, A., Mickelberg, J., Quesada, M. P., Ste-
venson, M., Sullivan, S., Warneke, M., Wojciechowski,
S., Wormell, D., Haig, D., Tardif, S. D. 2019. A com-
parative study of litter size and sex composition in a large
dataset of Callitrichine monkeys. Am. J. Primatol. 81(9).
McKinney, T. 2019. Ecological and behavioural exibility
of Mantled Howlers (Alouatta palliata) in response to an-
thropogenic habitat disturbance. Folia Primatol. 90(6):
456–469.
McNamara, A., Dunham, N. T., Shapiro, L. J. and Young,
L. W. 2019. e eects of natural substrate discontinui-
ties on the quadrupedal gait kinematics of freeranging
Saimiri sciureus. Am. J. Primatol. 81(9).
Medeiros, K., Bastos, M. and Jones, G. 2019. Behavior,
diet, and habitat use by blonde Capuchin monkeys (Sa-
pajus flavius) in a coastal area prone to ooding: direct
observations and camera trapping. Int. J. Primatol. 40:
511–531.
Milton, K., Armitage, D. W. and Sousa, W. P. 2019. Suc-
cessional loss of two key food tree species best explains
decline in group size of Panamanian howler monkeys (Al-
ouatta palliata). Biotropica 51(4): 600–614.
Miranda, T. S., Muniz, C. P., Moreira, S. Bp, et al. 2019.
Eco-epidemiological prole and molecular characteriza-
tion of simian Foamy Virus in a recently-captured in-
vasive population of Leontopithecus chrysomelas (Gold-
en-Headed Lion Tamarin) in Rio de Janeiro, Brazil.
Viruses-Basel 11(10): 931.
Molina, C. V., Bueno, M. G., Kierul, M. C. M., Pis-
sinatti, A., Cunha, M. P. V., et al. 2019. Spontaneous
meningoencephalitis by Staphylococcus aureus in an infant
goldenheaded lion tamarin (Leontopithecus chrysomelas).
J. Med. Primatol. 48(6): 370–373.
Muir, J., Barnett, A., Svensson, M. S. 2019. e vocal rep-
ertoire of Golden-Faced Sakis, Pithecia chrysocephala, and
the relationship between context and call structure. Int. J.
Primatol. 40(6): 721–743.
Murphy, A. M., Ross, C. N. and BlissMoreau, E. 2019.
Noninvasive cardiac psychophysiology as a tool for trans-
lational science with marmosets. Am. J. Primatol. 81(9).
Oliveira Da Silva, G. A., Falótico, T., Nash, S. D. et al.
2019. A green racer snake (Philodryas nattereri, Colubri-
dae) killed but not eaten by a blonde capuchin monkey
(Sapajus flavius, Cebidae). Primates 60(5): 459–465.
Ordóñez-Gómez, J. D., Santillan-Doherty, A. M. and
Hammerschmidt, K. 2019. Acoustic variation of spider
monkey (Ateles geoffroyi) contact calls is related to caller
isolation and aects listeners’ responses. Plos ONE.
Orkin, J. D., Webb, E. S. and Melin, A. D. 2019. Small to
modest impact of social group on the gut microbiome of
wild Costa Rican capuchins in a seasonal forest. Am. J.
Primatol. 81(10).
Painter, M. C., Russell, R. C. and Judge, P. G. 2019. Capu-
chins (Sapajus apella) and Squirrel monkeys (Saimiri sciu-
reus) fail to attend to the functional spatial relationship
between a tool and a reward. J. Comp. Psychol. 463–473.
Parrish, A. E., Beran, M. J. and Agrillo, C. 2019. Lin-
ear numerosity illusions in capuchin monkeys (Sapajus
apella), rhesus macaques (Macaca mulatta), and humans
(Homo sapiens). Anim. Cogn. 22(5): 883–895.
Neotropical Primates 25(1), December 2019 73
Pereira Gonçalves, G. H., de Souza, J. C., da Silva, H.,
Rezende, A., Schmidt, F. et al. 2019. Hematological
and serum biochemistry data on southern brown howler
monkeys (Alouatta guariba clamitans) in captivity in Bra-
zil. J. Med. Primatol. 48(6): 313–319.
Power, M. L., Adams, J., Solonika, K., et al. 2019. Diet, di-
gestion and energy intake in captive common marmosets
(Callithrix jacchus): research and management implica-
tions. Sci. Rep. 9(1): 12134.
Price, E., Coleman, R., Ahsmann, J., Glendewar, G.,
Hunt, J., Smith, T. and Wormell, D. 2019. Individual,
social, and environmental factors aecting salivary and
fecal cortisol levels in captive pied tamarins (Saguinus bi-
color). Am. J. Prim. 81(8).
Riviere, J., Kurt, A. and Meunier, H. 2019. Choice under
risk of gain in Tufted Capuchin monkeys (Sapajus apella):
a comparison with young children (Homo sapiens) and
Mangabey monkeys (Cercocebus torquatus torquatus). J.
Neurosci. Psychol. E. 12(3–4): 159–168.
Rocha, P., Borges, P. A., De Agostini, S. J. D., Marcel, L.,
Blank, H., Nichi, M., Pereira, R. J. G. 2019. Assessment of
dierent sperm functional tests in goldenheaded lion tama-
rins (Leontopithecus chrysomelas). Am. J. Primatol. 81(8).
Salleng, K. J., Apple, T. M., Yu, E. N. Z. and Himmel, L. E.
2019. Spontaneous pulmonary adenocarcinoma and subcu-
taneous cavernous hemangiomas arising in a squirrel mon-
key (Saimiri sciureus). J. Med. Primatol. 48(6): 374–377.
Santos, E. R., Ferrari, S. F., Beltrão-Mendes, R. B., et al.
2019. Anointing with commercial insect repellent by
free-ranging Cebus capucinus in Manuel Antonio Nation-
al Park, Quepos, Costa Rica). Primates 60(6): 559–563.
Schrock, A. E., Leard, C., Lutz, M. C., Meyer, J. S. and
Paxton, R. 2019. Aggression and social support predict
longterm cortisol levels in captive tufted capuchin mon-
keys (Cebus [Sapajus] apella). Am. J. Primatol. 81(7).
Serrano-Villavicencio, J. E. and Silveira, L. F. 2019. Notes
on Lagothrix flavicauda (Primates: Atelidae): oldest
known specimen and the importance of the revisions of
museum specimens. Zoologia 36: e29951.
Snodderly, D. M., Ellis, K. M., Lieberman, S. R., Link, A.,
Fernandez-Duque, E. and Di Fiore, A. 2019. Initiation
of feeding by four sympatric Neotropical primates (At-
eles belzebuth, Lagothrix lagotricha poeppigii, Plecturocebus
(Callicebus) discolor, and Pithecia aequatorialis) in Ama-
zonian Ecuador: Relationships to photic and ecological
factors. Plos ONE.
Souza-Alves, J. P. and Mourthe, I. 2019. Terrestrial behav-
ior in Titi Monkeys (Callicebus, Cheracebus, and Plec-
turocebus): potential correlates, patterns, and dierences
between genera. Int. J. Primatol. 40: 553–572.
Takehara, S., Zeredo, J. L., Kumei, Y., Kagiyama, K., Fuka-
sawa, K., et al. 2019. Characterization of oral microbiota
in marmosets: Feasibility of using the marmoset as a hu-
man oral disease model. Plos ONE.
Vaughan, E., Le, A., Casey, M., Workman, K. P. and
Lacreuse, A. 2019. Baseline cortisol levels and social be-
havior dier as a function of handedness in marmosets
(Callithrix jacchus). Am. J. Primatol. 81(9).
Versace, E., Rogge, J. R., Shelton-May, N., et al. 2019. Po-
sitional encoding in cotton-top tamarins (Saguinus oedi-
pus). Anim. Cogn. 22(5): 825–838.
Walker, N. J., Schaer-Smith, D., Swenson, J. J., et al.
2019. Improved connectivity analysis using multiple
low-cost paths to evaluate habitat for the endangered San
Martin titi monkey (Plecturocebus oenanthe) in north-
central Peru. Landscape Ecol. 34(8): 1859–1875.
Wooldridge, L. M. and Kangas, B. D. 2019. An assay of
druginduced emesis in the squirrel monkey (Saimiri
sciureus). J. Med. Primatol. 48(4): 236–243.
Zürcher, Y., Willems, E. P. and Burkart, J. M. 2019. Are
dialects socially learned in marmoset monkeys? Evidence
from translocation experiments. Plos ONE.
M
PIMATE SOCIETY OF GREAT BRITAIN MEET
ING, SRING 2020
e PSGB Spring meeting is being hosted by Liverpool
John Moores University on the 23rd - 24th April, 2020. e
theme is Latest Advances in Primatology. Seehttps://www.
psgb-ljmu2020.co.uk/for further information.
43Rrd MEETING OF THE AMERICAN SOCIETY OF
PRIMATOLOGY
e 43rd meeting of the American Society of Primatologists
will be held in Denver, Colorado, May 28 - 31, 2020 at
the Sheraton Denver Downtown Hotel. Abstracts are due
January 21, 2020. For more info go to: https://asp.org/
meetings/conference.cfm
JOINT MEETING OF THE INTERNATIONAL
PRIMATOLOGICAL SOCIETY AND THE LATIN
AMERICAN SOCIETY OF PRIMATOLOGISTS
e 28th edition of the IPS congress and the IV congress
of the SLAPRIM will be held together in Quito, Ecuador,
from August 16 – 22th, 2020. For more information go to
https://ipsquito.com/registration/
Scope
e journal aims to provide a basis for conservation information
relating to the primates of the Neotropics. We welcome texts on any
aspect of primate conservation, including articles, thesis abstracts,
news items, recent events, recent publications, primatological society
information and suchlike.
Contributions
Manuscripts may be in English, Spanish or Portuguese, should be
prepared with MS Word, and must use page and line numbering. e
full name and address for each author should be included.
Please avoid abbreviations and acronyms without the name in
full. Authors whose rst language is not English should have their
manuscripts written in English carefully reviewed by a native speaker.
Send all contributions to BOTH: Erwin Palacios, Conservación
Internacional – Colombia, e-mail: epalacios@conservation.org and
to Jessica Ward Lynch, University of California, Los Angeles, email:
jlynchalfaro@g.ucla.edu. Manuscripts that do not conform to the
formal requirements (formatting, style of references, etc.) will be
returned to authors without review. ey can be resubmitted, provided
all formal requirements are met.
Articles. Each issue of Neotropical Primates will include up to three
full articles, limited to the following topics: Taxonomy, Systematics,
Genetics (when relevant for systematics and conservation), Bioge-
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exceed 25 pages in length (including references). Please include an
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or Portuguese) and (optional) one in Portuguese or Spanish (if the text
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Short articles. ese manuscripts are usually reviewed only by the
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activities that contribute to our understanding of platyrrhines. We
encourage reports on projects and conservation and research programs
(who, what, where, when, why, etc.) and most particularly information
on geographical distributions, locality records, and protected areas and
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reporting geographic coordinates please utilize one of the following
formats consistently throughout the manuscript: DMS (degrees,
minutes, seconds) 4°’36’19.1’’N, 74°3’20.7’’W or DD (Decimal
Degrees) 4.605306, -74.055750.
Tables. Tables should be double-spaced, using font size 10, and
prepared with MS Word. Each table should have a brief title.
News items. Please send us information on projects, eld
sites, courses, esis or Dissertations recently defended, recent
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References. Examples of house style may be found throughout this
journal. In-text citations should be rst ordered chronologically and
then in alphabetical order. For example, “…(Fritz, 1970; Albert,
1980, 2004; Oates, 1981; Roberts, 2000; Smith, 2000; Albert et al.,
2001)…”
In the list of references, the title of the article, name of the journal,
and editorial should be written in the same language as they were
published. All conjunctions and prepositions (i.e., “and”, “In”) should
be written in the same language as rest of the manuscript (i.e., “y” or
“e”, “En” or “Em”). is also applies for other text in references (such
as “PhD thesis”, “accessed” – see below). Please refer to these examples
when listing references:
Journal article
Stallings, J. D. and Mittermeier, R. A. 1983. e black-tailed
marmoset (Callithrix argentata melanura) recorded from Paraguay. Am.
J. Primatol. 4: 159–163.
Chapter in book
Brockelman, W. Y. and Ali, R. 1987. Methods of surveying and
sampling forest primate populations. In: Primate Conservation in
the Tropical Rain Forest, C. W. Marsh and R. A. Mittermeier (eds.),
pp.23–62. Alan R. Liss, New York.
Book
Napier, P. H. 1976. Catalogue of Primates in the British Museum
(Natural History). Part 1: Families Callitrichidae and Cebidae. British
Museum (Natural History), London.
esis/Dissertation
Wallace, R. B. 1998. e behavioural ecology of black spider monkeys
in north-eastern Bolivia. Doctoral thesis, University of Liverpool,
Liverpool, UK.
Report
Muckenhirn, N. A., Mortensen, B. K., Vessey, S., Fraser, C. E. O. and
Singh, B. 1975. Report on a primate survey in Guyana. Unpublished
report, Pan American Health Organization, Washington, DC.
Website
UNESCO. 2005. UNESCO Man and the Biosphere Programme.
United Nations Educational, Scientic, and Cultural Organisation
(UNESCO), Paris. Website: http://www.unesco.org/mab/index.htm.
Accessed 25 April 2005. (“Acessada em 25 de abril de 2005” and
“Consultado el 25 de abril de 2005” for articles in Portuguese and
Spanish respectively).
For references in Portuguese and Spanish:
“and” changes to “e” and “y” for articles in Portuguese and Spanish
respectively. “In” changes to “Em” and “En” for articles in Portuguese
and Spanish respectively.
“Doctoral thesis” changes to “Tese de Doutoramento” and “Tesis de
Doctorado” for articles in Portuguese and Spanish respectively.
“MSc esis” changes to “Dissertação de Mestrado” and “Tesis de
Maestría” for articles in Portuguese and Spanish respectively.
“Unpublished report” changes to “Relatório Técnico” and “Reporte
no publicado” for articles in Portuguese and Spanish respectively.
Notes to Contributors
Neotropical Primates
A Journal and Newsletter of the IUCN/SSC Primate Specialist Group
Vol. 25(1), December 2019
Contents
Articles
Demographic Dynamics of Peruvian Black-Faced Spider Monkeys (Ateles chamek)
Reintroduced in the Peruvian Amazon
Farah Carrasco-Rueda and Raúl Bello ........................................................................................................................................... 1
Prolonged Inter-Specific Association Between Ateles fusciceps fusciceps and Alouatta palliata aequatorialis
(Atelidae) in a Forest Fragment In North Western Ecuador
Paola Moscoso Rosero, Sam Shanee, Santiago Burneo, Nathalia Fuentes, Felipe Alfonso-Cortés, Martín Obando and Diego G. Tirira .... 11
Demography, Habitat Use and Activity Budget of A Wild Group of Black-Faced Black Spider Monkeys
(Ateles chamek) in Las Piedras, South-Eastern Perú
Liselot Roos Lange and Nicola Marie Robson ...............................................................................................................................21
Densidad Poblacional y Composición de Grupos de Aotus nancymaae en Áreas de Aprovechamiento
de la Especie para Experimentación Biomédica en el Trapecio Amazónico Colombiano
Néstor Roncancio-Duque, Mariela Osorno, Liza M. Calderón-Espitia, Amilvia Acosta-Castañeda,
Lina M. García-Loaiza, Natalia Gómez-Melendro and Beatriz E. Henao ......................................................................................30
First Records of Gastrointestinal Parasites in Woolly Monkeys (Lagothrix lagothricha)
in Colombia, from Wild, Captive and Reintroduced Individuals
Camilo Quiroga-González, Elisa Jiménez, Nelson F. Galvis, Mónica A. Ramírez, Mario Ortiz,
Camila Gonzalez and Pablo R. Stevenson ................................................................................................................................... 38
Short Articles
Fur Rubbing Behaviour in Free Ranging Beni Titi Monkeys (Plecturocebus modestus) in Bolivia
Jesús Martínez, Freddy Zenteno-Ruiz, Laura Moya, Pamela Carvajal and Robert Wallace ................................................................44
Geographical and Altitudinal Range Extension of White-Bellied Spider Monkeys (Ateles belzebuth)
in the Northern Andes of Colombia
Victoria Andrea Barrera, Camila Valdés Cardona, Luisa Mesa, Sebastian Nossa and Andrés Link .....................................................48
Primer Registro de Pithecia milleri (Allen, 1914) en la Baja Bota Caucana, Corregimiento de
Miraflor, Municipio de Piamonte, Cauca
Laura Suárez and Hugo Mantilla-Meluk .................................................................................................................................... 53
Evidence of Opossum (Didelphis sp.) Predation by White-Fronted Capuchins (Cebus yuracus) in the
Copallín Private Conservation Area, Amazonas, Perú
Karen Pedersen, Sam Shanee and Christian Miguel Olivera Tarifeño .............................................................................................. 54
Ampliación del Área de Distribución del Mono Maicero Cachón (Sapajus apella): Nuevo Registro en
el Parque Nacional Natural Las Hermosas-GVC, Tolima, Colombia
Pablo Paya, Jesús-A Sánchez-C., Carolina Guzmán-V., Germán Rodríguez-P. and Néstor Roncancio-D. ............................................57
News ......................................................................................................................................................................................59
Obituaries ..............................................................................................................................................................................61
Recent Publications ...............................................................................................................................................................70
Meetings ................................................................................................................................................................................73
