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Title: Neotropical primates
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 Material Information
Title: Neotropical primates a newsletter of the Neotropical Section of the IUCNSSC Primate Specialist Group
Abbreviated Title: Neotrop. primates
Physical Description: v. : ill. ; 27 cm.
Language: English
Creator: IUCN/SSC Primate Specialist Group -- Neotropical Section
IUCN/SSC Primate Specialist Group -- Neotropical Section
Conservation International
Center for Applied Biodiversity Science
Publisher: Conservation International
Place of Publication: Belo Horizonte Minas Gerais Brazil
Belo Horizonte Minas Gerais Brazil
Publication Date: June 2009
Frequency: quarterly
regular
 Subjects
Subject: Primates -- Periodicals -- Latin America   ( lcsh )
Primates -- Periodicals   ( lcsh )
Wildlife conservation -- Periodicals   ( lcsh )
Genre: review   ( marcgt )
periodical   ( marcgt )
Spatial Coverage: Brazil
 Notes
Additional Physical Form: Also issued online.
Language: English, Portuguese, and Spanish.
Dates or Sequential Designation: Vol. 1, no. 1 (Mar. 1993)-
Issuing Body: Issued jointly with Center for Applied Biodiversity Science, <Dec. 2004->
General Note: Published in Washington, D.C., Dec. 1999-Apr. 2005 , Arlington, VA, Aug. 2005-
General Note: Latest issue consulted: Vol. 13, no. 1 (Apr. 2005).
 Record Information
Bibliographic ID: UF00098814
Volume ID: VID00057
Source Institution: University of Florida
Holding Location: University of Florida
Rights Management: All rights reserved by the source institution and holding location.
Resource Identifier: oclc - 28561619
lccn - 96648813
issn - 1413-4705

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Table of Contents
    Front Cover
        Front Cover
    Copyright
        Copyright
    Main
        Page 1
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        Page 3
        Page 4
        Page 5
        Page 6
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        Page 8
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        Page 23
        Page 24
        Page 25
        Page 26
        Page 27
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        Page 48
        Page 49
        Page 50
    Back Matter
        Back Matter 1
        Back Matter 2
        Back Matter 3
    Back Cover
        Back Cover
Full Text








Neotropical Primates
A Journal of the Neotropical Section of the IUCN/SSC Primate Specialist Group


Center for Applied Biodiversity Science
Conservation International
2011 Crystal Drive, Suite 500, Arlington, VA 22202, USA

ISSN 1413-4703 Abbreviation: Neotrop. Primates

Editors
Erwin Palacios, Conservaci6n Internacional Colombia, Bogoti DC, Colombia
Liliana Cort6s Ortiz, Museum of Zoology, University of Michigan, Ann Arbor, MI, USA
J6lio Cesar Bicca-Marques, Pontificia Universidade Cat61lica do Rio Grande do Sul, Porto Alegre, Brasil
Eckhard Heymann, Deutsches Primatenzentrum, Gbttingen, Germany
Jessica Lynch Alfaro, Washington State University, Pullman, WA, USA
Liza Veiga, Museu Paraense Emflio Goeldi, Belkm, Brazil
News and Books Reviews
Brenda Sol6rzano, Instituto de Neuroetologfa, UniversidadVeracruzana, Xalapa, M6xico
Ernesto Rodrfguez-Luna, Instituto de Neuroetologfa, Universidad Veracruzana, Xalapa, Mexico

Founding Editors
Anthony B. Rylands, Center for Applied Biodiversity Science Conservation International, Arlington VA, USA
Ernesto Rodrfguez-Luna, Instituto de Neuroetologia, Universidad Veracruzana, Xalapa, M6xico
Editorial Board
Hannah M. Buchanan-Smith, University of Stirling, Stirling, Scotland, UK
Adelmar E Coimbra-Filho, Academia Brasileira de Cidncias, Rio de Janeiro, Brazil
Carolyn M. Crockett, Regional Primate Research Center, University of Washington, Seattle, WA, USA
Stephen E Ferrari, Universidade Federal do Sergipe, Aracaj6, Brazil
Russell A. Mittermeier, Conservation International, Arlington, VA, USA
Marta D. Mudry, Universidad de Buenos Aires, Argentina
Horicio Schneider, Universidade Federal do Pari, Campus Universitirio de Braganya, Brazil
Karen B. Strier, University of Wisconsin, Madison, WI, USA
Maria Emflia Yamamoto, Universidade Federal do Rio Grande do Norte, Natal, Brazil
Primate Specialist Group
Chairman, Russell A. Mittermeier
Deputy Chair, Anthony B. Rylands
Coordinator, Special Section on Great Apes, Liz Williamson
Regional Coordinators Neotropics
Mesoamerica, Ernesto Rodriguez Luna
Andean Countries, Erwin Palacios and Eckhard W. Heymann
Brazil and the Guianas, M. Cecilia M. Kierulff
Regional Coordinators Africa
West Africa, John F. Oates
East Africa, David Mbora
Regional Coordinator Madagascar
Jarg U. Ganzhorn
Regional Coordinators Asia
China, Long Yongcheng
Southeast Asia, Jatna Supriatna and Christian Roos
South Asia, Sally Walker



Layout: Kim Meek, Washington, DC

IUCN/SSC Primate Specialist Group logo courtesy of Stephen D. Nash, 2002.

Front cover: Callimico clinging to vertical support at Camp Callimico, Department of Pando, Bolivia. Photo by Edilio Nacimento Becerra.


This 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 16(1), June 2009 1





DEVELOPMENTAL STAGES IN THE HOWLER MONKEY, SUBSPECIES ALOUATTA PALLIATA
MEXICANA: A NEW CLASSIFICATION USING AGE-SEX CATEGORIES

Cristina Domingo Balcells1, Joaquim Jose Veai Bar61


'Centre Especial de Recerca en Primats. Universitat de Barcelona. Gran Via de les Corts Catalanes, Barcelona, Spain.
cdbalcells@atmacaucho. corn

Abstract

We present a new classification of age-sex categories for the mantled howler monkey Alouatta palliata. This classification
includes only those physical and behavioral characteristics that can be distinguished under field conditions, with the goal
of being able to infer the approximate age of monkeys in the wild. Our classification is based on data collected ad libitum
during monthly censuses of 8 groups of A. p. mexicana in a fragmented landscape on the "Los Tuxtlas" Biosphere Reserve at
the northern limit of this species' distribution. Our new classification system contains 10 categories that can be compared
directly to existing classification schemes to facilitate cross-site studies. We compare the results of our study to the currently
used classification system which was based on more southern populations of A. palliata in Panami and Costa Rica.

Key Words: Age-sex categories, A. palliata


Resumen

Presentamos una nueva clasificaci6n de categories de edad-sexo para los monos aulladores Alouattapalliata. Esta clasificaci6n
incluye solamente aquellas caracteristicas fisicas y comportamentales que pueden ser distinguidas en condiciones de campo,
con el prop6sito de poder inferir la edad aproximada de los monos en estado silvestre. Nuestra clasificaci6n esti basada en
datos colectados ad libitum durante censos mensuales de 8 grupos de A. p. mexicana en un paisaje fragmentado el la Reserva
de la Bi6sfera "Los Tuxtlas" en el limited norte de distribuci6n de esta especie. Nuestro nuevo sistema de clasificaci6n contiene
10 categories que pueden ser comparadas directamente con esquemas de clasificaci6n existentes para facilitar lo studios de
diferentes sitios. Comparamos los resultados de nuestro studio con el sistema de clasificaci6n actualmente utilizado el cual
se basaba en poblaciones de A. palliata mias surefias en Panami y Costa Rica.


Palabras Clave: Categorias sexo-edad, A. palliata


Introduction

The study of ontogeny is essential to evolutionary anthro-
pology and primatology since it allows for the compari-
son of developmental and growth strategies among species.
Within a given species, establishing life stages allows one
to understand the degree of variability in the development
and maturation patterns found in different populations
(Neville et al., 1988). Furthermore, for a wide range of
primatological studies it is crucial to be able to determine
the main developmental stages of the individuals of a spe-
cies and estimate their age based on their characteristics.
For this purpose, the sequence of dental eruption and the
length of the long bones are considered to provide the most
accurate information (baboons: Phillips-Conroy and Jolly,
1988; howlers: DeGusta and Milton 1998; De Gusta et al.,
2003; vervet monkeys: Bolter and Zihlman, 2003; chim-
panzees: Zihlman etal., 2004). However, for the analysis of
hard tissue it is necessary to examine the individual directly


and in the majority of field studies this may not be feasible,
may be costly, or may even be harmful to the primates. As
such, standardized classifications for each species are useful
as they allow the ages of the individuals and their develop-
mental stage to be estimated based only on morphological
and behavioral characteristics that are observable from a
certain distance.

In demographic and ethological studies these classifica-
tions can be used to describe the group composition, age
at sexual maturity or migration, morphological and be-
havioral changes associated with these processes or to ex-
amine the influence of ecological constraints on the differ-
ent developmental stages in a primate population (Bolter
and Zihlman, 2003). On the other hand, depending on
the physical and behavioral criteria that are applied, the
assessment of these stages can vary within a species or even
within a population (Bramblett, 1980). Additionally, ge-
netic variation within and between populations has been





Neotropical Primates 16(1), June 2009


frequently identified as a cause of differences in the devel-
opment of individuals (Arendt, 1997). The habitat niche
can also modify the growth and development pattern of
different populations of the same species (Bolter and Zihl-
man, 2003). Geographic variation as well as altitudinal
and latitudinal, temperature and precipitation gradients,
often create genetic lines in growth and development
rates (Arendt, 1997). In contrast, when and how to grow,
mature and reproduce depend on the state of the organ-
ism, including its physiological condition and the asso-
ciated ecological costs (Gotthard, 2001), which in turn
depend on the environment, the risks of predation and
resource availability.

For the mantled howler monkey (Alouatta palliata) there
are few published classifications that define developmen-
tal stages by age based on observable characteristics. The
most used systems differentiate between immature in-
dividuals and adults, or between a few different stages
of development (Table 1) and are based on data for the
southern populations of howlers from Barro Colorado
Island (BCI), Panami (Carpenter, 1934, 1965) and from
Costa Rica (Glander, 1980; Clarke, 1990). These classifi-
cations have been used extensively to classify wild howler
monkeys by their age throughout their wide distribution.
Mantled howlers are found from southern Mexico through
Central America and part of Colombia and Ecuador. De-
spite being one of the most studied New World primate
genera, Alouatta species' systematic relationships remain
unclear (Cortes-Ortiz et al., 2003), and subsequently, it is
unknown whether this genetic differentiation has any in-
fluence on the development of individuals or the relation


between age and external changes. Here we present a new
system of classification in age-sex categories for the man-
tled howler monkey in its most northern distribution, in
the region of Los Tuxtlas, Mexico. We compare and dis-
cuss our results with the current classification systems from
Panami and Costa Rica.

Methods

Study site
This study was carried out in a fragmented landscape of
disturbed tropical rainforest, located in southern Veracruz,
Mexico. The area is within the buffer zone of the Los Tuxtlas
Biosphere Reserve (18034', 1837'N and 95002', 9508'W;
elevation in the study area: 25-400 m a.s.1.). The climate
is warm and humid (Soto and Gama, 1997) with a mean
annual temperature of 250 C and annual precipitation of
4710 mm (EBT, Los Tuxtlas Biology Station, 1996-2005).
The dry season occurs from January or February to May
and the rainy season is from June to December or Janu-
ary (EBT, 1996-2005), with strong winds from the north
from November to February (Soto and Gama, 1997). Cur-
rently, there are no large predators, such as jaguar or harpy
eagle, in the zone, although there have been reports of at-
tempted attacks by tayra on a troop of howlers (Asensio
and G6mez-Marin, 2002).

Data col(eIt, .ou
Eight groups of howler monkeys were monitored over a
total of 23 non-consecutive months in daily sessions of 6 to
8 hours starting at sunrise. Each group was visited several
times each month to ensure reliable observations. Data


Table 1. Classification of A. palliata by age-sex category.
Class Carpenter, 1934a Carpenter,1965b Glander,1980c Clarke,1990'
Infant 1 < 1 mo 0-5/6 mo < 2 days 0-3 mo
Infant 2 6 mo 5/6-10/12 mo 2-21 days 3-6 mo
Infant 3 12 mo 10/12-18/20 mo 21-90 days 6-12 mo
Juvenile 1 18 mo 20-30 mo 3-6 mo 12-20 mo
Juvenile 2 21 mo 30-40 mo 6-30 mo 20-36 mo
Juvenile 3 36 mo 40-50 mo
Subadult female 30-48 mo
Subadult male 30-48 mo
Adult female >50 mo >48 mo (first birth approx. >34-36 mo sexually mature
43 mo)
Adult male >50 mo >48 mo >36-40 mo sexually mature
Characteristics Estimated weight, hair Estimated weight, hair Weight, genitalia, hair, Travel, relation to mother
taken into color, relation to mother, color, relation to mother, transport and non-mother, play
account play play
Methods Observations in the wild Modified data from 1934. Discontinuous observa- Observations of 6 females
(approx. 8 months) and in tions of one group from and 5 males over 22
captivity (n= 3). Collections 1970-78. Capture (weight, months, focused on social-
(n 4). measures, palpation). ization patterns between
sexes.
Subspecies A. palliata aequatorialis. Data from Barro Colorado Island (BCI), Panama (98 N, 7949 W), tropical rain forest.
, d Subspecies A. palliata palliata. Data from La Pacifica, Costa Rica (1028 N, 8507 W), dry tropical deciduous forest.







Neotropical Primates 16(1), June 2009


were collected from October 2003 to November 2005 by

two teams, each with a researcher and a field assistant, who

made every effort to apply homogeneous criteria, as de-

scribed below. At the beginning of the study there were

a total of 20 immature in the eight groups and over the

observation period there were 20 births that could be as-

signed to a specific month. All the animals observed were

individually recognized by their natural markings typical of

the subspecies. Their identification cards were kept up-to-

date throughout the study, and complemented with draw-

ings, photographs and videos. To follow individual devel-

opment, during each session the observation date and the

particular characteristics of the individual at that moment

were recorded on each card ad libitum. Most of the mor-

phological and behavioral characteristics used in previously

established classification systems were included. Morphol-

ogy: color and length of fur, relative body structure and size,

appearance of the genitals, head shape. Behavior: relation-

ship with the mother, presence/absence of sexual behavior,

type of locomotion, feeding and play. The characteristics

are listed in Table 2 of the Results section.



Estimating the age corresponding to dtf r':'r developmental

stages in howlers

Once the field work had been completed, "time lines" were

drawn for each individual that was born during the study

and therefore of known age. We call the representation of

the age in months of each monkey its "time line", and used

these together with morphological and behavioral changes


Infant 1

1: : -


4:


7: -


10 :


13 :


16 :


19


22 :


25 -:

28 --


31 "

34 :-


37 --.


40 -.


Infant 2
:-- - -


that occurred as the study progressed to describe each stage.

Using the characteristics recorded, a life stage was assigned

to each individual for each observation, applying each of

the existing classification systems presented in Table 1. This

made it possible to compare the degree of agreement be-

tween these classification systems with respect to the as-

signed stage and in comparison with the animal's real age.

Owing to discrepancies detected, the classifications were

modified and a new one was created that homogenized

the criteria and fit the data of our study. Then, this new

system was used to estimate the age of the 20 immature

that were present in the first census of the study. Using

our pilot classification system, the life stage was assigned

to each individual for each observation based solely on the

animal's characteristics. In one column the age range esti-

mated using this classification was noted, and in another

column the age range estimated at the first observation of

the individual according to its characteristics was noted,

and to this age we added the elapsed months for the sub-

sequent observations. Finally, agreement between the col-

umns was compared to test whether the classification and

the estimated ages fit. Applying this method systematically,

we were able to estimate the age ranges for the life stages

leading up to maturity.



Results



Using the time lines, we present the development of the

40 immature studied (Fig. 1). The category corresponding


Infant 3 I Juvenile 1 Juvenile 2


=-- - - ------ ------ ----


I - - - - - - - - --1 -


-- ------ -- ----


4 $ 4


4i. . . . . .. .a . . . A. . ... . ..4. . . .


0 4


8 12 16


24 28 32 36


Age (months)


Figure 1. Time lines for the 40 immature individuals studied (see text). The category corresponding to the age in months is shown for each
individual, applying the classification scheme proposed in this study. Time lines starting at zero (individuals 21-40) correspond to the
20 individuals that were born during the observation period. Lines 1-20 represent immature already present at the beginning of the study.


Subadult


----------- -------- ; --- ---- --------
---------- itPi -------------------------


-----------------------------
-----------------------------
I
-----------------------------
-----------------------------
-----------------------------
.............................
-----------------------------
-----------------------------
-----------------------------
---------- -----------------
---------- -----------------
---------- -----------------
---------- -----------------

---------- -----------------
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.......... .................
---------- -----------------
---------- -----------------
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---------- -----------------
---------- -----------------
---------- -----------------


I
--------------- ------------


]


Juv 3
----------
----------


f


l


---------------
---------------
---------------
---------------
---------------
---------------
---------------
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...............
---------------
---------------
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---------------
---------------
---------------
---------------

---------------
---------------
...............
---------------
---------------
---------------
---------------
. ............


------------
------- r! ---
------------
------------
------------
............
------------
------------
------------
------------
------------
------------
------------

------------
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............
------------
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------------
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----------

............
------------
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--------------
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..............
--------------
--------------
--------------
--------------
--------------
--------------
--------------

--------------
--------------
P..............
--------------
I!n -----------





Neotropical Primates 16(1), June 2009


Table 2. Age-sex classification of the Los Tuxtlas howler monkeys (Alouatta palliata mexicana).
Class Infant 1 Infant 2 Infant 3
Age 0-2/3 3/4-7/8 8/9-13/14
(months)
Morphology Very short silvery gray coat, changing Short gray-brown to dark brown fur. Short brown fur, no mantle or beard.
to yellowish to light brown. Extremities No mantle. Body proportional to
and head proportionally more devel- extremities.
oped than the body.
Locomotion Carried ventrally by the mother during Carried dorsally by the mother or Carried dorsally by the mother during
and relation locomotion, sometimes dorsally. During sporadically ventrally during locomo- long or difficult locomotion and also
with mother rest, may try to explore surroundings tion (especially during rest or during alone, following the mother, becoming
very close to its mother without letting short movements by the mother when more independent about own locomo-
go of her. she gets up while the baby is feeding or tion which is quick and abrupt. When
during suspensory locomotion.) Rests on the mother's back, the baby on the
with the mother and starts to explore base of her tail and tends to wrap its tail
nearby surroundings alone, but stays around hers. Rests with the mother.
close to the mother.
Feeding Only suckles. Suckles and towards the end of this Suckles, but eats increasingly more solid
stage begins to try solid food (at approx. food as it grows.
6-8 months).
Other Other females and juveniles show Begins to play with other infants and Plays much of the time and is generally
behaviors interest in these infants. Sporadically juveniles, always in close proximity to tolerated by adult males.
allomaternal behavior can be observed, its mother.
with the baby being carried by other
individuals.


Table 2. cont'd. Age-sex classification of the Los Tuxtlas howler monkeys (Alouattapalliata mexicana).
Class Juvenile 1 Juvenile 2 Juvenile 3
Age 14/15-19/20 20/21-24/25 25/26-28/29 *
(months)
Morphology Coat similar to that of the adult in Fur similar to that of the adult in color, Fur similar to that of a young female
color, but shorter, particularly on but slightly shorter, particularly on the adult in length and color. Slightly
the head and sides of the body. Light head and sides of the body. Mantle smaller than subadult and adult females
colored fur on the sides, but without developing; fur light colored and longer and easily confused with same in the
long fringes. No beard and no fur on on the sides. Larger in size than Juvenile field. Sex organs not clearly visible.
the sides of the face, giving the head 1 and the body is longer, and its shape
the shape of a small triangle. Body more defined.
lengthening.
Locomotion Generally rests in contact with or near Independent adult locomotion. At the Independent adult locomotion. It is
and relation the mother. Independent, quick, agile beginning of this stage juveniles may impossible to know who the juvenile's
with mother locomotion; often follows the mother stay near a female (the mother), but do mother is.
when the troop moves as a unit. not generally rest in contact with her.
At the end of this stage it is difficult to
know who the juvenile's mother is.
Feeding Still suckles when the mother is resting, No longer suckles, only forages. Adult feeding habits.
but eats mainly solids when the group
is foraging.
Other Plays a lot with other immatures. Gen- Emigration stage**. Often elusive Final emigrations **. Often elusive
behaviors erally very well tolerated by adult males solitaries. If this juvenile remains in solitaries. Is totally independent if it
and can play with them. Stage at which the group, it is very independent. Still stays in the group. Still actively plays
the emigrations begin **. actively plays with other individuals of with other individuals of its cohort and
its cohort and with infants. with infants.
* The age limit probably depends on the sex of the individual.
** See text for more details.
*** As estimated by other authors (see Table 1), no precise data from this study.





Neotropical Primates 16(1), June 2009


Table 2. cont'd. Age-sex classification of the Los Tuxtlas howler monkeys (Alouattapalliata mexicana).
Class Subadult female Subadult male 3 Adult female Adult male
Age (months) 28/29-35 31/32 to 48 months, >36/40 >48
approx. ***
Morphology Adult coat, with a long Adult coat, with mantle. Dark brown coat, hair Dark brown coat, hair
light colored mantle. Secondary sex characteristics longer around the face with longer around the face
Juvenile in appearance. Hair developing: beard, lengthen- a long light colored mantle. with a long light colored
around face a little shorter ing and slight partitioning Full size. More robust than mantle. Full size. Second-
than that of adult females of head, testicles begin to previous stages. ary sex characteristics fully
and, in general, the face descend and the scrotum developed. Scrotum fully
is smoother and rounder changes from black to white pendulous and white, some-
than that of adults. Slightly with many black spots. times still has the remains of
smaller in size than a fully 31/32 months (scrotum not some black spots.
adult female, confusable pendulous and genital area
with a stage 3 juvenile, but black, but with the definite
the vulva is clearly visible, profile of a male).
although small and closed.
Locomotion Independent. Independent. Independent. Independent.
Feeding Adult feeding habits. Adult feeding habits. Adult feeding habits. Adult feeding habits.
Other behaviors Usually elusive solitaries. If Often elusive and solitary. First estrus and copulation Alone or with the group.
they stay in the group they Begins to howl at the end of at approximately 35 months Howling. Actively copulates
play actively and appear to this stage when the testicles old, and first birth at 41 when he has access to
have a low hierarchical rank. have descended. months ** (considering: females. Threatening behav-
They do not copulate. approximately 6 months for ior such as standing on his
Nulliparous. gestation). hind legs and arches body.
Occasionally fights with
other males.
* The age limit probably depends on the sex of the individual.
** See text for more details.
*** As estimated by other authors (see Table 1), no precise data from this study.


to the age in months is shown for each individual through-
out the study, from the first observation to end of the last
observation at the end of the study or when the animal
disappeared, either because it died or emigrated. To sim-
plify interpretation, adult categories are not included in the
figure and the time lines are drawn as continuous, even
though all individuals were not observed during all the
months (e.g. sample gaps or emigration-immigration events,
see Balcells, 2008 for further details on the groups and in-
dividuals history). The complete classification by age-sex
categories fit to our Los Tuxtlas population is summarized
in Table 2 where the distinguishing characteristics for each
stage and the estimated age range are listed. The classifi-
cation we propose is constructed based on those listed in
Table 1. There are 10 categories; more than those proposed
by other authors, but they can easily be grouped together
when required because of the data or the study. We suggest
that the maximum number of categories be used to obtain
a more accurate estimate of age based on characteristics
that are easy to record in the field over a reasonable amount
of observation time. On the other hand, any classification
of a continuous temporal process is arbitrary and because
of this, under field conditions we frequently find individu-
als that are difficult to assign to one or another of two adja-
cent categories; these i-ii transition stages (e.g. Infant 2-3)
can be read in Table 2 as n/n+ 1.


Some important behavioral events in the lives of primates
are of interest when comparing individual's age with ex-
ternal appearance. Howlers usually leave their natal group
before reaching maturity (Glander, 1992). Accordingly,
there is notable migratory activity in our study population
at the group level (Balcells, 2008), and the individuals in
the juvenile and subadult categories are often solitary and
secretive. In Los Tuxtlas natal emigration generally occurs
when the sex of the individual is not externally detect-
able under field conditions (see also Clarke et al., 2007,
for evidence of juvenile monomorphism in A. palliata).
As such any difference in migration age and behavior be-
tween the sexes is not easily distinguishable without later
long term follow-up. During our study, we were able to
observe only two individuals and determine their sex after
they had emigrated. Individual 10 (Fig. 1) returned to
his group and was identified as a Subadult male (accord-
ing to our classification system), having abandoned the
group at 27-29 months of age. Individual 15 emigrated
at 20-22 months old and later was identified as a small
solitary Subadult female behaving evasively. Our data sug-
gest that emigration can occur in any of the three juvenile
stages (25% Juvenile 1, 37.5% Juvenile 2 and 37.5% Juve-
nile 3, n=8 observed disappearances of immatures in age
of non-dependency from mother) and 3 to 4 of the migra-
tions coincided with the birth of a sibling.





Neotropical Primates 16(1), June 2009


In addition to migration, weaning and first reproduction
are also key periods in the lives of howlers. During our
study, we were only able to infer the age of one female
(individual 19, Fig.1) when she first gave birth, at between
39 and 42 months of age; as calculated for a gestation
period of 6 months (Cortes-Ortiz et al., 1993; Glander,
1980), and that first estrus and copulations occur at around
35 months. For males, the beginning of reproductive ac-
tivity probably depends on social aspects that give them
access to the females, but during our study we were not
able to observe this process. With respect to feeding, com-
plete weaning in Los Tuxtlas was observed at the end of the
Juvenile 1 stage, at 18-20 months of age. It is common to
observe a Juvenile 1 (from 15 to 19 months old) still suck-
ling opportunistically when the mother is resting, although
during this stage it appears that individuals are no longer
dependent on their mother for food, because they can sur-
vive as solitaries and some individuals leave the natal group
before reaching 15 months of age.

Discussion

Comparison of classification systems
The classification systems analyzed here for age-sex cat-
egories of Alouatta palliata coincide with each other to
differing degrees. On the one hand, Carpenter's (1965)
classes have wide age ranges and very advanced ages for
the accompanying physical and behavioral characteristics
when compared with other systems, including the one we
propose for Los Tuxtlas and an earlier one by the same
author from 1934. The age assigned for individuals with
similar characteristics can differ by as much as 15 months,
in spite of being classified as the same morphological stage
(e.g. Juvenile 1 is 3-6 months old according to Glander,
1980 and 20-30 months according to Carpenter, 1965).
Glander (1980) also proposes a wide range of ages for Ju-
venile 2 (6-30 months), that would include Carpenter's
(1934) Juvenile 1 and 2 stages (in both characteristics and
age), and from the end of Infant 3 to Juvenile 3 for the
system we propose for Los Tuxtlas. In general, our clas-
sification system is similar, with certain differences, to the
systems of Carpenter (1934) and Clarke (1990). Carpen-
ter (1934) classifies as Juvenile 3 those individuals with
characteristics similar to those of the Subadult stage in the
Los Tuxtlas classification system. Clarke's (1990) classifi-
cation proposes age ranges that are very similar to those
of our system, although she assigns an age of 20 to 36
months to Juvenile 2, and includes individuals that we
would classify as Juvenile 3 and Subadult in this stage.
However, for some studies it might be interesting to dif-
ferentiate between individuals that begin to exhibit sexual
traits and the juveniles that do not yet show any external
evidence of their sexual identity given that these stages
are associated with physiological and social changes. Addi-
tionally, differentiating between these stages allows a closer
fit to the estimated range of ages for the individuals in the
pre-maturation stages that are critical to group dynamics
(Glander, 1992).


As regards key events during the development of howler
monkeys, there is greater consensus. From our data, sexual
maturity in females occurs at approximately 36 months
and the first birth occurs at 43 months. This agrees with
reports by Glander (1980) and Clarke (1990). Accord-
ing to Clarke (1990) weaning occurs during Juvenile 1
(18 months) in females, while males become independent
earlier, both in locomotion and feeding. Carpenter (1934)
agrees with this, and although in 1965 he said weaning
occurs during Juvenile 1, a much older age is assigned
(20-30 months). Glander (1980) does not specify any age
for weaning. In Los Tuxtlas, complete weaning was ob-
served at the end of Juvenile 1, at 18-20 months old when
individuals can emigrate and survive without suckling,
and this coincides with the findings of Carpenter (1934)
and Clarke (1990). Finally, the emigration age in males is
12-20 months according to Clarke (1990), while females
emigrate at 22-24 months. Our data suggest that the birth
of a sibling is an important factor for triggering emigration,
and emigration tends to occur before the sex of the indi-
vidual can be identified and so any difference associated
with the sex of the individual is difficult to discern at the
time of emigration. More data are required to determine
whether there are differences between the sexes or individu-
als in emigration age, and to broaden our understanding
of the factors that might produce any differences observed.

Genetics, environment and development
Although growth rates are genetically imprinted, they are
phenotypically plastic (Laurila etal., 2001), and a function
of the adaptive balance between the costs and benefits as-
sociated with development (Gotthard, 2001). In two pop-
ulations of captive macaques, differences were found in
growth rates that could be attributed to their different ori-
gins, the different climates of the centers, different social
structure or genetic profile (Vancata et al., 2000). Also, in
langurs the socio-ecology of the species interacts with its
development patterns (Washburn, 1942). In baboons, as
a result of improved nutrition, growth rate varies among
groups during the same year and for the same group in dif-
ferent years (Strum, 2005). In vervets, reproductive ma-
turity is early compared to that of baboons and is consid-
ered an adaptation to unpredictable food sources (Rowell,
1977). On the other hand, the early consumption of solid
food in indris could reduce maternal investment (Godfrey
et al., 2004). However, in some Platyrrhini (Aotus, Cal-
licebus, Saimiri, Callimico, Saguinus, Leontopithecus, Ce-
builla and C .- ecological and social factors, such
as predation and competition for food do not appear to
adequately explain the differences observed in infant de-
velopment and growth rates (Garber and Leigh, 1997).
In howlers, the lack of consistency in the age classifica-
tions within each geographic area prevents us from assert-
ing that environmental differences significantly affect the
development strategies of the populations. Although the
forage available to the different populations studied might
offer differing nutritional value owing to differences in
habitat and vegetation (Table 1), this factor probably does





Neotropical Primates 16(1), June 2009


not have a significant influence on development (at least
for field observations). Howler monkeys can restrict their
energetic expenditure behaviorally (Milton, 1980) and,
owing to their highly folivore and generalized diet, are ca-
pable of using different resources, even in disturbed habi-
tats (Rodriguez-Luna et al., 2003; Cristobal and Arroyo,
2007). For the same reason, the effects of intra- or inter-
specific competition in habitats with limited resources are
mitigated (Van Schaik, 1989).

On the other hand, howler monkeys are not subject to
severe predation pressure in any of the study sites because
of their large size and the decrease in the populations of
potential predators; hence this factor is also not likely to
exert a significant influence at present. Finally, latitude
does not appear to have an important effect on the rate
of development of A. palliata, given that there are no con-
sistent differences between the Mexican and more south-
ern populations, in spite of the fact that latitude might
be important in fish and amphibians (Duponchelle and
Legendre, 2000). It is, however, worth mentioning that in
a study using 7 microsatellites for different populations of
A. palliata in Mesoamerica, Cortes-Ortiz (2003) found a
marked decrease in the genetic variation of the populations
from south to north where A. p. mexicana (from Mexico)
was the least variable population, followed by A. p. palliata
(from Costa Rica), and the population of A. p. aequetoria-
lis (from Panama) had the greatest variation. Even though
populations of A. p. mexicana do not appear to be facing
any detrimental effects owing to the reduction in the ge-
netic variation, this fact could cause differences between
populations and should be considered when making com-
parisons between different populations (subspecies). The
incorporation of molecular data in demographic-behavior-
al studies of different populations would help to reveal the
effect of the loss of genetic variation in the ontogenetic
development of howler monkeys.

The consequences of using d e/ft '':: criteria
According to Neville et al. (1988), the use of different cri-
teria for classifying wild Alouatta palliata individuals can
interfere with the comparison and interpretation of the re-
sults obtained by different authors over a wide variety of
studies. In demographic studies, not considering subadults
as a separate class could result in an underestimation of
the number of juveniles or reproductive adults in the cen-
suses. Similarly, certain individuals would be considered as
infants or juveniles depending on the classification system.
Therefore, it is necessary to keep in mind which classifica-
tion system has been applied to evaluate the evolution of
populations for censuses that use the number ofimmatures
per reproductive female (Heltne et al., 1976). Even purely
behavioral and socio-ecological studies (e.g. daily activity
pattern, diet, play, socialization) that use distinct age classi-
fications to compare behavior patterns between categories of
individuals can lead to contradictory conclusions as a result
of the criteria applied. The same problem occurs in studies
for which it is necessary to infer the age of the individuals


in order to prepare life tables, evaluate relative mortality for
each stage and age, infer the birth month of the individuals,
time of weaning, reproduction or migration.

Our results indicate the need to unify the criteria for classi-
fication by age-sex categories for mantled howler monkeys,
and to identify consistent differences between populations
with different characteristics. Further long term studies are
needed in Los Tuxtlas, Mexico and the other places where
this species is found.

Acknowledgements

We are grateful to B. Hervier and S. Vegas for providing
data and to C. P&rez for participating in long hours of field
work. We thank the Los Tuxtlas Biological Station-UNAM
for climate information. For valuable comments on a
previous version of the manuscript we thank L. Cortes-
Ortiz, P.A.D. Dias and J. Crist6bal-Azkarate. CD Balcells
was supported by Floquet de Neu scholarship 1S ed. and
from the Ministry of External Affairs in Mexico. For infra-
structure support we thank the Ministry of Education and
Science of Spain BSO02002-03340 and SESJ2005 1562/
PSIC, and E. Rodriguez-Luna of Universidad Veracruzana,
Mexico. The research complied with protocols approved
by the appropriate institutional animal care committee
of SEMARNAT-the Mexican Office for the Environment
and Natural Resources, and adhered to the legal require-
ments of Mexico.

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Neotropical Primates 16(1), June 2009


TRUNK-TO-TRUNK LEAPING IN WILD CALLIMICO GOELDII IN NORTHERN BOLIVIA

Paul A. Garber1 and Leila M. Porter2

1Department ofA_ .--' .. :.'.i.' 109 Davenport Hall, 607 S. Mathews Ave, Urbana, Illinois, 61801, USA /- .
2Department ofA .-' ..:.. '.:. Northern Illinois University, Dekalb, Illinois, USA


Abstract

Compared to other species of tamarins and marmosets, callimicos (Callimico goeldii) are characterized by hindlimb and
hindfoot elongation, and a pattern of locomotion dominated by leaping to and from vertical supports in the forest under-
story. We present field data on trunk-to-trunk leaping in a habituated group of callimicos in northern Bolivia. We measured
the DBH of the takeoff and landing platform, and the distance traveled during 110 trunk-to-trunk leaps. Our results indi-
cate that mean distance leapt by callimicos was 1.8 m (range 0.2-4.3m). There were no significant differences in the size of
takeoff (mean = 10.3 cm) and landing platforms (mean= 9.9 cm). In addition, longer leaps did not occur on larger diameter
supports than did shorter leaps. Although tree trunks and saplings were the most commonly used takeoff and landing plat-
forms, 31.8% of the time callimicos jumped to and from bamboo culms. These data highlight the facts that trunk-to-trunk
leaping represents a highly specialized pattern of locomotion in callimicos, and that these primates travel through mixed for-
ests that include stands of bamboo and canopy trees. Conservation efforts to sustain viable populations of Callimico goeldii
must focus on protecting and preserving habitats that contain large tracts of mixed bamboo and secondary forest.

Key Words: callitrichines; locomotion; bamboo; habitat.


Resumen

Comparado con otras species de tamarinos y monos titis, los callimicos (Callimico goeldii) se caracterizan por el alargamien-
to de sus extremidades posteriores y anteriores, y un patr6n de locomoci6n dominado por los saltos a y desde substratos
verticales en el sotobosque. Presentamos datos de campo sobre saltos de tronco a tronco en un grupo habituado de calli-
micos en el norte de Bolivia. Medimos el DBH de las plataformas de despegue y aterrizaje, y la distancia recorrida durante
110 saltos de tronco a tronco. Nuestros resultados indican que la distancia promedio saltada por los callimicos fue 1.8 m
(rango 0.2-4.3m). No hubo diferencias significativas en el tamafio de las plataformas de despegue (promedio= 10.3 cm)
y aterrizaje (promedio = 9.9 cm). Adicionalmente, los saltos mais largos no ocurrieron en soportes de mayor diimetro que
para los saltos mais cortos. Aunque los troncos de irboles y arbolitos fueron las plataformas de despegue y aterrizaje mas
cominmente utilizadas, el 31.8% del tiempo los callimicos saltaron hacia y desde tallos de bambds. Estos datos resaltan que
el saltar de tronco a tronco represent un patron de locomoci6n altamente especializado en callimicos, y que estos primates
se desplazan a trav6s de bosques heterog6neos que incluyen parches de bambi y irboles de dosel. Esfuerzos de conservaci6n
para sostener poblaciones viables de Callimico goeldii deben enfocarse en proteger y preservar habitats que contengan gran-
des extensions de bosque de bambd y bosque secundario.


Palabras Clave: callitrichines; locomoci6n; bambd; habitat.


Introduction

Tamarins, lion tamarins, marmosets and callimicos repre-
sent a highly successful radiation of 7 genera and 42 spe-
cies of small bodied New World monkeys (Rylands and
Mittermeier 2009). These animals exploit a variety of
mature, secondary, riparian, successional, highly seasonal,
and dry (caatinga, savanna, and cerrado) forest habitats
from Panama and across the Amazon basin extending as
far south as northern Bolivia and as far east as the Atlan-
tic Coastal forests of Brazil (Hershkovtiz, 1977; Rylands,
1996). Despite species specific differences in body mass,
hand and limb proportions (Bicca-Marques, 1999; Garber
and Leigh, 2001; Davis, 2002), and diet (Digby et al.,


2007), field studies indicate that all callitrichine species use
their claw-like nails to cling to large vertical and sharply
inclined supports in the forest understory (Garber, 1992).
These vertical trunks provide a stable foraging platform
for the exploitation of resources such as bark refusing in-
sects and small vertebrates, plant exudates, and fungi that
grow on bamboo culms (Kinzey et al., 1975; Peres, 1986;
Garber, 1992; Youlatos 1999; Porter et al., 2009). Trunks
also are used by callitrichines as a perch from which to scan
the ground in search of arthropod prey (Garber, 1992).

Although all callitrichines use vertical clinging postures
during feeding and foraging, most species do not fre-
quently leap between vertical trunks during travel. For





Neotropical Primates 16(1), June 2009


example, in Saguinus ... ..t Saguinus mystax, Saguinus
labiatus, S. tripartitus, and S. fuscicollis trunk-to-trunk leap-
ing accounts for only 1.5-7.7% of the total positional rep-
ertoire during travel (Garber and Leigh, 2001; Garber et
al., 2009). In Cebuella pygmaea, trunk-to-trunk leaping is
more common (12.9% of travel), however, claw climbing,
claw clinging, quadrupedal walking/bounding, and leap-
ing on small supports (Youlatos, 1999, 2009) represent its
primary modes of travel. In the case of C .-'( detailed
quantitative data on positional behavior are lacking, how-
ever, travel is generally described as quadrupedal with the
majority of leaping restricted to small diameter supports in
the tree canopy (Garber et al., 2009).

Callimico goeldii (hereafter referred to as callimicos) is dis-
tinct among callitrichines in the degree to which trunk-to-
trunk leaping dominates travel. In a field study of position-
al behavior in callimicos, Garber and Leigh (2001) report
that 55.1% of all leaps were between vertical supports in
the forest understory. These leaps accounted for 23% of
total travel (Garber and Leigh 2001). Similarly, Porter
(2004) found that compared to sympatric tamarins, a sig-
nificantly greater proportion of locomotion in callimicos
involved trunk-to-trunk leaping (45% of travel in callimi-
cos vs. 22% for Saguinusfuscicollis and 3% for S. labiatus).
Moreover, relative to other callitrichines, callimicos have
elongated hindlimbs that aid in generating large propulsive
forces required for leaping from noncompliant supports,
and derived features of the ankle that enhance joint stabil-
ity during takeoff and landing (Garber and Leigh, 2001;
Davis, 2002, Garber et al., 2005). Data from a kinematic
study of trunk-to-trunk leaping in captive callitrichines in-
dicate that when leaping across a gap of one meter both
pygmy marmosets and common marmosets are character-
ized by a low takeoff velocity and experience significant
vertical height loss upon landing (Garber et al., 2009). In
contrast, callimicos were found to generate significantly
greater velocity at takeoff and to gain or maintain height
when leaping these same distances (Garber et al., 2009).

Given that all previous accounts of trunk-to-trunk leaping
in wild callimicos are based on visual estimates of the size of
takeoff and landing platforms and the distance leaped, we
present data using direct measurements of trunk-to-trunk
leaping in wild adult callimicos in northern Bolivia. Our
goal was to collect detailed observations of leaping in order
to better evaluate habitat requirements that are critical for
the protection and conservation of this threatened primate
in northern Bolivia.

Methods

Study Group and Field Site
During June and July 2005, we collected data on trunk-
to-trunk leaping in a habituated group of three callimicos
(two adult males and one adult female) inhabiting the
forest around Camp Callimico (1123'S, 69006"W) in the
Department of the Pando, Bolivia (Fig. 1). The forest in


this area is representative of sandy-clay forests of the south
and southwestern Amazon Basin (Alverson, 2000), and ex-
periences pronounced dry and rainy seasons (Porter, 2001).
Rainfall is approximately 2,000 mm per year (Porter,
2001). Over the course of full day follows, we used a metric
tape to systematically measure the diameter at breast height
(DBH) of the takeoff and landing platforms used by cal-
limicos, and the distance between them, during 110 trunk-
to-trunk leaps. Previous studies at this field site indicate
that approximately 80% of all callimico behaviors occur
within 5 m of the ground (Porter, 2004), and therefore
DBH (taken at a height of 1.5 m) is expected to be a rep-
resentative measure of the actual size of the support used.
Takeoff and landing platforms were scored either as tree
trunk or woody bamboo. All three adult group members
were fully habituated to the presence of observers and each
had been the subject of previous behavioral studies (e.g.
Porter et al., 2007). Therefore, we are confident that our
presence had a negligible effect on the locomotor behavior
or distance leaped by the callimicos. However, given their
all black coat color and the lack of individually distinguish-
able markings or hair patterns, we could not consistently
identify individuals. Therefore, data for all three adult indi-
viduals were pooled for analyses.

In order to examine the distribution of habitat types within
the study group's home range, we divided the forest into
habitat categories based on canopy height, visibility criteria,
and the dominant plant species present. Using this method,
we identified five major habitats: primary forest with open
understory, primary forest with dense understory or matur-
ing secondary forest, bamboo forest, secondary forest, and
stream edge forest (see Porter et al., 2007). We estimated
habitat availability by recording the habitat category pres-
ent at 100m intervals (102 sample points) along all north-
south trails in the group's home range. Comparisons be-
tween the size of takeoff and landing platforms were made
using a Student's t-Test for paired sample means. Variance
in the size of takeoff and landing platforms was compared
using an F-Test. Correlations between the size of takeoff
platforms, landing platform size, substrate size, and dis-
tance leaped were analyzed using regression analyses. In all
statistical tests probability was set at <0.05.

Results

We measured 110 leaps in which callimicos traveled be-
tween vertical trunks in the forest understory. On aver-
age animals were located at 3.0 1.5m above the ground
on the take-off platform. Over 61% of leaps occurred at
heights of <3 m above the ground, and 30% occurred at
heights between 3-5 m. The average DBH of trunks used
by callimicos as takeoff platforms was 10.3 + 8.3 cm and
the average DBH of landing platforms was 9.9 + 8.7 cm
(Table 1). There were no statistical differences in the diam-
eter (t= 0.31, df= 109, p= 0.75, two-tailed test) or variance
in diameter (F= 0.9, df= 109, p= 0.29, one-tailed test) of
vertical supports used as takeoff platforms as compared to





Neotropical Primates 16(1), June 2009


supports used as landing platforms. Moreover, DBH of the
takeoff platform was not correlated with the DBH of the
landing platform (r= 0.04, p= 0.62). The culms of woody
bamboo (Guadua weberbaueri) served as the takeoff sub-
strate in 41.8% of trunk-to-trunk leaps and as the land-
ing substrate in 48.2% of these leaps (Table 1). Overall
40.9% of callimicos' leaps employed tree trunks as both
takeoff and landing platforms and 31.8% employed
bamboo culms as both takeoff and landing platforms.

Although we did not quantify the relative size distribution
of trunks and bamboo culms across the group's 114 ha
home range, we did quantify the presence and use of five
major habitat types. Our results indicate that despite the


fact that bamboo forest comprised only 5% and secondary
forest only 16% of the group's home range, callimicos spent
a total of 67% (17% and 50% respectively) of their time
in these habitats. In contrast, primary forest accounted for
74% of the callimicos' home range, but was used only 30%
of the time. These data highlight that callimicos frequently
travel through mixed forests that include stands of bamboo
and secondary forest trees, and that large diameter primary
forest trees were rarely used as leaping substrates. Less than
3% of takeoff platforms and less than 6% of landing plat-
forms involved vertical trunks with a DBH of greater than
30 cm. Foster and Hubbell (1990) describe trees of greater
than 30 cm DBH on Barro Colorado Island, Panama as
canopy trees.


Table 1. Trunk-to-trunk leaping in Callimico
Leaping Behavior
Take Off Platform Landing Platform Distance Leaped
(DBH in cm) (DBH in cm) (m)
Mean 10.3 + 8.3 9.9 + 8.7 1.8 + 0.8
Range 2.7-71 2.7 71 0.2 -4.3
Median 11.0 8.6 1.8
Substrate Type
Sample Size Sample Size
Bamboo 46 (41.8%) 53 (48.2%)
Trunk 64 (58.2%) 57 (51.8%)


Map Legend '= site of Callimico study Q= City or town V= river I = international boundary % = national boundary

Figure 1. Map of the callimico study site in the Pando region of northern Bolivia.





Neotropical Primates 16(1), June 2009


The mean distance callimicos traveled between vertical
trunks was 1.8 + 0.8 m (Table 1). The shortest leap spanned
a distance of 20 cm and the longest leap was 4.3 m. Trunk-
to-trunk leaps of 1-2 m (44.5%) and 2-3 m (30.9%) ac-
counted for 75% of all leaps (Figure 2). Less than 1% of
leaps were greater than 4 m. During the landing phase of
all trunk-to-trunk leaps, callimicos' forelimbs contacted
the landing platform in advance of their hindlimbs.

Overall, we found no significant relationship between
distance leaped and the size of either the takeoff (r= 0.03,
p= 0.74) or landing platform (r= 0.001, p= 0.98). In addi-
tion, the diameter of takeoff and landing platforms used
during the shortest leaps (<1 meter) did not differ from
those used during the longest leaps (>3 m) (takeoff plat-
form t= 0.25, p= 0.39; landing platform t= -0.02, p= 0.48).
Table 2 lists the size of takeoff and landing platforms during
the shortest and longest leaps. This suggests that given their
small body size and elongated hindlimbs, callimicos can
generate large propulsive forces pushing off both relatively
small (5 cm DBH) and relatively large (71 cm DBH) di-
ameter vertical trunks (Table 1).

We also examined takeoff and landing platform DBH
and leaping distance when callimicos traveled on bamboo
culms compared to tree trunks (Table 3). As a substrate,
bamboo culms were significantly smaller than tree trunks
(t=-9.34, p<.0001). The distance leaped when moving
from bamboo culm to bamboo culm (mean of 1.63 m) was
marginally shorter than the distance leaped when moving
from one tree trunk to another (mean of 2.02 m) (t= 1.95,
p= 0.054). Moreover, when trunks were used as a take-
off platform (even in cases of trunk to bamboo leaping),


distances leapt were consistently longer than when bamboo
culms were used as the takeoff platform (t= 2.47, p<0.015).
Although shorter distances leapt when traveling on bamboo
may reflect the fact that bamboo culms grow in dense patch-
es, it is also possible that rigid tree trunks provide a more
stable takeoff platform during leaping than hollow bamboo
culms allowing the animals to leap longer distances.

Discussion

Based on presently available field and captive studies, cal-
limicos appear to be the only callitrichine species charac-
terized by a suite of specialized morphological and behav-
ioral traits associated with trunk-to-trunk leaping (Garber
et al. 2009). Our results indicate that during trunk-to-
trunk leaping callimicos generally leapt distances of 1-3 m
(mean= 1.8 m) in the forest understory. These takeoff and
landing platforms varied in diameter from approximately
3-71 cm (DBH), however, most leaps occurred on relative-
ly small substrates (mean support diameter= 10 cm) includ-
ing small trunks, saplings, and bamboo culms. Overall, 59%
of all trunk-to-trunk leaps in callimicos involved bamboo
culms as either takeoff or landing platforms, and 31.8% of
leaps involved bamboo culms as both takeoff and landing
platforms. Relative to body mass, callimicos possesses both
a highly elongated hindlimb (femur and tibia) and hind-
foot (distance from calcaneous to the most distal extent of
the metatarsals) compared to other callitrichines (Garber
and Leigh, 2001). The callimicos also are characterized by
the lowest intermembral index [(ratio of humerus + radius)/
(femur + tibia) x 100] of any tamarin or marmoset spe-
cies (Davis, 2002). Hindlimb elongation has been argued
to represent an adaptation for trunk-to-trunk leaping (e.g.


Table 2. DBH of takeoff and landing platforms for the shortest and longest leaps.
Take Off Platform Landing Platform Distance Leaped
(DBH in cm) (DBH in cm) (m)
LEAPS <1 (N=20)
Mean 11.6 + 12.9 10.9 + 9.3 0.68 + 0.25
Range 3.5-57.3 2.7-38.8 0.2-1.0
LEAPS >3M (N= 10)
Mean 10.5 + 6.0 10.9 + 8.4 3.42 + 0.47
Range 4.7 25.1 5.0-33.1 3-4.3


Table 3. Distance leaped to and from different substrates.
Take Off Platform Landing Platform Distance Leaped
(DBH in cm) (DBH in cm) (m)
Bamboo to Bamboo 5.13 + 1.59 5.18 + 1.76 1.63 + 0.70
(N= 35)
Bamboo to Trunk 4.71 + 0.98 15.14 + 7.77 1.52+ 0.59
(N= 11)
Trunk to Bamboo 13.32 + 6.66 5.07 + 1.69 1.85 + 0.70
(N= 19)
Trunk to Trunk 14.35 + 31.36 14.19 + 34.10 2.02 + 0.99
(N= 45)





Neotropical Primates 16(1), June 2009


"vertical clinging and leaping") in several species of pros-
imians (e.g. Indri, Propithecus, Avahi, Galago, Lepilemur,
Hapalemur, Tarisus; Demes et al., 1995; Nekaris and Beard-
er, 2007) and one other species of New World primate,
Pithecia pithecia (Walker 1998). Elongated hindlimbs
improve leaping abilities as they increase the duration of
time over which the body can be accelerated during takeoff
(Garber, 2007). In contrast to vertical clinging and leaping
prosimians and Pithecia, callimicos (and all callitrichines)
land forelimbs-first rather than hindlimbs-first (Garber et
al. 2009). Forelimbs first landings impart high compressive
forces on wrist, elbow, and shoulder girdle. How exactly
callimicos dissipate these forces remains unclear. However,
forelimbs-first landing is common among anthropoids,
most of which, are not specialized leapers.

Based on over 1640 hours of observations of our study
group from 2002-2006, we estimate that our callimico
study group exploited a home range of 114 ha (Porter et al.,
2007). Although the home range was composed principally
of primary dense understory forest (74%), secondary forest
(16%) and bamboo forest (5%), areas of woody bamboo
and secondary forest were used by callimicos at signifi-
cantly greater frequencies than expected based on habitat
availability (17% and 50% of observation time respective-
ly) (Porter et al., 2007). Bamboo and secondary forests are
characterized by an extremely dense and thorny understory
containing considerable numbers of small to medium sized
vertical supports. We have previously suggested (Porter and
Garber, 2004) that based on their cryptic mode of behav-
ior, black pelage, and virtually exclusive use of the lowest
levels of the forest understory, trunk-to-trunk leaping
may enable callimicos to reduce predation risk from both
aerial and terrestrial predators by concealment and rapid
escape. Moreover, bamboo forests provide callimicos with
a major component of their diet, Ascopolyporous, a fungus
that grows exclusively on the culms and branches of woody


50
45

40
S35

S 30-

2-25
20.



10
15
10-

<1m >1<2m >2<3m >3<4m >4m

Figure 2. Frequency of trunk-to-trunk leaping in Callimico
across different horizontal distances.


bamboo (Guadua weberbaueri) (Hanson et al. 2006; Porter
et al., 2007). Porter and Garber (in prep) report that fungi
is consumed by callimicos during both the wet and dry sea-
sons, and accounted for 42% of yearly feeding time. Fifty-
eight per cent of the fungi consumed by callimicos in our
study group were Ascopolyporous.

We conclude that trunk-to-trunk leaping represents a
highly specialized pattern of locomotion that distinguishes
callimicos from all other callitrichine species. The callimi-
cos' use of vertical supports in the forest understory ap-
pears to be directly tied to its feeding ecology (exploita-
tion of trunks to obtain bamboo fungi and as a foraging
platform to locate insect prey), antipredator behavior, and
rapid mode of travel. Several species of birds and insects
are described as bamboo specialists (Lebbin, 2007) with
part or all of their ranges restricted to forests dominated
by Guadua bamboo. According to Lebbin (2007: 126)
Amazonian bamboo habitats are characterized by high pri-
mary productivity, and a "combination of rich arthropod
resources, a highly distinctive vegetation structure, occur-
rence across large geographic areas and [exist] in relatively
large patches." Although it remains unclear the degree to
which the callimicos' distribution and feeding ecology are
dependent on the presence and availability of bamboo
habitats, we suggest that conservation efforts to sustain
viable populations of callimicos must focus on protecting
and preserving habitats that contain large tracts of mixed
bamboo and secondary forest.

Acknowledgments

Funds to conduct this research were provided by the Uni-
versity of Illinois, Urbana, IL, and a National Geographic
Research and Exploration Grant, and approved through
the UIUC and NIU Institutional Animal Care and Use
Committees. The project adhered to the legal requirements
for animal research in Bolivia. We thank Edilio Nacimento
Anastacia and Edilio Nacimento Becerra for assistance in
data collection. PAG wishes to thank Chrissie, Sara, and
Jenni for their love and support.

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Neotropical Primates 16(1), June 2009


a um levantamento coproparasitol6gico de um grupo de
muriquis-do-norte isolado em um pequeno fragmento flo-
restal no Estado do Espirito Santo realizado com a finalida-
de de fornecer subsidies para a elaboraqao de estrategias de
agao para a conservagao das populag6es remanescentes.


ENDOPARASITOS EM MURIQUIS-DO-NORTE,
BRACHYTELES HYPOXANTHUS, ISOLADOS EM Material e MWtodos
PEQUENO FRAGMENTO DE MATA ATLANTICA


Priscila Santos Angonesi
Bdrbara Almeida-Silva
Sergio Lucena Mendes
Alexandre dos Santos Pyrrho

Introduao

Os parasitos tem um papel important nos ecossistemas ao
influenciarem a sobrevivencia e a reprodugao de seus hospe-
deiros (Dobson & Hudson 1992; Hudson etal. 1992; Coop
& Holmes 1996). Estudos parasitol6gicos com populagoes
selvagens de primatas nao-humanos tem registrado uma
alta diversidade de esp6cies parasitas do trato gastro-intesti-
nal e fornecido informa6oes sobre suas relagoes evolutivas e
ecol6gicas (Appleton et al. 1986; Eley et al. 1989; McGrew
et al. 1989; Ashford et al. 1990, 2000; Stuart et al. 1990,
1993; Stuart & Strier 1995; Stoner 1996; Muiller-Graf et
al. 1997; Martins 1999; Lilly etal. 2002; Hahn etal., 2003;
Gillespie et al. 2004, 2005). Aldm disso, o entendimento da
relagao parasito-hospedeiro 6 particularmente important
para a conservagao de esp6cies endemicas e ameagadas de
extingao (Stuart & Strier 1995), pois subsidia o monitora-
mento da sadde do meio ambiente, principalmente em am-
bientes perturbados, possibilitando uma melhor aplicadao
dos plans de manejo de esp6cies ameagadas.

0 muriqui-do-norte, Brachyteles .'... .-'.. Kuhl, 1820,
6 uma esp6cie Criticamente Em Perigo de extingao (Brasil,
MMA 2003) e endemica da Mata Atlrntica, cuja distribui-
gao abrange parte dos estados de Minas Gerais, Espirito
Santo e Bahia (Mendes et al., 2005). A principal ameaga a
sobrevivencia do muriqui-do-norte 6 a perda e a fragmenta-
gao da cobertura florestal, que contribui para a redugao do
tamanho das populagoes e o seu isolamento. Segundo Sasal
et al. (2000), populagoes pequenas de hospedeiros estarao
mais suscetiveis aos potenciais efeitos negativos dos para-
sitos. No caso do muriqui-do-norte, o risco de ocorrencia
de doengas pode ser alto, pois a maioria dos fragments
florestais habitados por este primata sofre frequentemente a
interferencia de animals domrsticos e pessoas, o que torna
o monitoramento parasitol6gico altamente recomendivel
para a sua conservagao (Mendes et al. 2005). A pesquisa
de long prazo de K. B. Strier e colaboradores na Reserva
Particular do Patrim6nio Natural Feliciano Miguel Abdala
(RPPN-FMA), Caratinga, Minas Gerais, tem contribuido
significativamente com conhecimento acerca do comporta-
mento, ecologia e conservagao do muriqui-do-norte (Strier
& Mendes 2009), incluindo estudos parasitol6gicos (Stuart
etal. 1993; Santos etal. 2004). 0 present trabalho se refere


Area de Estudo
0 municipio de Santa Maria de Jetibi, localizado na regiao
serrana do Espirito Santo, apresenta vegetagao de Mata
Atlhntica em diversos estigios de sucessao. Suas areas de flo-
resta encontram-se distribuidas em fragments parcialmen-
te isolados por pastagens, plantac6es, redes elktricas de alta
tensao e represas, onde sao encontrados grupos pequenos e
isolados de muriqui-do-norte. 0 maior grupo identificado
no municipio possuia 18 individuos (Mendes et al., 2005).
Este estudo foi conduzido em um fragmento de mata com
128 ha, localizado em propriedades privadas (2002'32"S,
4041'45"O0). No period do estudo, o fragmento abrigava
um grupo de muriquis que various de 13 a 15 individu-
os (2-3 machos adults, 1-0 macho subadulto, 1 macho
juvenile, 2-3 machos infants, 4 femeas adults, 1 femea
subadulta, 1 femea juvenile e 1-2 femeas infantss, alkm
de quatro outras esp6cies de primatas: Callicebus personatus
(E. Geoffroy, 1812), Alouatta guariba clamitans (Humbol-
dt, 1812), C flaviceps (Thomas, 1903) e a ex6tica
( .-.' .-..- ....i (H um boldt, 1812).

Levantamento Coproparasitoldgico
Foram feitas coletas de fezes de muriquis entire os meses de
novembro de 2004 e abril de 2005. As amostras foram clas-
sificadas em tres categories: 1) amostras individuals identifi-
cadas, onde foi possivel identificar o individuo que defecou;
2) amostras individuals nao identificadas; e 3) e amostras
coletivas didrias, contend fezes de mais de um individuo.
Porgoes dos bolos fecais que nao entraram em contato com
o solo foram coletadas logo ap6s o ato de defecanyo e acon-
dicionadas em tubos de 50 ml tipo "Falcon" contend MIF
1:>4 (fixador merthiolate -iodo-formaldeido) ou SAF 1:>4
(fixador Acetato de S6dio-Acido Ac&tico-formaldeido) con-
forme descrito por De Carli (2001). 0 processamento e
identificacao das esp6cies de parasites foram realizados no
Laborat6rio de Imunoparasitologia do Departamento de
Anilises Clinicas e Toxicol6gicas da Faculdade de Farmicia
da Universidade Federal do Rio de Janeiro, utilizando-se os
m6todos de Hoffman, Pons e Janer (sedimentagao esponti-
nea) e de Faust (centrifugo-flutuacao em solugao de sulfato
de zinco). As lrninas foram coradas com lugol e observa-
das em microsc6pio 6ptico, marca Nikon, modelo eclipse
E200, munido de sistema fotografico digital em aumentos
de 100x e 400x.

Resultados

Foram coletadas 28 amostras, das quais 16 foram individu-
ais nao identificadas, sete foram individuals identificadas
(representando cinco individuos) e cinco foram coletivas





Neotropical Primates 16(1), June 2009


diarias. Apenas quatro amostras foram negatives. Dentre
as amostras positivas, duas apresentaram alteragoes de con-
sistencia e coloracao, mostrando-se pastosas e contend
sangue. Sete taxons de parasites em diferentes estigios de
desenvolvimento foram identificados (Tabela 1). Foram en-
contrados trofozoitas e cistos de Balantidium coli, um ne-
mat6ide ancilostomideo em estigio larval em uma amostra
e um ovo em outra e um ovo de um tremat6deo digen&tico.
As maiores prevalencias foram observadas entire os protozo-
irios e os cest6ides (Tabela 1).

Discussed

0 protozoirio mais comum foi o Balantidium coli que 6 o
dnico ciliado associado a les6es de trato intestinal de pri-
matas nao-humanos. Esta esp6cie foi recentemente descrita
para a populagao de muriquis da RPPN-FMA, em Minas
Gerais, por Santos et al. (2004). Segundo Rey (2001), os
suinos sao reportados como hospedeiros reservat6rios desta
espcie, cuja prevalencia pode oscilar entire 50 e 100%.
A infeccao ocorre por ingestao de cistos infectantes ou tro-
fozoitos na agua ou alimento (Rey, 2001). A observagao de
cistos dos generos Entamoeba e Giardia reforga a impor-
tincia da agua como fonte de infeccao. Estes dois generous
possuem veiculagao predominantemente hidrica e grande
importincia em pianos de sadde pdblica, pois sao agents
etiol6gicos de diarrdias agudas em humans (WHO, 2000).
Segundo Bennett et al. (1995), algumas esp6cies do genero
Giardia sao transmissiveis entire humans e outros animals.
Ja o genero Entamoeba 6 considerado incomum ou raro em
primatas neotropicais de vida livre e a identificacao das es-
pcies 6 de fundamental importncia, ji que nem todas sao
reportadas como patogenicas, sendo E. histolytica capaz de
gerar les6es graves na mucosa intestinal de primatas neotro-
picais (Bennett et al., 1995).

Moniezia 6 um cest6ide que habitat o intestino delgado
de herbivoros como coelhos, ovelhas, bovinos e primates

Tabela 1. Parasitos encontrados em amostras fecais de Brachyteles
(N= 28 amostras).
xon n Prevalancia
(Amostras positivas) (%)
Protozoa 22 79
Balantidium coli 16 57
Entamoeba sp. 4 14
Giardia sp. 2 7
Nematoda 2 7
Ancylostomidae 2 7
(genero nao identificado)
Cestoda 10 36
Moniezia sp. 7 25
cf. Hymenolepis sp. 5 18
Trematoda 1 4
Digenea 1 4
(genero nao identificado)


(Bowman, 1995). Seu ciclo vital 6 heteroxenico e envolve
um carrapato como hospedeiro intermedidrio (Rey, 2001).
A Moniezia rugosa ji foi encontrada em muriquis-do-sul
(Brachyteles arachnoides) por Artigas (1937) e Dunn (1963).
A existencia de pastos para pecudria ao redor do fragmento
facility a dispersao de carrapatos infectados corn a larva cis-
ticerc6ide destes cest6ides. A possivel infeccao corn o ces-
t6ide Hymenolepis sp. 6 compativel corn a ocorrencia deste
parasito em roedores, humans e primatas nao-humanos
(Bowman, 1995; Bennett et al., 1995). Hymenolepis spp.
podem apresentar ciclo monoxenico corn transmissao oral-
fecal ou heteroxenico, tendo insetos (pulgas, por exemplo)
como hospedeiros intermediarios (Rey, 2001). A alta pre-
valencia de ancilostomiase na populagao humana no muni-
cipio de Santa Maria de Jetibi (Angonesi, 2005) sugere que
os muriquis podem ser infectados por este parasito ao en-
trarem em contato corn substrato contaminado corn fezes
humans durante deslocamentos pelo chao. 0 ciclo de
vida de Ancylostoma spp., por exemplo, 6 direto e a infeccao
pode se dar por via passiva direta (ingestao de L3 infectan-
tes) ou por via ativa (penetracao percutinea) (Rey, 2001).

A diversidade de parasites encontrados sugere uma estrei-
ta relagao corn atividades desenvolvidas pela populagao
humana do entorno do fragmento florestal taiss como sui-
nocultura, bovinocultura, avicultura e o trinsito de pessoas,
caes e gatos), sobre a sadde dos muriquis de Santa Maria
de Jetibk. 0 comportamento dos muriquis de consumer
agua de c6rregos, como observado no present estudo e
em outras localidades (Mourthd et al., 2005), certamente
aumentam o risco de infeccao dos muriquis. A deficiencia
do saneamento bisico municipal tambdm deve contribuir
negativamente na sadde dos muriquis. Em 2000, o muni-
cipio possuia cerca de 28.750 habitantes e a rede de esgotos
ou de drenagem pluvial atendia apenas <10% das residen-
cias. Na irea rural nao havia rede de esgotos e os moradores
utilizavam fossas rudimentares ou despejavam os efluentes
diretamente em rios e riachos (Instituto Brasileiro de Ge-
ografia e Estatistica-IBGE 2008). Esta deficiencia no tra-
tamento de efluentes 6 refletida no alto ndmero de casos
humans de doengas de veiculagao hidrica no municipio.
Segundo o Laborat6rio Santa Maria Ltda., os registros mais
frequentes em humans em 2004 foram esquistossomose,
giardiase, amebiase e ancilostomiase (Angonesi, 2005), das
quais apenas a esquistossomose nao foi detectada nos muri-
quis no present estudo.

Os resultados sugerem a necessidade de uma abordagem
de paisagem que envolva o ambiente antr6pico. Portanto,
paralelamente aos pianos de recuperacao do habitat, sao
necessirios pianos de educacao em sadde e programs
de saneamento rural para a populagao humana de Santa
Maria de Jetibi. Esta estrategia promoveria a melhoria da
sadde das populagoes do entorno das ireas naturais e, assim,
reduziria o risco dos efeitos antr6picos negativos sobre a
fauna silvestre. Aldm disso, se faz necessirio o monitora-
mento constant da sadde de todos os grupos de muriquis
do municipio.





Neotropical Primates 16(1), June 2009


Agradecimentos


Agradecemos a familiar Seick por permitir o desenvolvi-
mento deste trabalho em sua propriedade. Ao professor
Alan Lane de Melo do Departamento de Parasitologia
ICB-UFMG pela verificacao das analises e a Rog&rio
R. dos Santos, Heverton Filipe G. DalZilio, Danie-
la Rozas e Adhemar Wallach pelo apoio no desenvolvi-
mento do trabalho de campo. Este trabalho foi apoiado
pelo IPEMA Instituto de Pesquisas da Mata Atlhntica e
parcialmente financiado pelo CNPq, PROBIO/MMA e
Conservagao Internacional.

Priscila Santos Angonesi, ESFA-Educandirio Sao Fran-
cisco de Assis, Santa Teresa, Espirito Santo, Brasil, e-mail:
, Birbara Almeida-Silva,
S6rgio Lucena Mendes, Departamento de Ciencias Bio-
16gicas, Universidade Federal do Espirito Santo, Espirito
Santo, Brasil and Alexandre dos Santos Pyrrho, Departa-
mento de Anilises Clinicas e Toxicol6gicas, Faculdade de
Farmicia, Universidade Federal do Rio de Janeiro, Rio de
Janeiro, Brasil.

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HABITAT CHARACTERIZATION AND POPULATION
STATUS OF THE DUSKY TITI (CALLICEBUS ORNATUS)
IN FRAGMENTED FORESTS, META, COLOMBIA

Marcela Wagner
Francisco Castro
Pablo R. Stevenson

Introduction

Tropical forests have important ecosystem functions such
as soil protection, climate regulation, supply of goods, etc.
(Foley et al., 2007). In Colombia, an accelerated process of
transformation of natural ecosystems is occurring, which
results in habitat reduction and fragmentation. It has
been estimated that a third of the country's forest cover
has been eliminated (Alexander von Humboldt Institute


et al., 1997), and the principal causes of deforestation are
the expansion of the agricultural frontier and colonization.
In fact, Colombia is the fourth country with highest levels
of deforestation among South American countries (FAO,
2006). In Orinoquia, colonizers have converted forest to
savanna ecosystems for agriculture and livestock. Further-
more, recently the African oil palm industry has greatly
expanded with government support (Moreno, 2000) and
Meta department ranks first in the nation as a producer
of African palm (Phoenix dactylifera). The land destined to
this cropping system covers 47,525 ha, and the produc-
tion is estimated to be increased by 35,000 ha in the next
few years (Gobernaci6n del Meta, 2006), which implies
more land conversion and, therefore, further habitat de-
struction. According to local inhabitants, in the 1940s the
study region (San Isidro de Chichimene, Acacias) was an
intact forest. Since then, agriculture has greatly expanded
in the region with the production of corn, coffee and cas-
sava, and wood extraction and hunting have also increased.
In a period of only 30 years colonists have depleted the for-
ests by creating fragments that continue to be intervened
through time. Currently, livestock and the expansion of oil
palm are the principal causes of deforestation in the region.
Earlier deforestation in the region created forest fragments
especially fragments along streams in which many species
have become isolated. Such is the case of the Vereda San
Isidro de Chichimene, a fragmented landscape which still
holds rich fauna and flora.

The Colombian endemic primate Callicebus ornatus inhab-
its this region and it has been classified as vulnerable by the
IUCN (VU Blab (iii)) (IUCN, 2008). According to Defler
(2004), Callicebus ornatus populations are small, and their
major threat is colonization; "since C. ornatus is endemic to
Colombia, its conservation within the country is very im-
portant". He recommended censuses to evaluate the species'
status in detail and proposed local environmental educa-
tion campaigns, to insure its survival. Traditionally, primate
studies have been conducted in reserve areas. However, the
risk of extinction is highest for small populations that are
generated when the habitat is fragmented or modified. For
this reason, studies outside reserves could help to evaluate
the status of such species (Chapman and Peres, 2001), their
responses to disturbance, and extinction risk. Furthermore,
fragmentation has caused a reduction in plant species diver-
sity and composition in the region (Stevenson and Aldana,
2008). Since fruit production and plant composition may
affect primate populations (Stevenson, 2001), we were also
interested in the potential effects of vegetation composition
on the populations of C. ornatus. We were also interested in
the potential effects of fragment size (i.e., the area of each
fragment) on the population density of the primates, since
this factor has demonstrated to have strong effects on pri-
mate demographic patterns (Marsh, 2003). In this study, a
census of Callicebus ornatus and a vegetation sampling were
conducted in forest fragments in Vereda San Isidro de Chi-
chimene, to evaluate the status of this species and to deter-
mine conservation implications in private lands.





Neotropical Primates 16(1), June 2009


Methods

Study Area
The Vereda San Isidro de Chichimene is located in the Mu-
nicipality of Acacias in the department of Meta (480 m
a.s.l., 7342'W, 0355'N). This region corresponds to a
very humid tropical forest (Agustin Codazzi Geographic
Institute, 1995). Photographic images were taken to regis-
ter the landscape heterogeneity and the forest cover was de-
scribed by a LANDSAT image (2000, Figure 1) provided
by RedVerde.

The study was carried out in private land. Eight fragments
were studied (Figure 2) within 86.24 ha of forest, which
corresponded to 8.5% of forest cover remnants in a total
of 1010 ha (framed area in Figure 1). The forest remnants
consist mainly of riparian secondary forest. These forests
tend to be narrow with an average width of 30 m, and show
large variations in age and degree of human intervention.

Census of Callicebus ornatus
The census was carried out from January to March 2007
by one, and sometimes two observers, between 5:30 and
12:30 h, during a total of 392 h. Each fragment was visited
12 times. When a primate was detected, the following data
were registered: (1) time, (2) group size, (3) group com-
position, (4) geographical position (GPS, Garmin eTrex,
Legend), (5) special traits of individuals, (6) activity of an-
imals when encountered (Williamson and Feistner, 2003).
A map of the study area was generated using GPS (Figure
2). Routes through forest fragments and coordinates
of group locations were transferred to a PC using Map-
Source 6.9.1 software. Population densities were based on
the number of groups and individuals per group in each
fragment (only fragments with more than 3 groups were
considered in further analyses: fragments 1, 3, 5 and 8),
and forest areas were estimated from the map using GIS


tools. Eight fragments were selected in the study area and,
since the fragments were not wide (mean 30m. wide), we
tried to count all individuals and groups by direct obser-
vations from the trails (total length= 57.1 km, estimated
from the map). Age categories were determined by size
according to Kinzey (1981): Infant, individual depend-
ing on locomoting adults; Juvenile I, a second year indi-
vidual (4-12 months); and Juvenile II a third year indi-
vidual (12-24 months), sub-adults and adults. Morning
calls of Callicebus were important cues for detecting them,
since they helped to locate the groups. In the afternoon
Callicebus ornatus is less active than in the morning and
vocalizations are not very common, for this reason the
census was restricted to morning hours. Whenever possi-
ble, photographs were taken with a digital camera to allow
differentiation of groups. In the widest fragment (no. 1),
walking along trails was not an effective way for detecting
all individuals of Callicebus ornatus, since low visibility in
and cryptic behavior made their detection difficult. For
this reason, in fragment no.1, two observers always per-
formed censuses early in the morning, when the vocal-
izations started. Photographs and the number of group
members allowed group differentiation Vocalizations
"chirrups" were also used to locate individuals. Juveniles
were differentiated by the description of the white head
band which develops after the sixth week (Kinzey, 1981).
The relationship between C. ornatus population densities
and the area of the fragment was assessed using simple
regression analysis.

Vegetation Sampling
From April to June, 2007 floristic inventories of trees
(>10 cm diameter at breast height) were conducted in
two plots of 1-hectare (200 m x 50 m) in the fragment
1, divided in 100 m2 subplots. We considered two con-
trasting vegetation types found in forest fragments. One
plot was built in less disturbed forest and the second one


Figure 1. LANDSAT image (RedVerde, 2000). The square indicates
the study area, black zones correspond to forests and palm crops.


Figure 2. Study site. Fragments where censuses were carried out.
Points indicate groups and individuals observed .





Neotropical Primates 16(1), June 2009


is a secondary forest (50 years old). Less disturbed forest
refers to a primary forest with some degree of human in-
tervention (i.e. selective logging has occurred in the past).
Census methodology was based on two guides of the
IAvH (Alexander von Humboldt Institute) (Villareal et al.,
2006 and Vallejo-Joyas et al., 2005). Trees in each plot
were marked with numbered aluminum tags. Sterile and
fertile material were collected and identified by the au-
thors and compared with vouchers in Los Andes Univer-
sity Herbarium and the SINCHI (Institute for Scientific
Amazonian Research) herbarium. A species accumulation
curve was determined by the program EstimateS, Version
7.5 (Colwell, 2005). Importance indexes were determined
by adding the relative frequency, relative density and the
relative basal area.

Results

Census of Callicebus ornatus
Four primate species inhabit the fragments in the study
area: Saimiri sciureus (Squirrel monkey), Cebus apella (Ca-
puchin), Aotus brumbacki (Night monkey) and C. ornatus
(Titis). Forty three titi groups were detected (Table 1) and
its age categories are described in Table 2. The population
density was found to be 192.2 individuals/km2 (Table 3).

There was no relationship between fragment size and popu-
lation density of Callicebus ornatus in the fragments stud-
ied (F =5.12, p=0.15).

Vegetation Sampling
A total of 136 tree species (>10cm DBH) were found in
2 ha. The plant species accumulation curves for each plot
do not reach an asymptote and show that the less disturbed
forest is more diverse than the secondary forest (Figure 3).
The density of Callicebus ornatus in the secondary forest
was 559.1 ind/km2 and 188.2 ind/km2in the less disturbed
forest.

A total of 1,070 trees were marked. Tree density was
571 individuals/ha in the less disturbed forest and
499 individuals/ha in the secondary forest. The less dis-
turbed forest plot shares 26.2% of the plant species with the
secondary forest. The percentage of species found only in
less disturbed forest was higher than the percentage unique
to secondary forest (73.8 vs. 55%). In the less disturbed
forest Socratea exorrhiza, Oenocarpus bataua and Mabea
maynensis, were the most important species (Table 4). In
the secondary forest Casearia sp, Apuleia leiocarpa and Jaca-
randa copaia dominated.

Discussion

Census of Callicebus ornatus and considerations for its
conservation
Agriculture expansion has caused fragmentation in the
study area and the remnants are linear tracts along water-
ways in a pastureland matrix. Deforestation has caused loss


of biodiversity and ecosystem degradation in the region
(Stevenson and Aldana 2007). Despite the highly disturbed
habitat in the region, some endemic and charismatic spe-
cies survive (e.g., titi monkeys, night monkeys, otters, and
giant anteaters). The population density of species, such
as Callicebus ornatus is high in the fragments (192.2 indi-
viduals/km2) and even higher than estimates reported for
undisturbed forest in the same region (8 individuals/km2;
Polanco, 1992). However, it is important to consider these
comparisons with caution because differences in the census
methods and a lower visibility in the primary forest could
result in an underestimation of C. ornatus populations.
However, these large differences indeed reflect variation in
group density, since group size was similar in fragments
and undisturbed forests (Polanco, 1992).

On other grounds we found considerable variations in den-
sity estimates between fragments that were not explained
by area nor by hunting pressure (currently local people do
not hunt primate species in the region), but may be associ-
ated with fine grained variations in resources, and other
demographic and history processes. Callicebus ornatus can
survive in secondary forest because pioneer plants are im-
portant in their diet (Mason, 1968; Hernindez-Camacho
and Cooper, 1976; Polanco, 1992; Sinchez, 1998). Other
important aspects of their survivorship in degraded forest
are their frugivorous-folivorous-insectivorous diet, small
size (Fimbel, 1994), and the local extinction of competi-
tors such as large-bodied primate species that have histori-
cal records in the area (Stevenson & Aldana, 2008). For
instance, fragment 3 showed the lowest population den-
sity (60 individuals/km2). Two reasons could be influenc-
ing this result: 1. It is a large tract of forest without fence
protection, which means that livestock may transit among
the forest preventing plant regeneration. 2. This fragment
is connected with the riparian forest of La Uni6n creek,
which was the only fragment with Cebus apella. This may


Figure 3. Expected number of plant species in two plots,
(a) Less disturbed forest, (b) secondary forest, where all individu-
als (DBH >10 cm) were identified to species or morphospecies,
near Acacias, Meta, Colombia. The grey lines show 95% confi-
dence intervals.


Number of sampl -
Number of samples





Neotropical Primates 16(1), June 2009


Table 1. Group composition of C,... "'n ornatus in forest fragments in Acacias, Meta, Colombia.
Fragment Group Adults Male Sub-Adults Juveniles Infants Undetermined Total
1 1 2 1 3
2 2 2
3 2 1 2 1 6
4 2 1 3
5 2 2
6 2 1 3
7 2 2
8 2 1 1 4
9 2 1 3
10 2 1 3
11 2 1 3
12 2 1 3
13 2 1 3
14 2 1 3
15 2 1 1 4
16 2 2
17 2 1 3
18 2 2
19 2 1 1 4
UNDT 7 7
2 20 2 1 1 4
3 21 2 1 3
22 2 1 1 4
23 2 1 1 4
35 2 1 1 4
36 2 1 1 4
37 2 2
38 2 1 3
4 24 2 1 3
5 25 2 1 3
26 2 2
27 2 2
28 2 2
29 2 1 3
30 2 1 3
31 2 2
UNDT 1 1
6 33 2 2
34 2 1 3
7 32 2 2
8 39 2 1 1 1 5
40 2 2
41 2 1 1 4
42 2 1 3
43 2 2
Total 43 86 4 23 16 8 137





Neotropical Primates 16(1), June 2009


imply a higher level of interspecific competition for space
(Sinchez, 1998) or even predation pressure from Cebus
apella, a species known to hunt and kill small mammals
(Galetti, 1990; Izawa, 1990, Sampaio and Ferrari, 2005;
Defler, com. pers.).

Fragments of less disturbed forests in which floristic inven-
tories were studied showed an acceptable conservation level
and a high density of Callicebus ornatus (368.7 ind/km2).
However, the density of Callicebus ornatus in the secondary
forest was in general higher (mean: 559.1 ind/km2) than
the less disturbed forest (mean: 188.2 ind/km2), suggesting
a preference for secondary forest (Mason, 1968; Hernhn-
dez-Camacho and Cooper, 1976; Polanco, 1992; Sinchez,
1998). According to Quiniones-Porras (2007), who stud-
ied a group in a secondary forest during 4 months (March
to June), the most consumed fruits by C. ornatus during
this period were Miconia .iff',.s. Inga thibaudiana and Mi-
conia elata, as it has been reported in other studies (Po-
lanco, 1992; Sinchez, 1998 & Ospina, 2006). According
to Polanco (1992) and Sinchez (1998) during wet season


C ornatus still consumes Miconia and Inga species but
lower proportions. Additional observations are required to
evaluate fruit feeding preferences in long term studies at
the study area.

The density reported for fragment 1 was 368.7 individu-
als/km2, a similar estimate as the one found by Mason
(1966) of 400 individuals/km2. This fragment seems to
have better conditions than the others, since it is protected
from livestock by fences and has a rich plant assemblage.
Another potential explanation for these high estimates is
the lack of interspecific competition with larger primates
(for instance Alouatta seniculus was locally exterminated for
bushmeat 50 years ago). Yet a third explanation that must
be considered is that these high population densities repre-
sent refugees from destroyed forests. Thus, these may be hy-
perdense populations as a result of forest destruction. This
possibility must be evaluated, especially since much forest
has been destroyed in the area. High population densities
such as the ones found in the fragments could also imply
a high probability of epidemics and endogamy. Long term


Table 2. Age structure of the C. ornatus population.
Adults Sub-Adults Juveniles Infants Total
Counts 86 4 23 16 129
Proportion (%) 66.7 3.1 17.8 12.4 100


Table 3. Population density estimates of C:... 'n ornatus in the forest fragments near Acacias, Meta, Eastern Colombia.
Fragment Area (ha) Groups Individuals Groups / ha Individuals / km2
1 17.63 19 65 1.08 368.7
3 40 7 24 0.18 60.0
5 10 7 18 0.70 180.0
8 10 5 16 0.50 160.0
Total 77.63 38 123
Mean 0.61 192.2 + 128.9


Table 4. Most important plant species in the less disturbed and secondary forests.
Less disturbed forest Secondary Forest
Species RF RD RBA IVI Species RF RD RBA IVI
Socratea exorrhiza 0.108 0.183 0.377 0.668 Casearia sp. 0.105 0.067 0.015 0.187
Oenocarpus bataua 0.097 0.121 0.380 0.598 Apuleia leiocarpa 0.074 0.044 0.017 0.135
Mabea maynensis 0.068 0.074 0.055 0.197 Jacaranda copaia 0.076 0.035 0.005 0.116
Virolasebifera 0.044 0.041 0.028 0.113 .',, morototoni 0.050 0.035 0.005 0.09
Iriartea deltoidea 0.031 0.043 0.023 0.097 Alchornea glandulosa 0.048 0.025 0.002 0.075
Pourouma bicolor 0.033 0.028 0.017 0.078 Guatteria recurvisepala 0.048 0.023 0.002 0.073
Caraipa cf. punctulata 0.029 0.025 0.016 0.07 Sapium laurifolium 0.057 0.001 0.000 0.058
Guatteria recurvisepala 0.029 0.025 0.013 0.067 Loreya strigosa 0.040 0.017 0.001 0.058
Senefelderainclinata 0.031 0.028 0.006 0.065 Himatanthusarticulata 0.033 0.017 0.001 0.051
Lauraceaesp. 2 0.026 0.023 0.010 0.059 Trattinnickia aspera 0.033 0.014 0.000 0.047
RF (Relative frequency), RD (Relative density), RBA (Relative basal area), IVI (Importance Value Index) RF + RD + RBA (Curtis & McIntosh, 1951).





Neotropical Primates 16(1), June 2009


monitoring of populations and studies of genetic diversity
will be necessary to assess the viability of these populations,
especially since they may represent refugees. Given that
fragments are small, only 8.5% forest cover remains and
the permanence of them is uncertain. However, they seem
to have a high probability of survival, as long as the destruc-
tion of forest remnants stops. In the study area individuals
of C. ornatus y S. sciureus were observed walking on the
ground, moving from fragment 1 to 5 (400 m separated).
This represents a predation threat for these primates; we
witnessed a domestic dog killing the infant of the group 7,
when his father tried to gather fruit on the ground. Tree-
fences are important structures that help groups to travel
between fragments and as food sources (Carretero, 2008).
Their use in private lands could be important for primates
and other fauna.

Callicebus ornatus is also found in La Macarena and Ti-
nigua National Parks, but these parks have been affected
by illicit crops and institutional presence has been jeopar-
dized by lack of personal security. About 4,500 ha of coca
crops have been reported in La Macarena park (Acci6n
Social, 2006). The conservation of this endemic primate
in private forests is important for its survival. A conserva-
tion program for the black lion tamarin from the Brazilian
coast on private lands, is showing great success, thanks
to a well constructed environmental education program
where landowners agreed to participate, increasing pro-
tected habitat by about 5,000 ha (Valladares-Pidua et al.,
1994; Kleiman and Mallinson, 1998). Conservation pro-
grams using private lands seem very important to supple-
ment the efforts of the government, and this effort should
be undertaken by all Colombians. It seems important to
restore the quality of Callicebus ornatus habitat to main-
tain healthy populations. Political activism is also neces-
sary to take important actions against forest destruction
in the region: environmental education and laws must be
enforced, forest fragments must be connected and their
areas must be increased to avoid the destruction of forest
remnants in the piedmont and to protect endemic species
in the region.

Acknowledgements

We want to thank Thomas Defler, Diana Guzmin, and
Eckhard W. Heymann for their suggestions and improve-
ments to the manuscript. We thank Fundaci6n Chimbi-
lako and Jos6 Delgado and his SIGAMOS Association for
their cooperation, and Gonzalo Acosta, Anthony Rylands,
Eduardo Plata, Gabriel Guillot, H&ctor Lancheros, Ivan
Sinchez, Jhon Aguiar, Sandra Valderrama, Antonio Qui-
fiones, Maria Juliana Ospina and Xyomara Carretero for
their collaboration. We are grateful to Los Andes Univer-
sity Herbarium, SINCHI and CIEM (Centro de Investiga-
ciones Ecol6gicas La Macarena). This work was supported
by the Primate Action Fund from Margot Marsh Biodi-
versity Foundation (Conservation International Primate
Action Fund 2006-2007).


Marcela Wagner-Medina, Fundaci6n Chimbilako, Bogoti,
Colombia, e-mail: ; Fran-
cisco Castro, Departamento de Agronomia, Universidad
de los Llanos, Villavicencio, Colombia; Pablo R. Steven-
son, Departamento de Ciencias Biol6gicas, Universidad de
los Andes, Bogoti, Colombia.

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ANTHROPOGENIC CHANGE AND PRIMATE
PREDATION RISK: CRESTED CARACARAS
(CARACARA PLANCUs) ATTEMPT PREDATION ON
MANTLED HOWLER MONKEYS (ALOUATTA
PALLIATA)

Tracie McKinney

Introduction

Anthropogenic change in primate habitats may be an im-
portant factor in predation risk. Predation is often con-
sidered a principle selective pressure in primate evolution,
and thus an important determining factor for grouping
behavior, travel patterns, and choice of sleeping sites
(van Schaik, 1983; Isbell, 1994; Treves, 2002; Shultz et
al., 2004). Predation events are rarely witnessed in the
wild due to their rarity, short duration, and the effects
of observer presence. Reports of failed predation attempts
or even the absence of predation events (Boinski et al.,
2000) will broaden our understanding of this impor-
tant issue. With our currently limited scope on primate
predators and risk factors, we may be missing the impact
of human habitat alteration on predation risk and rates.
This paper reports a presumed predation attempt by two
crested caracaras (Caracara plancus) on infant mantled
howler monkeys (Alouatta palliata) in Costa Rica. Crest-
ed caracaras are generally associated with human activity





Neotropical Primates 16(1), June 2009


(Rodriguez-Estrella et al., 1998; Morrison & Humphrey,
2001), suggesting that habitat disturbance at this site may
alter predation risks for these monkeys.

Large-bodied, arboreal howler monkeys should have
fewer potential predators than many other primate genera
(Di Fiore, 2002). Researchers have confirmed predation
by jaguar (Peetz et al., 1992; Chinchilla, 1997), puma,
Puma concolor (Chinchilla, 1997; Ludwig et al., 2007),
ocelot, Leopardus pardalis (Miranda et al., 2005; Bian-
chi & Mendes, 2007) and harpy eagles, Harpia harpyja
(Sherman, 1991) on wild howler monkeys. Predation at-
tempts by black hawk-eagles, Spizaetus tyrannus (Miranda
et al., 2006), crested eagles, Morphnus guianensis (Julliot,
1994), and tayras, Eira barbara (Phillips, 1995; Asensio
& G6mez-Martin., 2002) are also reported in the litera-
ture. While incidences of snake predation on Ateline pri-
mates have not been documented, large snakes may also
be considered a potential threat to juvenile howlers be-
cause they prey on many other Neotropical primates (Di
Fiore, 2002). Birds are the most common predators for
many monkey species, both in the Old and New Worlds.
Only a few Neotropical birds, including the Harpy eagle
(Harpia .'. :., ). the crested eagle (Morphnus guianensis),
and the hawk eagle (Spizaetus spp.), are believed large
enough to capture adult Atelines (Julliot, 1994; Miranda
et al., 2006). Infant howler monkeys, however, are cer-
tainly reasonably sized prey for many Neotropical raptors
(Di Fiore, 2002).

In the observed incident, an apparent predation attempt
on infant howler monkeys (Alouatta palliata) was made
by two crested caracaras (Caracara plancus). The crested
caracara ranges from the southern United States to Tierra
del Fuego and the Faulkland Islands (Travaini et al., 2001;
Henderson, 2002; Vargas et al., 2007). It is a medium-sized
raptor in the falcon family (Falconidae), weighing approxi-
mately 1 kg and with a wingspan of 120-130 cm (Hender-
son, 2002). While they are mostly known as a scavenging
species, caracaras are opportunistic hunters that feed on
a variety of invertebrate and vertebrate prey (Travaini et
al., 2001; Vargas et al., 2007), and may in fact consume
more fresh meat than carrion (Richmond, 1976). Mam-
mals account for nearly one quarter of crested caracara
prey (Vargas et al., 2007). Although the majority of mam-
malian preys are rodents, caracaras are known to prey on
larger animals, such as skunks and young rabbits (Hender-
son, 2002). While caracaras are not confirmed predators
on even small monkeys, a taxidermized caracara did elicit
alarm responses from captive marmosets (Callitrhixpenicil-
lata) in an experimental setting (Barros et al., 2002). Ca-
racaras are particularly suited to act as active predators of
monkeys in anthropogenic environments yet pose relative-
ly little risk in more forested habitats. As open-habitat spe-
cies (Morrison & Phillips, 2000), caracaras thrive in areas
with little tree cover, such as natural clearings and man-
made pastures. They are highly tolerant of human activity,
and are often found hunting and scavenging on farms or


along roadways (Rodriguez-Estrella et al., 1998; Morrison
& Humphrey, 2001). Like many open-area raptors, cara-
caras seek out fragmented habitats, using the forest cover
for nesting while hunting in the fields (Rodriguez-Estrella
et al., 1998; Sinchez-Zapata & Calvo, 1999). Habitat
changes that favor caracara activity may place local wildlife
confined to narrow forest fragments at risk of heavy preda-
tion (Morrison & Phillips, 2000).

Study Population and Observation

The observed event took place at the Refugio Nacional
de Vida Silvestre Curd, a 1,500 ha private "hacienda"
and wildlife refuge in western Costa Rica (9047'43"N,
84055'15"W) (for a complete description of the site see
Baker & Schutt, 2005). The incident was witnessed during
data collection of a long-term project concerning the
impact of human disturbance on mantled howler monkey
(Alouatta palliata) and white-faced capuchin (Cebus ca-
pucinus) ecology and social behavior. Curd is an ideal site
for such studies, as it incorporates a variety of man-made
and natural habitats including primary and advanced sec-
ondary forest, mangrove swamp, mango, banana, coco-
nut, and African oil palm plantations, and open pastures
with living fences. The refuge has a high density of howler
monkeys, with some troops found in entirely anthropo-
genic habitats, others completely removed from human
interaction, and many troops living in territories between
these two extremes. The study troop of mantled howl-
ers presented here ranges through riparian forest, living
fences, mango and banana plantations, and secondary
forest. The troop is fully habituated to human observers,
and regularly encounters tourists, vehicles, and domestic
animals. At the time of this observation, the troop con-
sisted of 30 individuals- 5 adult males, 16 adult females,
and 9 immatures. Comparable troop sizes are common
at Curd; the relevance of such large groups at this site
is not yet clear. The events were recorded through ad li-
bitum observation and continuous focal animal samples
(Altmann, 1974) and were witnessed by two researchers
and two volunteers.

The interaction with the caracaras took place at approxi-
mately 8:25 am on December 12, 2007. The monkeys were
traveling and foraging through a strip of riparian forest be-
tween a cattle pasture and a dirt road. Two females with
small infants crossed a gap in the canopy on an exposed
horizontal branch 12-15 meters in height and approxi-
mately 5 meters long. Such exposed areas are risky for ar-
boreal primates (Isbell, 1994), and these females were trav-
eling quickly and in the presence of an adult male. Both
infants were riding dorsally and appeared 4-6 weeks of age.
The two raptors approached across the open pasture as the
females were in the center of the branch, and swooped at
the monkeys. The birds did not make contact or land on
the branch. Both females ducked as the birds passed over-
head, then hurried along the branch to cover. The entire
interaction lasted less than 30 seconds.





Neotropical Primates 16(1), June 2009


There were few overt anti-predator behaviors from the fe-
males or other troop members. Anti-predator behaviors in
howler monkeys typically include descent and dispersion,
vocalization, and grouping quietly high in the trees (Eason,
1989; Julliot, 1994; Phillips, 1995; Miranda et al., 2006).
In this incident, the nearest adult male howled for about
15 seconds shortly after the event, but a truck was passing
at the same time, so it is unclear whether the vocalization
was in response to the birds or to the motor. After the in-
teraction with the caracaras, the troop continued to forage
and settled down in the same area for their midday rest.
A second observer recorded a single caracara flying through
the trees at 12:36 pm. In this case, there were no interac-
tions or responses from the monkeys. This is the only pre-
dation-related event observed for this monkey troop over a
period of 491.25 hours of data collection. This represents
a predation-related event rate of 0.002 events/hour. Even
though the young howlers survived this interaction, caraca-
ras should now be considered and monitored as a potential
threat to infant monkey survival in edge habitats.

Discussion

Anthropogenic change means much more than habi-
tat loss for non-human primates. The effects of human
disturbance are pervasive, impacting parameters like
foraging patterns, social interactions, and predation. Se-
idensticker (1983) proposed a consideration of preda-
tion when discussing disturbance, noting that primate
predation by big cats depends largely on the availability
of livestock. In the 25 years since, little has been made
of human alteration and predation, and the few reports
that have considered the idea are contradictory. Some
authors suggest that predation rates decrease with close
proximity to humans (Isbell & Young, 1993; Stanford,
2002), while others point out that certain types of preda-
tion may be favorable in anthropogenic habitats (chim-
panzees: Grieser Johns & Grieser Johns, 1995; leopards:
Ludwig et al., 2007). Domestic dogs are now reported in
the literature as effective monkey predators (De Oliveira
et al., 2008; Raguet-Schofield, 2008), and some wildlife
may seek out anthropogenic habitats as well. Certainly
human factors impact predation, but the nature of the
change will be site specific. While we cannot account
for every impact human disturbance places on a primate
community, it is important to realize that wild primates
face different challenges than they would in the absence
of human encroachment. Predation rates may be im-
pacted in a number of ways, namely: (1) predators may
be adverse to human altered habitats, reducing predation
risk; (2) anthropogenic habitats may encourage certain
predators, increasing predation risk; or (3) the predator
assemblage of a habitat changes, with potentially drastic
effects on endemic wildlife that lack the experience and
selection-driven behavioral patterns necessary to avoid
these predators. As primate habitats become increasingly
anthropogenic, their predation risks-and potential
predators-are bound to change.


Acknowledgements

Many thanks are due to the Schutt-Valle family of Refu-
gio de Vida Silvestre Curd, for permission to work on
their land and for their continued friendship. Volunteers
from Earthwatch Institute, Carolina Orozco Zamora, and
Caspar Harris provided excellent field assistance. Dr. Scott
McGraw offered helpful comments on an earlier draft of
this manuscript. This research was funded by generous
support from Earthwatch Institute, Conservation Interna-
tional, and The Ohio State University.

Tracie McKinney, Department of inrl.i. .p..1..;,, The Ohio
State University 4034 Smith Laboratory, 174 W. 18' Ave.,
Columbus, OH 43210.

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113-1.


EARLY BEHAVIORAL DEVELOPMENT OF A FREE-
RANGING HOWLER MONKEY INFANT (ALOUATTA
GUARIBA CLAMITANS) IN SOUTHERN BRAZIL

Luciana Regina Podgaiski
Mdrcia Maria de Assis Jardim

Introduction

In comparison with other mammals, the offspring of pri-
mates undergo a relatively long period of behavioral devel-
opment and dependency upon their mothers. During this
period, the mother is a secure base from which the infant
is able to explore the environment and engage in social
behavior (Vochteloo et al., 1993), acquiring the ecological
skills of the species and the social traditions of the family
troop (Southwick and Siddiqi, 1974). Independence is the
result of a long period of increasing self-sufficiency in ac-
tivities such as locomotion and feeding, as well as growing
sociability and distance from the mother (Altmann, 1980;
Odalia-Rimoli, 1992). Mother-infant ties constitute one
of the most intense types of social relationship in primates
(Harlow and Zimmermann, 1958, Altmann, 1959), and
have a positive effect on infant survival and development.

Howler monkeys (genus Alouatta Lacepede, 1799) are the
most widely-distributed Neotropical primates (Chapman
and Balcomb, 1998), and are also the best studied in the
wild. They occupy a variety of habitat types, and are well-
adapted to anthropogenic fragmentation (Crocket, 1998),
although some species are declining rapidly in the wild and
have been classified as threatened (IUCN, 2009). Howlers
have been translocated and re-introduced at a number of





Neotropical Primates 16(1), June 2009


sites (e.g. Agoramoorthy, 1995), and a critical factor for
such management procedures is the successful handling of
females with nursing infants (Baker, 2002). Knowledge of
the behavioral development of infants can obviously con-
tribute to the efficiency of such procedures (International
Primatological Society, 2007).

Studies of the behavioral development of primate infants
have focused on their social behavior and spatial relation-
ships with their mothers. In howlers, studies have been
conducted on free-ranging Alouatta guariba (Kats and Otta,
1991), Alouatta palliata (Altmann, 1959; Clarke, 1990;
Lyall, 1996), and Alouatta seniculus (Mack, 1979; Cabrera,
1997). Allomaternal care is well documented in female
howlers (Calegaro-Marques and Bicca-Marques, 1993),
but is rare in males (Marques and Adis, 2000). In this
study, the early behavioral development of a male infant
A. guariba clamitans was monitored in a free-ranging group
in southern Brazil.

Materials and methods

Study area and subjects
The study was undertaken in Itapua State Park (3023'S,
5130'W), in the city of Viamao, Rio Grande do Sul,
Brazil, from August 2003 to April 2004. The climate in
the region is temperate, with hot summers and no clear
dry season (Cfa type of K6ppen's classification; Peel et al.,
2007). The home range of the study group was estimated
to be approximately 8.71 ha of semi-deciduous forest on a
granite hillside bordering a sandy beach, known as Pedreira
(Marques, 2001; Jardim, 2005). In August 2003, the study
group was composed of two adult males, one sub-adult
male, one juvenile male, two adult females, and one male
infant (the study subject-see below). Although the exact
date of this infant's birth could not be determined, we es-
timated that it was between two and three months of age,
based primarily on body size (Carpenter, 1934; Altmann,
1959; Kowalewski and Zunino, 2004) and the ontogeny
of independent behaviors. In March 2004, another male
infant was born in the troop, an adult female immigrated,
and an adult male disappeared.

Observation methods
From August, 2003 to April, 2004, the behavior of the
infant male subject was monitored for two days each month,
except October (one day). Data were collected using focal-
animal sampling with continuous recording (Altmann,
1974) from sunrise to sunset (around 9 hours of observa-
tion per day). Samples of three minutes duration were col-
lected at ten-minute intervals, with a total of 810 samples
collected over 155 hours of monitoring. During each
sample, the infant's behavior and its position in relation
to its mother were recorded according to the categories
defined in Table 1. Other behaviors, such as drinking and
rejection by the mother, were recorded in adlibitum fashion
(Altmann, 1974). Nursing was not recorded here because of
the difficulty of determining this behavior reliably.


Results

Infant-mother relationships
In the first month of observations, when the infant was
two or three months old, he spent 86.8% of the day on the
mother, mostly in the ventral position (Fig. 1), although
he was carried on the dorsum during troop movements. In
subsequent months, the infant spent increasingly less time
on the mother. Ventral carrying during troop movements
ceased in November (5-6 months), and dorsal carrying in
December (6-7 months), although ventral and dorsal con-
tact with the mother were recorded up to March and April,
respectively. By the end of the study period, the infant was
in contact with its mother less than 30 percent of the time.

Resting (Fig. 2a)
Initially, the infant spent most of its time at rest, and
almost always rested while being carried by the mother
until 4-5 months old. The infant was observed resting at
a distance from its mother for the first time in Novem-
ber, but this only became common by the end of the study.
By the age of 8-9 months, time spent resting stabilized at
55-60% of observation time.

Locomotion (Fig. 2b)
The earliest bouts of independent locomotion occurred in
September (3-4 months old). This activity increased pro-
gressively until 6-7 months, but was subsequently irregular.
Independent movement of the infant was monitored and
stimulated by the mother, by moving very slowly through
the trees and waiting for the infant to follow. Sometimes,
the mother would move to a branch and emit a vocaliza-
tion until the infant arrived. When crossing a wide gap in
the trees, the mother used her own tail or body as a bridge
or carried the infant on her dorsum.


Figure 1. Mean percentage observation time spent by the
A. infant in different contact categories (see Table 1) in
each month during the study period.


1- Ventral
- Dorsal
-0- In contact
... < Im
-A- > Im


100

S80-

0 60-

0 40-

b 20-


Records











A) REST


B) LOCOMOTION


0 1


D) GROOMING


28 C) FEED

21

14

7 II


-L


1 Ventral
S- Dorsal
S- In contact
S< im
1 > Im


E) INDIVIDUAL PLAY


0 J-


Records


F) SOCIAL PLAY


CA 0 z A


Records


Figure 2. Percentage of time spent by the howler infant in different behaviors and in different forms of contact with its mother during the
study period. See Table 1 for behavior and contact categories.


Neotropical Primates 16(1), June 2009


100

75

50

25


0 --





Neotropical Primates 16(1), June 2009


Feeding (Fig. 2c)
The infant also started eating solid food at 3-4 months.
Initially, the infant was usually either being carried by its
mother or close to her during this behavior, which allowed
it to observe the items ingested by the mother and then
repeat her movements. Contact declined rapidly by the fol-
lowing month. The howlers usually drank water from bro-
meliads, and this behavior was first noticed in the infant
at 8-9 months, the same period when the mother began
rejecting the infant when it tried to nurse.

Grooming (Fig. 2d)
The infant was observed grooming on two occasions. On
the first, he was 4-5 months old, and mimicked his mother
when grooming an adult female. On the second occasion,
at 6-7 months, the infant groomed its mother.

Play (Fig. 2e-f)
The infant already exhibited play behavior when obser-
vations began. The highest frequency occurred at 5-6
months, reaching around 50% of the daily observation
period. After this peak, the behavior tended to decline to-
wards the end of the study. Play almost always took place
when the troop was at rest. During individual play, the
infant explored its immediate environment. Social play
initially involved the infant's mother, and gradually in-
volved a juvenile male. Play was also recorded with the
dominant adult male.

Discussion

While the infant grew progressively independent, it main-
tained relatively close ties with its mother, invariably resting
together, even at the end of the study. Overall, the behav-
ioral development of the infant was similar to that record-
ed in previous studies of howlers (Altmann, 1959; Mack,
1979; Clarke, 1990; Kats and Otta, 1991; Lyall, 1996;


Cabrera, 1997). The transition from exclusive ventral car-
rying in the first few weeks of life to a predominance of the
dorsal position is a typical pattern in monkeys, including
howlers (Altmann, 1959; Mack, 1979; Shoemaker, 1979;
Kats and Otta, 1991; Lyall, 1996; Miranda et al., 2005).
Increasing distance from the mother is also typical. Kats
and Otta (1991) confirmed a progressive increase in dis-
tance from the mother at 3-4 month of age in A. guariba,
while Miranda et al., (2005) found that contact with the
mother declined to 10% of activity time by the fifth month
of age. In the present study, the infant was more than 1 m
from its mother for 6% of the time at 2-3 months old,
increasing to 70% only at 1 year. A possible regression in
this trend was recorded at 7-8 months, however, which
may represent a critical period of insecurity or a regression
in suckling (Horwich, 1989).

According to Mack (1979), prior to six months of age,
howler infants may bite and chew the same type of object
that the adults are eating, but not necessarily consume
it. Maybe, the high feeding percentages observed in the
first months of this study refer to an exploratory feeding
which occurred in contact or near the mother. The stabi-
lization of rest at 55-60% by 7-8 months corresponds
to the typical rate of adults in this study group (Marques,
2001). This stabilization occurred at the same time as the
frequency of play behavior began to decline. Both play
and grooming have an important social function (South-
wick and Siddiqi, 1974). One possible factor determining
rates of social play in the present study was the availabil-
ity of potential partners, i.e. other immature individuals.
Grooming appears to be relatively common in A. guariba
in comparison with other howlers (Kinzey, 1997); this
behavior was part of the behavioral development of the
studied infanWhile behavior patterns are best evaluated
on the basis of a sample of different individuals, the pres-
ent study provides some useful preliminary insights on


Table 1. Howler monkey infant behavioral categories based on proximity to the mother and activity.
Position Description
Ventral Carried by the mother in a ventral position
Dorsal Carried by the mother in a dorsal position
In contact In contact with the mother's body, other than the ventrum or dorsum
< im Less than a meter from the mother's body
> im More than a meter from the mother's body
Activity Description
Rest Sitting or lying
Locomotion Moving independently
Feed Handling, processing or ingesting solid foods
Grooming Sifting through another animal's fur with the hands
Individual play Handling objects, hanging from tail and jumping between branches
Social play Interactions with other troop members involved mock fighting (holding, pulling, baring teeth, and biting) and chasing,
often involving jumping
Drink Ingesting water





Neotropical Primates 16(1), June 2009


the behavioral development of infant howlers of the spe-
cies Alouatta guariba. The patterns observed appeared to
be typical of the genus.

Acknowledgments

We thank Ana Alice B. de Marques for initial advice on
the project; Paula C. Colombo for technical support; Aline
E Quadros, Andre E B. Lima, and Ver6nica G. Sydow for
comments on earlier versions of the manuscript.

Luciana Regina Podgaiski, Programa de P6s-Graduacao
em Ecologia, Instituto de Biociencias, Universidade Fed-
eral do Rio Grande do Sul (UFRGS), Av. Bento Gongalves,
9500; Predio 43422, Postal box: 15007, Porto Alegre, Rio
Grande do Sul, Brazil, and Marcia
Maria de Assis Jardim, Setor de Mastozoologia, Museu de
Ciencias Naturais (MCN), Fundagao Zoobotdnica do Rio
Grande do Sul (FZBRS), Porto Alegre, Rio Grande do Sul,
Brazil

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Neotropical Primates 16(1), June 2009


HUNTING STRATEGY OF THE MARGAY (LEO-
PARDUS WIEDII) TO ATTRACT THE WILD PIED
TAMARIN (SAGUINUS BICOLOR)

Fabiano de Oliveira Calleia
Fabio Rohe
Marcelo Gordo

Introduction

Wild primate predation has been widely reported for vari-
ous Neotropical cat species. Apparently, prey body size
and predator body size are related, with large cats prey-
ing mainly on large primates. Remains from different
species of primates have been observed in scats of differ-
ent Neotropical cat species (Table 1). According to Ca-
brera and Yeppes (1940), primates are the favorite prey
of Puma yaguaroundi in some regions of Central America.
More recently, Miranda et al. (2005), found fingers and
nails from Alouatta guariba clamitans in two fecal samples
from Leoparduspardalis and suggests that the ocelot may
be a potential predator of all Neotropical primates.

In this study, we focus on a hunting technique by the
margay, Leopardus weidii. Morphologically, margays have


arboreal adaptations, but there are no published reports of
the predation strategy of wild margays. The few studies on
the margay suggest that its diet is mainly composed of ar-
boreal mammals. Mondolfi (1986) analyzed the stomach
contents of margay from Venezuela and found remains of
squirrel (Sciurus granatensis) and the wedge-capped capu-
chin monkey (Cebus olivaceus-cited as nigrivittatus, a junior
synonym). Margay prey species in Guyana were also ar-
boreal mammals (Beebe 1925). In captivity, margays were
observed preying on Saguinus niger (Oliveira, 1998).

In the course of our field research on felids, we interviewed
local Amazon jungle inhabitants (woodsmen and mestizo
indians) in different regions of central Amazonia to learn
about the biodiversity of local habitats, and in particular,
the natural history of Neotropical cat species, including
their prey capture techniques. Interestingly, several of the
interviewees described a common predation strategy by
Neotropical cats as attracting their prey by mimicking the
prey species' vocalizations. More than a dozen reports of
Puma concolor, Panthera onca and Leopardus pardalis mim-
icking vocalizations of agoutis (Dasyprocta spp.), tinamous
or nambds (C (:.-. .. sp.) and solitary tinamous or mac-
ucos (Tinamus sp.) were made in different river basins (Ma-
deira, Jurui and Purus) (Table 2). Until now, no scientific
observations of this type of behavior have been published


Table 1. Review of primates predated by Neotropical cat species.
Predator Prey Location Citation
Panthera onca Ateles belzebuth La Macarena, Colombia Matsuda and Izawa (2008)
Alouatta seniculus Venezuela Peetz et al. (1992)
Brachyteles arachnoides Intervales State Park, Southeast Brazil Olmos (1994)
Ateles paniscuss] chamek Peri Emmons (1987)
Puma concolor Ateles., o ot.' Corcovado National Park, Costa Rica Chinchilla (1997)
Ateles.: o, ot. Maya Biosphere Reserve, Guatemala Novack et al. (2005)
Ateles Belzebuth La Macarena, Colombia Matsuda and Izawa (2008)
Alouatta pigra Maya Biosphere Reserve, Guatemala Novack etal. (2005)
Alouatta caraya Mutum Island, Southern Brazil Ludwig et al. (2007)
Ateles chamek Peri Emmons (1987)
Leopardus pardalis Saguinus spp. Goldizen (1987)
Saguinus nigricollis Colombia Izawa (1978)
Alouatta Caratinga Biological Station, Southeast Brazil Bianchi & Mendes (2007)
Brachyteles hypoxanthus Caratinga Biological Station, Southeast Brazil Bianchi & Mendes (2007)
Cebus apella nigritus Caratinga Biological Station, Southeast Brazil Bianchi & Mendes (2007)
Alouatta g. clamitans ChAcara Payquere, Southern Brazil Miranda et al (2005)
Saguinusfuscicollis Peri Emmons (1987)
Saimiri sciureus Peri Emmons (1987)
Puma i Primates Cabrera & Yeppes (1940)
Callithrixjacchus Paraiba State, Northeast Brazil Ximenes (1982)
Leopardus wiedii Cebus olivaceus Venezuela Mondolfi (1986)
Saguinus niger (in captivity) Oliveira (1998)
Cebus apella British Guiana Beebe (1925)





Neotropical Primates 16(1), June 2009


for Neotropical felids. Here we report the first field observa-
tion of margay mimicking behavior, recorded during field
research on the primate pied tamarin (Saguinus bicolor) at
the Reserva Florestal Adolpho Ducke (59 56' 15,71556" W,
02 56' 25,75037" S) in Manaus, Brazil (for a description
of the area, see Ribeiro et al., 1999). In this brief report we
suggest that L. wiedii uses a mimicking strategy to capture
its prey. Our record confirms the reliability of the informa-
tion provided by the local Amazonian inhabitants.

On October 12, 2005, at 9:13 am, a group of eight pied
tamarins monitored by telemetry was feeding in a Mora-
ceae (Ficus sp.). A large vine at 15 meters height connected
the surrounding trees to the fig tree. At 9:18 am, a margay
attracted the attention of a tamarin sentinel (Gordo et al.,
2005) by producing calls similar to those emitted by pied
tamarin pups. The adult male sentinel climbed up and
down the tree to investigate the calls coming from behind
the liana tangles. It assumed a surveillance position and,
using specific calls, warned the group about the foreign calls.
At 9:22 am we observed movements in the vine and keep
hearing the call imitations. At 9:29 am three pied tamarin
individuals were feeding on Ficus sp. while the tamarin sen-
tinel was keeping surveillance. At 9:40 am, four pied tama-
rins climbed up and down the Moraceae in response to the
repeated aggressive calls from the tamarin sentinel. At that
moment, was observed a cat with small body but big feet,
huge eyes and a long tail walking down the trunk of a tree
(like a squirrel); it quickly jumped to a liana that was con-
nected to the fig tree and moved toward where the tamarins
were feeding, about 15 meters away. At this moment, the
sentinel emitted a high scream as the predator approached
the group; and the group fled immediately.

In our observations, the strategy used by Leopardus wiedii
to imitate its prey was not effective in catching Saguinus
bicolor. However, we suggest that this strategy is very effec-
tive in attracting prey, facilitating the attack and reducing
energy expenditure during a possible pursuit. Curiously, all
the potential prey (agoutis, macucos, and nambus) cited by


the Amazonian inhabitants produce extremely acute vocal-
izations, which possibly match the potential repertoire of
felines. In addition, all the aforementioned potential prey
species use vocalizations in intra-specific territorial demar-
cation. This increases the cats' chance of success in attract-
ing prey by imitation.

Acknowledgments

We thank INPA (Instituto Nacional de Pesquisas da
Amaz6nia) for permission to carry out fieldwork at the
Reserva Florestal Adolpho Ducke. The observations re-
ported here were made during a study supported by grant
from PROBIO MMA but we also wish to thank CNPq
to provided financial support to Fabiano Calleia and the
Wildlife Conservation Society (WCS) and Conservation
Leadership Program (CLP) for provided financial support
to Fabio Rahe. We are deeply indebted to several collabo-
rators for their inestimable help in the fieldwork (Projeto
Sauim-de-Coleira) supported by PROBIO/MMA, FNMA/
MMA, WCS, CI, Durrell Wildlife Conservation Trust Ap-
enheul Primate Conservation Trust, Shaldon Wildlife Trust,
La Palmyre Zoo, Newquay Zoo, and Philadelphia Zoo. We
thank M. Benchimol for comments in the manuscript and
B. G. Luize for the interview in Purus River.

Fabiano de Oliveira Calleia, Projeto Sauim-de-Coleira/
UFAM , Fabio Rohe, WCS
- Wildlife Conservation Society ,
Marcelo Gordo, UFAM / Projeto Sauim-de-Coleira
.

References

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Bianchi, R. C. and Mendes, S. L. 2007. Ocelot (Leopardus
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Station, Southeast Brazil. Am. J Primatol. 69:1-6.


Table 2. Reports of mimicking vocalizations of Puma concolor, Panthera onca and Leoparduspardalis.
Location Cat Species Prey Species Imitated
Rio Madeira/2005* Panthera onca Dasyprocta fuliginosa
Rio Aripuana92005* Panthera onca C i
Rio Aripuana/2005* Puma concolor Dasyprocta sp.
Rio Aripuana/2005* Leopardus pardalis C i
Rio Jurua/2004 Leopardus pardalis i
Rio JuruaI2004 Puma concolor C ,i Tinamus sp.
Rio Javari/2009 Panthera onca C i
Rio Purus/2009 Leopardus sp. < undulatus
Rio Urubu/2006 Puma concolor Dasyprocta leporina
Atlantic Forest/2003** Puma concolor i obsoletus
*see R6he 2007 for a description of the area.
** Atlantic Forest location is Serra de Paranapiacaba, Sao Paulo State, Brazil (see R6he etal. 2003; T6foli etal. 2009).





Neotropical Primates 16(1), June 2009


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(Vida, Costumbres y Description). Historia natural Ediar.
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el puma (Felis concolor) y el manigordo (Felispardalis) en
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Federation, Washington, District of Columbia.
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2005. Foraging ecology of jaguar (Panthera onca) and
puma (Puma concolor) in hunted and non-hunted sites
within the Maya Biosphere Reserve, Guatemala. J of
Zool. 267: 167-178.
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tion. Edufma, Sao Luis, Brazil, 220 pp.
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arachnoides. Neotrop. Primates 2: 16.
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tion by jaguar on howler monkeys (Alouatta seniculus) in
Venezuela. Am. J Primatol. 28: 223-228.
Ribeiro, J. E. L. S., Hopkins, M. J. C., Vicentini, A., Soth-
ers, C. A., Costa, M. A. S., Brito, J. M., Souza, M. A.,
Martins, L. H., Lohmam, L. G., Pereira, E. C., Silva, C.
E, Mesquita, M. R. and Proc6pio, L. C. 1999. Flora da
Reserva Ducke: guia de identificaado das plants vasculares


de umafloresta de terra firme na Amazonia Central. INPA,
Manaus, 816 pp.
Rohe, E, Antunes, A. P. and T6foli, C. E 2003. The Dis-
covery of a new sub-population of the black lion tama-
rins (Leontopithecus chrysopygus) at Serra de Paranapia-
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Rio Madeira. In: Py-Daniel, L. R. et al. (Org.). Biodivers-
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T6foli, C. E; Rohe, E; Setz, E. Z. F. 2009. Jaguarundi
(Puma yagouaroundi) food habits in mosaic of Atlan-
tic Rainforest and eucalypt plantations of southeastern
Brazil. Braz. J Biol. 69(3): 631-637.
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Observaciones sobre el contenido estomacal y el compor-
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Nord. de Biol. 5(1): 89-91.


PERUVIAN RED UAKARI MONKEYS (CACAJAO
CALVUS UCAYALII) IN THE PACAYA-SAMIRIA
NATIONAL RESERVE A RANGE EXTENSION
ACROSS A MAJOR RIVER BARRIER

Mark Bowler
Javier Noriega Murrieta
Maribel Recharte
Pablo Puertas
Richard Bodmer

According to Hershkovitz (1987) Cacajao calvus ucayalii,
listed as Vulnerable by the IUCN, (Veiga & Bowler, 2008)
is distributed from the east bank of the Rio Ucayali in
an easterly direction to the Rio Yavari and from the Rio
Amazonas in the north to the Rio Urubamba in the south.
Hershkovitz (1987) also includes the east bank of the lower
Yavari in Brazil, but its presence there has not been con-
firmed and it is possible that museum specimens marked as
collected on the Brazilian bank of the Yavari actually came
from the Peruvian side where this primate is locally abun-
dant. Surveys conducted between 1979 and 1986 (Aquino
1988) showed that the range was much reduced, hunting
having exterminated the species in several areas. Aquino
(1988) suggested that the southern limit is now probably
the Rio Sheshea and that populations close to the Rios
Ucayali and Amazonas have also been reduced and in some
areas populations have been exterminated (Fig. 1). Popula-
tions of Cacajao calvus observed by Peres (1997) on the
upper Rio Jurui and unconfirmed reports by Fernandes
(1990) in the Brazilian state of Acre on the upper Jurui and
Purus are either of Cacajao calvus novaesi or Cacajao calvus
ucayalii, which would extend the known ranges of either of
these subspecies.

The Rio Ucayali is the largest tributary of the Rio Amazo-
nas and at 400-1,200m wide presents a significant barrier
to primate populations. However, the constantly-changing
course of the river means that very large islands of forest





Neotropical Primates 16(1), June 2009


big enough to support small primate populations effec-
tively cross from one side of the river to the other as oxbow
lakes are formed, particularly near the mouth of the river
where it meets the Rio Marafion to form the Rio Amazo-
nas. Cacajao calvus calvus has been found on both sides
of the Rio Amazonas (Sousa e Silva Jdnior and Martins
1999), demonstrating that the ranges of subspecies of
Cacajao calvus can traverse major river barriers. Isolated re-
ports of red uakari monkeys west of the Ucayali on the Rio
Yanayacu, a tributary of the Rio Marafion, running more
or less parallel to the Rio Ucayali, in the Pacaya-Samiria
National Reserve (PSNR) have occurred for a number of
years. Until now, these reports have been unconfirmed. Ru-
moured sightings have emanated largely from the commu-
nity of Yarina on the Rio Yanayacu, a seasonally blackwater
stream about 40m in width flowing exclusively through
white-water varzea forests in the Pacaya-Samiria National
Park. The Yanayacu flows 158 km from Lago El Dorado,
to meet the Rio Marafion 30km upstream from the city of
Nauta. Yarina was founded in the PSNR in the 1980s, and
for this reason most of the adults in the community have
not lived in Yarina or the PSNR all their lives. The NGO
ProNaturaleza has worked with the communities on the
Yanayacu for various years, and has coordinated a success-
ful community-based conservation program here. Hunting
for wild meat is not a principle activity in Yarina, and there
are healthy populations of wild animals.

In September 2006, we made a short expedition to con-
duct interviews in Yarina and search the site for red uakari
monkeys. Although red uakaris were not encountered
during this expedition, several residents of Yarina report-
ed seeing red uakari monkeys, usually in small groups on


Figure 1. The original distribution of Cacajao calvus ucayalii
(Hershkovitz, 1987), the distribution in 1986 (Aquino, 1988)
and the newly discovered population. Map adapted from Aquino
(1988).


the banks of the river. Only two residents of Yarina regu-
larly hunt, and both reported infrequent observations of
groups of 20 or more uakaris. In addition to the recent
observations, 3 older men (one from Yarina and two from
the small nearby village of Arequipa) claimed to have seen
red uakari monkeys years ago, when they used to make
hunting and fishing expeditions into the forest. There was
a high level of consistency between interviews, and con-
siderable detail was given within some of the interviews.
The observations were virtually all within an area of about
200km2 (20,000ha) bounded by a large bend in the Rio
Yanayacu (Fig. 2).

On three days between 3-10-2008 to 5-10-2008, during
investigations on the Rio Yanayacu for a project on Giant
Otters Pteronura brasiliensis, Mark Bowler from the Dur-
rell Institute of Conservation and Ecology and Tony Laiche
from the community of Yarina visited Quebrada Ahuara, a
site highlighted during interviews in 2006 as one where
persistent sightings of red uakaris occurred. At 10am on
3rd October 2008, we encountered a group of red uakaris
near Quebrada Ahuara (0456'19.9"S, 7408'26.1"W)
(Fig. 2). We followed the group for one hour and 10 min-
utes covering at least 900m, but the uakaris were nervous
and fled throughout the encounter. During the follow, we
counted at least six individuals including at least one adult
male, an adult female carrying a baby, a juvenile, and two
older juveniles or sub adults. From the contact calls given
by the monkeys, we estimated that the group contained
at least ten individuals. Four clearly-different individuals
were photographed (Fig. 3). We searched the area around
the sightings for several hours on the following two days,
but were unable to relocate the group. These new observa-
tions and interviews confirm the presence of the species on
the west bank of the Ucayali extending the known range of
Cacajao calvus ucayalii into the PSNR (Fig. 1). Until this
discovery, the only protected area known to contain the
subspecies was the regional Tamshiyacu-Tahuayo Commu-
nal Reserve, and while managing hunting is seen as the
priority in this region (Bodmer 1995), protected areas play


Figure 2. Locations of red uakari sightings on the Rio Yanaya-
cu given in interviews (open triangles) and by Mark Bowler on
3-10-2008 (closed triangle).


A Uakari sightings reported in interviews
A Uakari sighting by Mark Bowler 3-10-08

Qb. Tinflo Yan
PVSoledBd

O. b. Fana Su.
I

Tanbo El nnan


Lago El Doruda


Peru





Neotropical Primates 16(1), June 2009


an important role in national and regional conservation
strategies and conservation projects often focus around
these areas.

The confirmation of red uakari monkeys in the Pacaya-
Samiria National Reserve adds a new primate to the species
list for the reserve, bringing the total number of species to
13. This is an extremely diverse primate community and
one unequalled in areas of extensive vdrzea. The striking
appearance and rarity of this monkey means it is used as a
flagship species and as focus for conservation efforts in the
Peruvian Amazon and will may prove a draw for tourism
on the Rio Yanayacu, even though sightings of the mon-
keys would probably be very infrequent. Tourism already
appears to be working well within the successful manage-
ment plans for the area overseen by ProNaturaleza.


Informal conversations with people from the commu-
nities of Yarina and Manco Capac who were working in
the community guard posts around Lago El Dorado and
on the Yanayacu during our expedition, mentioned that
large groups of uakaris used to inhabit the area around the
community of Manco Capac in the Reserve, on the bank
of the Ucayali River contiguous with the forests around
Quebrada Ahuara. However, the species had not been seen
there for 10 or 20 years. Higher levels of activity on this
river in the past, from illegal loggers and people entering
the reserve to extract resources have probably reduced den-
sities of this primate by hunting. The uakaris observed at
Quebrada Ahuara were very nervous, and fled from inves-
tigators. This suggests that the group may have experienced
hunting in the past. However, the area is now protected by
members of the community of Yarina, who do not hunt


(a) (b)




















(c) (d)

Figure 3. Four recognisably different red uakaris photographed on the River Yanayacu on 3-10-2008 by Mark Bowler; a) Juvenile,
b) juvenile/subadult, c) juvenile/subadult, d) adult male.





Neotropical Primates 16(1), June 2009


this primate. This small population of uakaris would be
extremely vulnerable to illegal hunters entering the reserve
from the Rio Ucayali. Although a detailed census has yet
to be conducted, the population must be extremely small,
may be experiencing inbreeding, and it will require spe-
cial consideration if it is to persist. The population in the
PSNR is the only known population of the subspecies Ca-
cajao calvus ucayalii occurring in the complete absence of
non-flooding terra firme forests. Establishing the size and
composition of this population will be essential in estimat-
ing its viability, and putting in measures for its conserva-
tion. Monitoring the population in the long term might
also give an idea about how this species might fare when
its densities are low. More complete census is therefore re-
quired. Community groups and ProNaturaleza will then
have to consider conservation actions for this primate.

Acknowledgements

These surveys were funded by: The LA Zoo, The Earthwatch
Institute and WCS-Peru. Thanks are due to: ONG ProNa-
turaleza, the community of Yarina (RNPS), Robert Pickles
(DICE), ONG WCS-Perd. Arbildo Uraco Canaquiri, Or-
lando Laiche, Tony Laiche.

Mark Bowler, Durrell Institute of Conservation and Ecol-
ogy Department ofAnrl-. ..-p..1. .;,, Marlowe Building, Uni-
versity of Kent, Canterbury, Kent, CT2 7NR, UK, Javier
Noriega Murrieta, ProNaturaleza Bermddez #791, Iqui-
tos, Perd, Maribel Recharte, Universidad Nacional de la
Amazonia Peruana Pebas #5, Iquitos, Perd, Pablo Puertas,
WCS-Perd Maelcon-Tarapaca #332, Iquitos, Perd, and
Richard Bodmer, Durrell Institute of Conservation and
Ecology Department ofAnrl-.i .p. .1..;.,, Marlowe Building,
University of Kent, Canterbury, Kent, CT2 7NR, UK.

References

Aquino, R. 1988. Preliminary surveys on the population
of Cacajao calvus ucayalii. Primate Conservation 9: 24-26.
Bodmer, R. E. 1995. Susceptibility of mammals to overhunt-
ing in Amazonia. In: Integrating People and 'i ; j. for a
Sustainable Future, J. Bissonette and P. Krausman (eds.),
The Wildlife Society, Bethesda, Maryland, pp. 292-295.
Fernandes, M. C. A. G. 1990. Distribuicao de primates
nao-humanos no estado de Acres e vizinhancas: Um estudo
preliminary. Monograph, Departmento de Ciencias da
Natureza, Universidade Federal do Acre, Rio Branco.
Hershkovitz, P. 1987. Uacaries, New World monkeys of
the genus Cacajao (Cebidae, Platyrrhini): A preliminary
taxonomic review with the description of a new subspe-
cies. Am. J. Primatol. 12: 1-53.
Peres, C. A. 1997. Primate community structure at twenty
Amazonian flooded and unflooded forests. J. Trop. Ecol.
13: 381-405.
Sousa e Silva Jr., J. de, and Martins, E. de S. 1999. On a
new white bald uakari population in Southwestern Bra-
zilian Amazonia. Neotrop. Primates. 7 (4): 119-121.


Veiga, L. M. & Bowler, M. 2008. Cacajao calvus ssp. ucay-
alii. In: IUCN 2008. 2008 IUCN Red List of Threat-
ened Species. . Downloaded on
12 March 2009.


COMUNICACION VOCAL DE UN GRUPO DE TITi
GRIS (SAGUINUS LEUCOPUS) EN MARIQUITA,
COLOMBIA

Luz Helena Rueda
Enrique Zerda Orddnez

Introducci6n

El titi gris (Saguinus leucopus) es un primate arboricola pe-
queno, end6mico de Colombia, que habitat bosques prima-
rios y secundarios y en la actualidad, muchas de sus pobla-
ciones se han adaptado a sobrevivir en habitats altamente
fragmentados y degradados (Fajardo, 2000). La alteraci6n
de sus habitats naturales y otros factors como la caceria y
el comercio ilicito, han puesto en riesgo la supervivencia
de las poblaciones naturales (Defler, 2003). En cuanto a es-
tudios sobre bioacistica de la especie, Blumer y Epple (re-
porte no publicado) realizaron un trabajo sobre el compor-
tamiento y las vocalizaciones de tres machos y una hembra
titi gris, en condiciones de laboratorio. Sin embargo, hasta
el moment no se habian realizado investigaciones sobre el
tema con poblaciones naturales. Aunque Saguinus leucopus
es una especie objeto de interns a nivel national e interna-
cional, lo cual se refleja en las diferentes investigaciones rea-
lizadas enfocadas hacia su ecologia, comportamiento, gen6-
tica, manejo ex situ, entire otras temiticas (Vargas y Solano,
1996; Cuartas-Calle, 2001, 2004; Poveda y Sinchez-Palo-
mino, 2004; Roncancio, 2005; Leguizam6n-Hernindez
et al., 2006; Morales-Jimenez, 2007; Sinchez-Londofo,
2007a, 2007b), adn existen vacios de informaci6n prin-
cipalmente sobre aspects como densidad, distribuci6n,
comportamiento y salud fisica de las poblaciones naturales
actuales. En este sentido, el present trabajo pretend am-
pliar el conocimiento sobre la comunicaci6n vocal de la es-
pecie y aportar informaci6n novedosa desde la bioacistica,
que pueda aplicarse en studios de ecologia poblacional;
especificamente el uso de vocalizaciones como herramienta
en censos y en la estimaci6n de densidades poblacionales
para la especie. Esta investigaci6n present una caracteriza-
ci6n del repertorio vocal de un grupo de Saguinus leucopus,
en la cual se identifican, described y relacionan las vocali-
zaciones con los patrons comportamentales, sexo y edad
de los individuos.

Mtodos

Area de studio
El studio se desarroll6 en San Sebastian de Mariquita, de-
partamento del Tolima, en la casa de la Fundaci6n Segun-
da Expedici6n Botanica-Funbotinica (FSEB) (Fig. 1).
Mariquita esti localizada al norte del departamento del





Neotropical Primates 16(1), June 2009


Tolima a una altura de 535 msnm, a los 7447'54"W y
5 11'42"N. La casa de la FSEB tiene un irea de 4,210 m2
(Rueda, 2003), en la que crecen irboles frutales de gran
porte como mangos (Mangifera indica), cauchos (Ficus
sp.), naranjos (Citrus aurantium), marafones (Anacar-
dium occidentale) y platanos (Musa sapientum) (Poveda,
2000).

Descripcidn delgrupo Funbotdnica
El grupo resident en la casa de la FSEB no se encon-
traba en cautiverio ni semi-cautiverio, pues los animals
no ocuparon dicho espacio por acci6n humana, sino por
efectos naturales. Al parecer una pareja de titis qued6 ais-
lada del Bosque Municipal "Jos6 Celestino Mutis" (cer-
cano a la casa de la Fundaci6n) durante el event de la
Avalancha del Volcan Nevado del Ruiz en el afo 1985,
buscando refugio y alimento en las casas cercanas y esta-
blecidndose en la casa de la FSEB que cuenta con uno de
los solares mis grandes de la vecindad. Por consiguiente,
para efectos de este studio el grupo se consider como
"grupo urbanizado". Durante el period de studio, los
titis se desplazaron libremente de una casa a otra utili-
zando los arboles de los solares y los muros de separa-
ci6n entire las casas y contaban con recursos alimentarios
(frutos, resinas y otras parties vegetativas de las plants de
los solares; insects, entire otros) y refugios para sobrevi-
vir. Sin embargo, el grupo estuvo restringido por la poca
disponibilidad de recursos alimentarios en ciertas 6pocas,
sumada a los intentos de capture por parte de los vecinos
de la casa. Al inicio del studio, el grupo estaba confor-
mado por 11 individuos (7 machos y 4 hembras) y pos-
teriormente en el mes de mayo nacieron dos crias, para
un total de 13 individuos. Se definieron las categories de
edad (cria, juvenile y adulto) con base en el tamafo corpo-
ral, en particular, tamafo de la melena, longitud cabeza-
cuerpo y longitud de la cola. Esto se logr6 s6lo mediante
observaciones a distancia de los individuos, debido a que
no se realizaron captures.


Figura 1. Ubicaci6n de la poblaci6n de Mariquita y vista de la
Casa Funbotanica.


Fase de campo
El trabajo de campo se realize durante los meses de
marzo, mayo y de julio a septiembre de 2002, con un
esfuerzo de muestreo de 1200 horas, correspondiendo
a muestreos de 10 dias por mes. Inicialmente se hizo
el reconocimiento del sitio de studio y la habituaci6n
del grupo a estudiar. Durante esta fase (marzo-mayo y
julio-septiembre) se realizaron observaciones desde las
07:00 hasta las 18:00 horas, con el prop6sito de conocer
el nimero de individuos, establecer su ritmo de activi-
dad e identificar los lugares frecuentados para descanso,
alimentaci6n y demis actividades diarias. Para el reco-
nocimiento de los individuos se consideraron caracte-
risticas particulares tales como sexo, tamafo del cuerpo,
tamafo de la melena y vocalizaciones. Las primeras ob-
servaciones de comportamiento fueron efectuadas desde
las 05:45 hasta las 18:00 horas durante el mes de marzo
de 2002. Se utilizaron los m6todos de muestreo ad li-
bitum y animal focal y el m6todo de registro continue
(Altmann, 1974), con ayuda de binoculars Tasco' 7 X
35 mm y de una cimara de video Sony' CCD-TRV-308,
460x. Se registry la fecha y hora del muestreo, identifi-
caci6n del animal (nombre y/o rasgos distintivos) y des-
cripci6n del comportamiento observado (bisicamente
comportamientos de locomoci6n, exploraci6n, alimen-
tarios, sociales, sexuales y agonisticos).

Durante los meses de mayo y julio a septiembre de 2002
se desarroll6 la fase de grabaci6n de las vocalizaciones,
con un esfuerzo de muestreo de 480 horas aproximada-
mente. Se utiliz6 una grabadora Sony' TCM-5000EV,
casetes Sony micr6fono Sennheiser' ME66 y audifonos
de aro. Para las grabaciones se efectuaron "muestreos del
comportamiento" con registro continue (Zerda 2002);
sin embargo, el tiempo de grabaci6n fue variable, depen-
diendo de la actividad vocal de los titis. Para cada registro
se anot6 la fecha y hora de la vocalizaci6n, el ndmero de
registro, la identificaci6n del emisor, el context (com-
portamiento del animal al emitir la vocalizaci6n y acon-
tecimientos alrededor del mismo) y en algunos casos se
registry la respuesta a la vocalizaci6n emitida. Para algu-
nos registros de grabaci6n no fue possible identificar ni el
emisor ni su comportamiento asociado, asi que s6lo se
cont6 con el registro de la vocalizaci6n.

Digitalizacidn y andlisis de las vocalizaciones
La digitalizaci6n de los vocalizaciones se realize con una
grabadora Marantz' CP 430, en un computador Toshi-
ba' portitil satdlite 2800. Los archives fueron analizados
con el program Syrinx' (Burt 2001) version 2.2 K y se
filtraron para discriminar las vocalizaciones de los titis del
resto de sonidos o ruido ambiental. Se elaboraron espec-
trogramas y en cada uno se midi6 la frecuencia y duraci6n
de la seal fundamental. Se aplic6 estadistica descriptive
a los datos de frecuencia maxima, frecuencia minima y
duraci6n de las vocalizaciones. Se calcul6 una media de
tendencia central (media) y dos medidas de variabilidad
(varianza y coeficiente de variaci6n de Pearson).


N Funbotanica House





Neotropical Primates 16(1), June 2009


Resultados

Caracterizacidn de las vocalizaciones
Se obtuvieron 270 registros de grabaci6n y se identificaron
en total 14 vocalizaciones distintas. La cobertura de mues-
tra (Fagen y Goldman 1977) fue 0= 0.9523. Para clasifi-
car las vocalizaciones se consideraron tres aspects: forma,
propiedades acisticas y referencias "-bli.. 1i,: i. (Blumer y
Epple report no publicado; Proyecto Titi 2009). Se iden-
tificaron 8 categories o classes de vocalizaciones: Silbido,
'chiiih', chirrido, 'pip', chillido, chirrr', 'chirchi' y 'U' inver-
tida. En la Tabla 1 se muestran las frecuencias y duraciones
de cada vocalizac6n.

Catdlogo de vocalizaciones
En la tabla 2 se present el nombre, descripci6n, compor-
tamiento asociado, categoria de edad y/o sexo asociado y
el sonograma de las 14 vocalizaciones identificadas. Los
titis emitieron sefales vocales asociadas a contextos espe-
cificos como alimentaci6n, contact con otros individuos
del grupo a la vista y fuera de ella, desplazamiento, agre-
si6n, juego, alarma y amenaza. Las vocalizaciones 'chiiih'
A y 'chiiih' B fueron especificas de los adults. El chirri-
do A, chirrido B, chillido A y chillido B fueron emitidos
solamente por individuos juveniles. El chirrr' y el 'chirchi'
fueron especificas de las crias. Las vocalizaciones emitidas
por machos y hembras fueron muy similares, aunque se
registraron variaciones (modulaciones) entire ambos sexos,
dentro de la misma categoria de edad.

Discusi6n

Las vocalizaciones emitidas por los titis presentaron fre-
cuencias y duraciones consistentes con los resultados obte-
nidos por Blumer y Epple reporte no publicado) quienes


sefalaron que las vocalizaciones se encuentran entire 0.5 y
11.0 KHz y 0.05 y 1.5 seg, respectivamente. En compara-
ci6n con la informaci6n de Proyecto Titi (2009) sobre las
vocalizaciones de S. oedipus, tambidn existe similitud en las
vocalizaciones emitidas; particularmente, se observa una
relaci6n entire las frecuencias fundamentals, cuyo rango
oscila entire 2.0 y 11.0 KHz. Es de esperar que dos species
cercanamente emparentadas produzcan vocalizaciones si-
milares en cuanto a propiedades acdsticas y significado. Tal
es el caso de la combinaci6n de sefales para reconocimien-
to individual y para brindar informaci6n sobre sucesos en
el ambiente (por ejemplo, llamadas de alarma), vocalizacio-
nes ampliamente estudiadas en la especie S. oedipus (Cleve-
land y Snowdon, 1982; Weiss, 2001; Weiss y Hauser, 2002;
Sproul et al., 2006).

El silbido A fue la vocalizaci6n asociada especificamen-
te a contextos alimentarios, en particular aproximaci6n,
manipulaci6n y consumo de alimento. El grupo prefiri6
recursos en fruto como los mangos (cuya disponibilidad
depend de la 6poca de fructificaci6n), tal como lo registra
Poveda (2000) y cuando los consume se incrementa la
frecuencia, duraci6n y el ndmero de silbidos de este tipo.
Los 'chiiihs' fueron las vocalizaciones mais fuertes o agudas
y se asociaron a comportamientos de contact con aque-
llos individuos que estan fuera de vista. Mediante algunos
experiments de 'playback', se observ6 que los individuos
se acercaron a la fuente sonora (adn estando a grande dis-
tancias) y exploraron el lugar, posiblemente para ubicar la
fuente de emisi6n. Estos resultados sugieren que la seal
comunica la ubicaci6n de los individuos y permit la co-
hesi6n e integraci6n del grupo, por lo tanto podria atri-
buirsele la funci6n de llamada. Blumer y Epple reporte no
publicado) identificaron unas vocalizaciones como 'cheeeh'
con caracteristicas similares a los 'chiiihs' de este studio e


Tabla 1. Medidas estadisticas de las frecuencias y duraciones de las vocalizaciones.
Media Varianza Coeficiente deVariaci6n (%) Valor miximo Valor minimo
Vocaliz. n E mix. E min. Dur. E mix. E min. Dur. E mix. E min. Dur. Frec. Dur. Frec. Dur.
(KHz) (KHz) (seg) (KHz) (KHz) (seg) (KHz) (KHz) (seg) (KHz) (seg) (KHz) (seg)
SilbidoA 85 8.40 4.750 0.067 4.750 0.318 0.0001 12.434 11.872 17.89 10.947 0.114 3.235 0.035
Silbido B 16 8.25 5.588 0.478 0.208 0.314 0.016 5.529 10.038 27.204 9.472 0.742 4.761 0.272
'Chiiih'A 3 9.537 6.831 1.815 1.067 0.993 0.545 10.832 14.591 40.67 10.428 2.54 5.681 1.064
'Chiiih'B 2 7.563 4.047 2.895 3.109 1.375 0.169 23.312 28.983 14.23 8.810 3.186 3.217 2.604
'Chiiih' C 7 7.737 6.357 0.678 2.078 2.142 0.121 18.632 23.025 51.28 8.975 1.128 3.856 0.182
ChirridoA 8 6.483 4.103 0.711 0.273 0.663 0.022 8.070 19.844 21.10 6.961 0.906 2.882 0.499
Chirrido B 11 10.634 4.422 0.576 0.784 0.260 0.025 8.326 12.059 27.743 11.025 0.82 3.327 0.278
'Pip' 58 3.560 3.160 0.058 0.052 0.037 0.0001 6.424 6.158 23.598 4.570 0.108 2.790 0.002
ChillidoA 10 8.793 3.570 0.654 0.436 0.780 0.099 7.515 24.741 48.12 10.091 1.2 2.004 0.130
Chillido B 3 9.031 3.292 0.606 0.035 0.286 0.002 2.096 16.264 7.697 9.241 0.66 2.712 0.572
Chillido C 4 5.686 3.198 0.420 1.174 0.232 0.021 19.057 15.074 34.966 6.726 0.64 2.553 0.335
'Chirr' 4 6.076 4.260 0.499 0.132 0.211 0.092 5.990 10.781 60.972 6.615 0.956 3.683 0.335
'Chirchi' 2 6.679 3.476 2.547 0.011 0.004 0.0001 1.577 2.0202 0.499 6.754 2.556 3.426 2.538
'U' invertida 44 7.164 4.055 0.115 0.539 0.169 0.002 10.252 10.158 40.211 9.364 0.222 2.205 0.039





Neotropical Primates 16(1), June 2009


igualmente correspondieron a las sefiales mris fuertes. Los
chirridos fueron vocalizaciones especificas de los juveniles,
no registradas en adults ni en crias. Esta particularidad
permit sugerir que los chirridos pueden utilizarse para
identificar individuos juveniles en studios sobre compo-
sici6n de grupos silvestres. La vocalizaci6n 'pip' comunic6
la presencia de objetos inquietantes o que pueden cons-
tituir una amenaza. Se observ6 que los titis emitieron
'pips' cuando una persona se les aproxim6 demasiado y


el ndmero de ellos estuvo condicionado al nivel del esti-
mulo, es decir, entire m~s cercano el objeto estimulante
mayor cantidad de 'pips'. Los individuos que escucharon
esta vocalizaci6n respondieron con este mismo tipo de
vocalizaci6n, con otras vocalizaciones de alarma o con vo-
calizaciones entremezcladas. Esta vocalizaci6n present ca-
racteristicas similares con la vocalizaci6n 'peep' identificado
por Blumer y Epple reporte no publicado). El chillido A
se registry en algunas ocasiones asociado a contextos de


Tabla 2. C ar Il.... de vocalizaciones del grupo de Saguinus leucopus localizado en la casa Funbotinica. A: adulto, J: juvenile, C: cria,
M: macho, H: hembra.
Categoria de Descripcin Comportamiento Edad Sonograma
No. Descripci6n ciaSonograma
Vocalizaci6n Asociado Sexo
001 Silbido A Monosilaba asociada a contextos alimentarios. Alimentario: aproximaci6n, A, J, M,
Dependiendo del nivel de estimulaci6n del manipulaci6n e ingesti6n de H
animal, se registran secuencias desde dos hasta alimento
apr6x. ocho vocalizaciones



002 Silbido B Monosilaba para establecer contact con otros Movimiento: desplazamien- A, J, M,
individuos. Despues de enviar esta vocalizaci6n, tos. H
pueden emitir vocalizaciones de llamada ('chiiih') Social: contact con otros
individuos del grupo i



003 'Chiiih' A Vocalizaci6n conformada por dos silabas de Social: para integraci6n del A, M, H ,
frecuencia creciente, emitida para 'llamar' a los grupo r
demrs del grupo cuando estin fuera de contact
visual




004 'Chiiih' B Vocalizaci6n trisilibica de frecuencias crecientes, Social: para "llamar" a los A, M, H
emitida al igual que el anterior, para ubicar a miembros del grupo. Inte-
individuos que estin distantes y fuera de con- graci6n y cohesi6n grupal i
tacto visual B




005 'Chiiih' C Monosilaba muy similar a los 'chiiihs' de Social: ubicaci6n dentro del A, J, C, 7
llamada, pero su frecuencia es inferior. Se tienen grupo e integraci6n con los M, H F6
algunos registros en los que emiten esta vocaliza- demas individuos
ci6n junto con una o dos mas, de caracteristicas 4
similares


006 Chirrido A Vocalizaci6n emitida por juveniles Alimentario: J, M, H
Forrajeo.
Movimiento y exploraci6n



007 Chirrido B Vocalizaci6n combinada (es decir, multisilibica, Alimentario: b6squeda y J, M, H
conformando una unidad vocal) caracteristica de manipulaci6n del alimento '
los juveniles, emitida en diferentes contextos Movimiento: diferentes .,
desplazamientos
4 **





Neotropical Primates 16(1), June 2009


pacificaci6n de la agresi6n o resoluci6n del conflict; uno
de los siete contextos en los que ocurre el intercambio de
informaci6n (Bradbury y Vehrencamp, 1998) y la duraci6n
de esta vocalizaci6n podria estar condicionada al nivel de
agresi6n. Blumer y Epple reporte no publicado) identifi-
caron una vocalizaci6n 'chee' con caracteristicas similares al
chillido A aqui reportado, y fue emitida dnicamente por la
pareja dominant durante encuentros agonisticos con otros


individuos. El chillido B fue emitido durante contextos de
juego, por lo general estuvo acompanado de otras vocali-
zaciones como chirridos y sefiales tactiles, caracterizando
contextos de agresi6n de tipo lidico; lo cual fue observado
en los dos juveniles del grupo.

Las caracteristicas y el significado especifico de las voca-
lizaciones chirrr' y 'chirchi' no fueron definidos, debido a


Tabla 2. cont'd. C ar ... de vocalizaciones del grupo de Saguinus leucopus localizado en la casa Funbotanica. A: adulto, J: juvenile, C: cria,
M: macho, H: hembra.

No. Categora de Comportamiento Edad So
Vocalizaci6n Asociado Sexo
008 'Pip' Monosilaba producida al estar en contact visual Defensa: para protecci6n del A, J, M,
cercano con objetos que general inquietud o que grupo ante posibles amena- H 3.*
pueden constituir una amenaza. Se presentan zas o predadores potenciales. 3.4
secuencias de dos hasta 15 6 mas vocalizaciones, 3.2 *
dependiendo del grado de motivaci6n del animal Tim

009 Chillido A Vocalizaci6n combinada, emitida cuando Comportamiento ago- J, M, H .
ocurren encuentros agresivos entire dos o mas nistico: resoluci6n de F .
individuos y su duraci6n podria defender del conflicts.
nivel de agresi6n Juego



010 Chillido B Vocalizaci6n combinada, emitida en contextos Comportamiento agonis- J, M, H
de juego y por lo general va acompafnada de tico. .
chirridos; constituyendose junto con estos, en las Juego
vocalizaciones mas caracteristicas de los juveniles

T..2 E6 8


los juveniles en diferentes contextos plazamientos y exploraci6n H
Social: juego y contact con
otros individuos



012 'Chirr' Vocalizaci6n combinada emitida por las crias con Movimiento: desplaza- C, M, H
various significados miento, exploraci6n. ''
Social: contact con otros
individuos.
Alimentario: solicitud de Z 4
alimento me e 1

013 'Chirchi' Vocalizaci6n combinada con cinco silabas, las Movimiento: exploraci6n, C, M, H
dos primeras similares al chirr y las otras tres diferentes desplazamientos.
semejan un 'chi' Social





014 'U' invertida Monosilaba emitida cuando existen amenazas Defensa y comportamientos A, J, M,
como la presencia de predadores. Producen antipredadores H
secuencias numerosas dependiendo del grado de
estimulaci6n del individuo

4 2-





Neotropical Primates 16(1), June 2009


que el tamafo de muestra no fue representative para tener
informaci6n concluyente al respect. Blumer y Epple (re-
porte no publicado) no identificaron sefales especificas
de las crias, debido a que ellos trabajaron con individuos
adults, por consiguiente estas sefales son registros nuevos
para la especie. Es probable que los titis en las primeras
etapas de desarrollo envien vocalizaciones poco definidas y
repetitivas como ocurre en el lenguaje human, particular-
mente lenguaje infantil; aspect lingiiistico denominado
reduplicaci6n (Martin, 2006). Ademis, emitir vocalizacio-
nes dificiles de identificar, especialmente por predadores,
podria constituir una estrategia adaptativa y de supervi-
vencia (Bradbury y Vehrencamp 1998). Los comporta-
mientos de alarma ante predadores estuvieron asociados la
vocalizaci6n de 'U' invertida. Cuando los titis escucharon
los ladridos de un perro, respondieron aproximindose al
'predador' hasta una posici6n segura y emitieron una se-
cuencia numerosa de estas vocalizaciones, acompafada de
conductas tales como erguimiento del cuerpo. En otras
ocasiones cuando el estimulo no fue auditivo sino visual,
es decir, el perro no ladr6, sino fue observado, la respues-
ta fue la misma y se increment6 cuando el "predador" se
acerc6 mris o exhibi6 movimientos bruscos como brincos
y correteos. Un studio con S. oedipus (Friant et al., 2008)
sugiere que los individuos no reconocen vocalizaciones de
los predadores, pero pueden responder a sefales visuales
como tamafo corporal grande o movimientos corporales
bruscos, lo que podria indicar amenaza o agresi6n; esti
podria ser la explicaci6n a la emisi6n de sonidos por parte
de los titis ante un estimulo visual y no auditivo. Blumer
y Epple reporte no publicado) describieron una categoria
denominada 'V' invertida, que redne tres tipos de sefales
('chat', 'chatter' y 'tsik') con caracteristicas muy parecidas
a la vocalizaci6n de 'U' invertida de este trabajo y aso-
ciada a contextos de amenaza y alarma ante la presencia
de predadores.

La presencia de vocalizaciones especificas de cada categoria
de edad (adulto, juvenile, cria) puede deberse a que la pro-
ducci6n de las vocalizaciones varia de acuerdo a la etapa de
desarrollo del individuo, aspect identificado en S. oedipus
(Roush y Snowdon, 1999). En esta especie, las llamadas
de los subadultos y los juveniles son similares, pero difie-
ren de los adults, debido a que exhiben variaciones en
estructura y significado. Por ejemplo, los juveniles y los
subadultos produce 'chirps' asociados al alimento ante
la presencia de otros objetos (no alimentos) y cuando en
realidad el recurso no esti disponible. El 'chiiih' C fue
emitido por las tres categories de edad y bajo distintos
contextos. Es possible que el titi gris como otras species de
primates exhiba plasticidad vocal en respuesta a alteracio-
nes en la composici6n del grupo social, lo cual puede ocu-
rrir en cualquier etapa del desarrollo del individuo como
lo sugieren Snowdon y Elowson (1999). Sumado a esto,
Zuberbiihler (2002) sugiere que los primates no-humanos
podrian tener la capacidad cognitiva de cambiar el signifi-
cado de las vocalizaciones (sintaxis 16xica), contextualizan-
do dicha plasticidad vocal.


Agradecimientos

Esta investigaci6n se desarroll6 con el apoyo de la DIB (Di-
visi6n de Investigaci6n de la sede Bogoti, de la Universidad
Nacional de Colombia), la Fundaci6n Segunda Expedici6n
Botinica, la Pontificia Universidad Javeriana y la Fundaci6n
Natura Colombia. Tambidn agradecemos a Maria Claudia
Diazgranados de la Fundaci6n Omacha y Carlos Andr5s
Botero del Departamento de Neurobiologia y Comporta-
miento de la Universidad de Cornell, por sus asesorias en el
analisis de las vocalizaciones; a los integrantes de Cabildo
Verde de Mariquita, a Orlando Velisquez y Te6filo Ochoa,
por su colaboraci6n con el trabajo en campo.

Luz Helena Rueda y Enrique Zerda Ord6fiez, Grupo de
Investigaci6n en Comunicaci6n Animal. Departamento de
Biologia, Universidad Nacional de Colombia sede Bogoti.
Carrera 30 No. 45-03, Edificio: 421, Of. 142 E. E-mail:
, .

Referencias

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Burt, J. 2001. SYRINX-PC. A Windows program for spec-
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respond similarly to vocalizations of predators and sym-
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M. I. 2006. Aplicaciones de los analisis gen&ticos pobla-
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communication. Anim. Behav. 63(2):293-299.


OWL MONKEY VOCALIZATIONS AT THE PRIMATE
RESEARCH INSTITUTE, INUYAMA

Sachi Sri Kantha
Hiroki Koda
Juri Suzuki

Introduction

Quantitative evaluations of vocalizations of nocturnally
active owl monkeys (Aotus species) have been attempted
only twice (Andrew, 1963; Moynihan, 1964). Andrew
(1963) identified four call types (twitter-trill, sharp call,
boom and squeak) in two captive individuals, and Moyni-
han (1964) identified six call types (low trill, gulp, grunt
complex, moan, scream and hoot) in a quasi-wild simula-
tion. These two reports record the study subjects as belong-
ing to Aotus trivirgatus species and pre-date the current re-
vision of Aotus genus into nine species (Hershkovitz, 1983;
Ford, 1994). Their subjects would now be classified as
A. lemurinus griseimembra, ranging from Colombia to east
and extreme northeastern Venezuela, as described by Ford
(1994). As such, they are representative of the gray-necked
group, distributed in the regions north of Amazon River. It
is unknown whether the other clade of owl monkeys, the
red-necked species group also produces identical call types.
The objective of this study was to identify the call types
produced by members of captive A. azarae, a species that
belongs to the red-necked group distributed in the regions
south of Amazon River (Ford, 1994). Preliminary results
of this study have appeared in abstract format (Sri Kantha
et al., 2004).

Methods

Subjects and maintenance
The subjects of this study were 16 owl monkeys (12
A. azarae pure breds and 4 Aotus hybrids of red-necked
types) reared at the Kyoto University's Primate Research
Institute (PRI) facility. All, excluding one founder member
from Bolivia, were captive born and have been studied since





Neotropical Primates 16(1), June 2009


2002 as previously reported (Sri Kantha and Suzuki, 2006;
Suzuki and Sri Kantha, 2006; Sri Kantha et al., 2007). All
experiments were carried out following approval from the
Research Committee of the Institute, and according to the
Primate Research Institute's Guidelines for the Care and
Use of Laboratory Primates.

Acoustic Analysis of Vocalization Behavior

Under the premise that the vocalizations of dark-active owl
monkeys have to be studied in the dark without distraction
to the study subjects, we avoided using vision-enhancing
goggles or other supporting aids to identify the individual
monkeys eliciting the vocal notes. As such, the group vo-
calization behavior of 16 monkeys in the colony room was
studied in two installments.

(A). Pilot observations: Pilot observations were made by one
or two researchers, standing quietly in the colony room
for 60-120 min during the dark phase for one session to,
(a) distinguish the call type sounds, and (b) to allow the
monkeys to become habituated to the researchers and the
recording equipment. Two hundred and forty hours were
spent on this installment.

(B). Sampling observations for acoustic analysis: Sampling
observations were carried out in four sessions on separate
days. The length of each session varied between 60 min
and 240 min. Spontaneously elicited calls of the colony
members as a group during dark cycle were recorded
by digital audiotape recorder (Sony TCD-D100) con-
nected to a hand-held microphone (Sony ECM-672) by
ad libitum sampling with minimum interference. During
recording, the two researchers and the recording equip-
ment were stationary and the recording distance varied
between 0.5 m proximall cage) and 6.0 m (distal cages).
Scream vocalizations were also elicited and recorded in
one member, in response to the threat of trapping by net,
during the light cycle (Moynihan, 1964). Sound spectro-
grams of vocal repertoires were analyzed by Multi Speech
Signal Analysis Workstation Model 3700 ver. 2.21 (Kay El-
emetrics Corp.), as described previously (Koda, 2004), to


Table 1. Categories and acoustic properties of Owl monkeys calls.
Mean Values of Acoustic Properties
Call Category ----------------
Duration (sec) Bandwidth (Hz)
Moan' 0.41 140-300
Long scream2 0.26 2,800-5,800
Gulp' 0.054 1,800-5,800
Low trill1 0.052 2,000-3,100
Short scream2 0.19 980-3,300
Sneeze grunt1 0.050 1,580-3,310
1 Based on a representative 1-hour recording period in dark phase. Thirty-
nine calls were recorded and distinguished.
2 Specifically elicited from a female hybrid individual by threat induction
due to net capture, under light phase.


quantify frequency and duration of calls. On the basis of
these two acoustic parameters, a cluster analysis was carried
out to identify the different call types. For conformity, we
adhered to the call type t, iin. .1. ._ ,- introduced previously
for owl monkeys by Moynihan (1964). Data collection
began in October 2002 and ended in April 2004.

Results

From the recorded and analyzed vocal repertoire of the owl
monkey colony we distinguished six categories of acoustic
call types. Table 1 shows the six categories of calls elicited
during a 60 min recording session. Four call types, the
sneeze grunt, low trill, gulp and moan (in the increasing
order of mean duration, from 50 to 410 msec.) were re-
corded in the dark period spontaneously without any
threat stimulus. Among these four call types, the moan
call with the longest mean duration (410 msec.) had the
lowest bandwidth range of 140-300 Hz (Fig. 1). The
mean duration of the other three call types varied only
by 4 msec.; their bandwidths ranged between 1,580 and
5,800 Hz. During the recording period, low trill was the
most frequent and sneeze grunt was the least frequent call.
We also elicited two categories of scream call (short scream
and long scream) from one Aotus hybrid female by threat
induction due to net capture under light conditions. As
shown in Fig. 1, the bandwidth range of short scream
(980-3,300 Hz) and long scream (2,800-5,800 Hz) varied
markedly, and the difference in mean duration between the
two screams was only 70 msec.

Discussion

Andrew (1963) identified four call types (twitter-trill,
sharp call, boom and squeak) in two captive grey-necked
owl monkeys. Moynihan (1964) identified six call types
(low trill, gulp, grunt complex, moan, scream and hoot) in
captive grey-necked owl monkeys. We were able to confirm
the presence of five of the six specific call types, excluding
hoot, reported by Moynihan (1964) in the 12 red-necked
owl monkey subjects. Considering the restraints of captiv-
ity, we acknowledge that not all call types of red-necked
owl monkeys may have been elicited during our recording.
For example, we did not record the short sequence pure
tone hoots, audible to humans in the night at a distance of
500 meters, as reported in the descriptive records of natu-
ralists (Moynihan, 1964). The frequency range of noctur-
nally active Aotus monkey (140-5,800 Hz) vocalizations
are narrow compared to the determined frequency range of
vocalizations of other diurnally active, small-framed Plat-
yrrhine monkeys such as Cebuella pygmaea (800-14,000
Hz), C .-' spp. (500-14,800 Hz), Saguinus spp.
(1,150-10,400 Hz) and Saimiri spp. (500-11,250 Hz),
as tabulated by Hauser (1993). However, the frequency
ranges of owl monkeys (this study, Moynihan 1964) are
identical to that of diurnally active, large-framed Platyr-
rhini such as Cebus spp. (500-6,500 Hz) and Ateles spp.
(200-3,800 Hz), as reviewed by Hauser (1993).




Neotropical Primates 16(1), June 2009


5k




c 2.5k

I-


20k




10k


500msec


5.Short scream









500msec


20k




10k


4. Low Trill


500msec


500msec


Figurel. Representative sound spectrograms of six call categories of Aotus azarae monkeys. In all six frames, X-axis indicates time (mil-
lisec.) and Y-axis indicates frequency (kHz).


20k




10k


1. Moan




-. B '--
--- -. -- --


2. Long scream


I0'






500msec


Time


500msec


20k




10k










20k




10k


6. Sneeze grunt





Neotropical Primates 16(1), June 2009


In sum, with respect to frequency bandwidth and call
duration, we have confirmed the six categories of calls re-
ported for captive gray-necked Aotus recorded in Panama,
in captive-born individuals of red-necked Aotus of Bolivian
origin. The practical necessity of collecting acoustic data of
owl monkeys in the dark somewhat hinders the precision
of assembled data due to difficulty identifying the subjects
generating the calls. As such, the reported vocalization data
of owl monkeys in this study as well as earlier reports of
Andrew (1963) and Moynihan (1964) need additional
confirmation from carefully controlled playback studies
(Byrne, 1982).

Sachi Sri Kantha, Section of Pharmaceutical English, Gifu
Pharmaceutical University, 5-6-1 Mitahora higashi, Gifu
502-8585, Japan , Hiroki Koda,
Cognition and Learning Section, Dept of Behavioral and
Brain Sciences, Kyoto University Primate Research Insti-
tute, Inuyama City 484-8506, Japan, and Yuri Suzuki,
Center for Human Evolution Modeling Research, Kyoto
University Primate Research Institute, Inuyama City 484-
8506, Japan.

References

Andrew, R. J. 1963. Origin and evolution of the calls and
facial expressions of the primates. Behaviour 20: 1-109.
Byrne, R. W. 1982. Primate vocalizations: structural and
functional approaches to understanding. Behaviour 80:
241-258.
Ford, S. M. 1994. Taxonomy and distribution of the owl
monkey. In: Aotus-The Owl Monkey, Baer, J. E, Weller,
R. E. and Kakoma, I. (eds.), pp. 1-57. Academic Press,
San Diego.
Hauser, M. D. 1993. The evolution of nonhuman primate
vocalizations: effects of phylogeny, body weight and
social context. Am. Nat. 142: 528-542.
Hershkovitz, P. 1983. Two new species of night monkeys,
genus Aotus (Cebidae, Platyrrhini): A preliminary report
on Aotus taxonomy. Am. J. Primatol. 4: 209-243.
Koda, H. 2004. Flexibility and context-sensitivity during
the vocal exchange of coo calls in wild Japanese macaques
(Macacafuscatayakui). Behaviour 141: 1279-1296.
Moynihan, M. 1964. Some behavior patterns of platyr-
rhine monkeys. I. The night monkeys (Aotus trivirgatus).
Smithsonian Miscellaneous Collections 146(5): 1-84.
Sri Kantha, S., Koda, H. and Suzuki, J. 2004. Basic rest ac-
tivity cycle (BRAC) rhythm and vocal repertoires of owl
monkeys (Aotus sp). Folia Primatol. 75 (suppl.1): 417.
Sri Kantha, S. and Suzuki, J. 2006. Sleep profile and lon-
gevity in three generations of a family of captive Bolivian
Aotus. Int. J Primatol. 27: 779-790.
Sri Kantha, S., Suzuki, J., Hirai, Y. and Hirai, H. 2007.
Sleep parameters in captive female owl monkey (Aotus)
hybrids. Neotrop. Primates 14: 141-144.
Suzuki, J. and Sri Kantha, S. 2006. Quantitation of sleep
and spinal curvature in an unusually longevous owl
monkey (Aotus azarae). J Med. Primatol. 35: 321-330.


MANEJO COMUNITARIO DE LA CACERIA DE
SUBSISTENCIA EN LACHUA, GUATEMALA

La caceria de animals silvestres para consumo domestico
forma parte de la identidad de muchas comunidades indi-
genas del irea rural de Guatemala. En la ecoregi6n Lachui
habitan 55 comunidades Maya-Q'eqchi' que poseen pricti-
cas tradicionales de aprovechamiento de recursos, como es la
caceria. En el afio 2000, la Escuela de Biologia de la Univer-
sidad de San Carlos de Guatemala inici6 un studio de car-
acterizaci6n de la caceria de subsistencia en las comunidades
aledafias al Parque Nacional Laguna Lachud. En el 2004,
un equipo transdisciplinario empez6 a promover esfuerzos
participativos y consensuados, orientados al manejo comu-
nitario de la caceria de subsistencia; y desarroll6 el Programa
de Educaci6n Ambiental Bilingiie Participativo, el cual se
esti implementando actualmente. Este proyecto esti siendo
construido y planificado con autoridades, lideres y organiza-
ciones de 21 comunidades locales, organizaciones guber-
namentales y ONGs que trabajan en la ecoregi6n Lachui,
constituyendo un fuerte vinculo entire la conservaci6n de la
vida silvestre y el conocimiento traditional y cosmovisi6n
Maya-Q'eqchi'. Para mayor informaci6n visitar www.or-
condeco.org, o comunicarse con Marleny Rosales marleny.
rosales@gmail.com


CAPTIVE CARE AND CONSERVATION OF
CALLITRICHIDS AND LEMURS

Durrell's International Training Centre (ITC), in conjunc-
tion with the Mammal Department are running the course
Captive Care and Conservation of Callitrichids and Lemurs.
The course will be based at the ITC at Durrell's headquar-
ters on the island of Jersey, British Channel Islands, from
September 28th October 2nd, 2009. The main topics will
include: Planning your captive collection: making the link
to the wild; Enclosure design, stress management and nutri-
tion; Population management for controlled breeding pro-
grammes; Past, present and future for callitrichid and lemur
conservation, and the role of zoos. For further details con-
tact Catherine Burrows at catherine.burrows@durrell.org


THE MOHAMED BIN ZAYED SPECIES
CONSERVATION FUND

The Mohamed bin Zayed Species Conservation Fund is a
significant philanthropic endowment established to pro-
vide targeted grants to individual species conservation
initiatives, to recognize leaders in the field of species con-
servation, and to elevate the importance of species in the
broader conservation debate. The fund's reach is truly global,
and its species interest is non-discriminatory. It is open to





Neotropical Primates 16(1), June 2009


applications for funding support from conservationists
based in all parts of the world, and will potentially sup-
port projects focused on any and all kinds of plant and
animal species, subject to the approval of an independent
evaluation committee. For more information visit: www.
mbzspeciesconservation.org/


SEED DISPERSAL By GOLDEN-HANDED
TAMARINS (SAGUINUS MIDAS) IN BROWNSBERG
NATUURPARK, SURINAME: PRELIMINARY
RESULTS

Brian W. Grafton, Ph.D and E. Natasha Vanderhoff,
Ph.D conducted a preliminary study of seed dispersal by
golden-handed tamarins (Saguinus midas) during June
2008 in Brownsberg Natuurpark, Suriname in prepara-
tion for a long-term study of the importance of small-
bodied primates as seed dispersers. We collected 22 dung
samples containing the seeds of 11 plant species from an
unhabituated group at a single dispersal site (a Ficus spp.
tree used as a feeding tree). The recovered seeds varied in
size from 0.48 cm to more than 1.5 cm (largest dimen-
sion), and belonged to a minimum of six plant families
(Apocynaceae, Caesalpiniaceae, Chrysobalanaceae, El-
aeocarpaceae, Rubiaceae, and Verbenaceae). Research on
primate seed dispersal in the Neotropics is biased toward
large-bodied primates, which may lead to an incomplete
picture of seed dispersal in many Neotropical primate
communities. We plan to investigate the potentially im-
portant ecological role small primates like Saguinus may
play in tropical ecosystems. For more information, con-
tact Brian W. Grafton and E. Natasha Vanderhoff, at
bgrafton@kent.edu and nvander4@ju.edu.


BoOKS

Best Practice Guidelines for the Prevention and M.r.giia.on
of Conflict between Humans and Great Apes, by K. Hock-
ings and T. Humle. 2009. IUCN/SSC Primate Specialist
Group. 40pp. ISBN: 978-2-8317-11331. The IUCN/
SSC Primate Specialist Group is developing a series of
guidelines to address critical issues in great ape conserva-
tion, drawing on the expertise of PSG members to create
a consensus of best practices for field conservationists.
Each publication in the new series will provide up-to-
date guidance for scientists working on a daily basis with
great apes, as well as for the many development organiza-
tions, donors and government agencies that are involved
in great ape conservation. Contents: 1. Summary; 2. In-
troduction, review and use osf these guidelines; 3. Assess-
ment of human-great ape conflict (HGAC): Preparatory


issues; 4. Review of potential HGAC counter measures
and their effectiveness; 5. Planning a HGAC management
strategy; 6. Conclusions. http://www.primate-s; ,.,, I-r
practices.htm

Ameranthropoides loysi Montandon 1929: the History of a
Primatological Fraud, by B. Urbani and A. L. Viloria. 2009.
Libros en red. 296pp. ISBN: 978-1597544450. This his-
tory reviews the information published on the contro-
versy of the discovery of an alleged Neotropical ape that
resulted in one of the most notorious scientific frauds of
the 20th Century. Such finding supposedly occurred either
in 1917 or 1918 while oil prospecting in the forests of the
Tarra River region, located in the southwestern part of
Lake Maracaibo, Zulia state, Venezuela. This case was as
much discussed as it was unresolved. Detailed analysis of
the archival sources suggested that the naming of such a
primate was a fraud orchestrated by the Swiss physician
George Montandon and de Loys himself, resulting in one
of the most notorious scientific frauds of the 20th Century.
This investigation provides previously unpublished infor-
mation about this case -whose development seems to be
resolved in Venezuela, through the account of a third wit-
ness, the Venezuelan physician Enrique Tejera.

Tinbergen's Legacy: Function and Mechanism in Behavioral
Biology, edited by S. Verhulst and J. Bolhuis. 2009. Cam-
bridge University Press. 262pp. ISBN: 978-0521697552.
In this book, an international cast of leading animal bi-
ologists reflect on the enduring significance of Tinbergen's
groundbreaking proposals for modern behavioral biol-
ogy. It includes a reprint .- I.i n, n, original article on
the famous 'four whys' and a contemporary introduction,
after which each of the four questions are discussed in the
light of contemporary evidence. There is also a discussion
of the wider significance of recent trends in evolutionary
psychology and neuroecology to integrate the 'four whys'.
With a foreword by one of Tinbergen's most prominent
pupils, Aubrey Manning, this wide-ranging book demon-
strates that Tinbergen's views on animal behaviour are cru-
cial for modern behavioral biology. Contents: 1. On aims
and methods of ethology N. Tinbergen; 2. Tinbergen's
four questions and contemporary behavioral biology J.
A.Hogan and J. J. Bolhuis; 3. Causation: the study of be-
havioral mechanisms J. A.Hogan; 4. Tinbergen's fourth
question, ontogeny: sexual and individual differentiation
- D. Crews and T. Groothuis; 5. The development of be-
havior: trends since Tinbergen (1963) -J. A. Hogan and J.
J. Bolhuis; 6. The study of function in behavioral ecology
- I. Cuthill; 7. The evolution of behavior and integrating
it towards a complete and correct understanding of be-
havioral biology M. J. Ryan; 8. Do ideas about function
help the study of causation? D. F. Sherry; 9. Function
and mechanism in neuroecology: looking for clues J. J.
Bolhuis.

Linking Conservation and Poverty Reduction: Landscapes,
People and Power, by R. Fisher, S. Jeanrenaud, S. Maginnis,





Neotropical Primates 16(1), June 2009


W. Jackson, E. Barrow, A. Ingles, R. Friend, R. Mehortra,
T. Farvar, M. Laurie and G. Oliviedo. 2008. Earthscan
Publications & IUCN. 144pp. ISBN: 978-1844076369.
This book provides a grand overview and a conceptual
framework for addressing poverty reduction in the context
of conservation and conservation in the context of poverty
reduction, including recent developments in theory, field-
work and new case studies from Francophone Africa and
Latin America. The book begins by looking at the rationale
for addressing the links between conservation and poverty
reduction, arguing that such a focus is both ethically es-
sential and a source of opportunities. This is followed by
a review of experiences in dealing with people and conser-
vation and identifies some key lessons and concepts. The
next section presents key illustrative case studies followed
by a discussion of some of the issues that appear when
implementing combined conservation and poverty reduc-
tion. The emphasis is on the importance of multiple spa-
tial scales and seeking negotiated trade-offs between scales.
Contents: 1. Introduction; 2. Past Experiences; 3. Case
Studies; 4. Scale, Landscapes, Boundaries and Negotiation;
5. Structures, Institutions and Rights; 6. Linking Conser-
vation and Poverty Reduction.


ARTICLES

Aguiar, L. M., Ludwig, G. and Passos, E C. 2009. Group
size and composition of black-and-gold howler monkeys
(Alouatta caraya) on the Upper Parana River, Southern
Brazil. Primates. 50(1). Pgs: 74-77.
Amendola-Pimenta, M., Garcia-Feria, L., Serio-Silva, J. C.
and Rico-Gray, V. 2009. Noninvasive collection of fresh
hairs from free-ranging howler monkeys for DNA extrac-
tion. Am. J. Prim. 71(4). Pgs: 359-363.
Asensio, N., Korstjens, A. H. and Aureli F 2009. Fission-
ing minimizes ranging costs in spider monkeys: a multi-
ple-level approach. Behav. Ecol. & Sociobio. 63(5). Pgs:
649-659.
Bezerra, B. M., Barnett, A. A., Souto, A. and Jones, G.
2009. Predation by the tayra on the common marmo-
set and the pale-throated three-toed sloth. J Ethol. 27(1).
Pgs: 91-96.
Bower, B. 2009. Capuchin monkeys choose the right tool
for the nut.Science news. 175(4). Pgs: 12.
Campo, E A. and Fedigan, L. M. 2009. Behavioral adap-
tations to heat stress and water scarcity in white-faced
capuchins (Cebus capucinus) in Santa Rosa National Park,
Costa Rica. Am. J. Phys. Anthropol. 138(1). Pgs: 101-111.
de laTorre, S. and Snowdon, C. T. 2009. Dialects in pygmy
marmosets? Population variation in call structure. Am. J.
Prim. 71(4). Pgs: 333-342.
Figueiredo, M. S. L. and Grelle, C. E. V. 2009. Predicting
global abundance of a threatened species from its occur-
rence: implications for conservation planning. Diver. &
Distributions. 15(1). Pgs: 117-121.
Gonzalez-Zamora,A., Arroyo-Rodriguez,V., Chaves, 0. M.,
Sinchez-L6pez, S., Stoner, K. E. and Riba-Hernindez, P.


2009. Diet of spider monkeys (Ateles .. ..r .i in Meso-
america: current knowledge and future directions. Am. J.
Prim. 71(1). Pgs: 8-20.
Kay, R. E, Fleagle, J. G., Mitchell, T. R. T., Colbert, M.,
Bown, T. and Powers, D. W. 2009. The anatomy of Doli-
chocebus gaimanensis, a stem platyrrhine monkey from
Argentina. J Hum. Evol. 54(3). Pgs: 323-382.
Liu, Q., Simpson, K. Izar, P., Ottoni, E., Visalberghi, E.
and Fragaszy, D. 2009. Kinematics and energetic of
nut-cracking in wild capuchin monkeys (Cebus libidino-
sus) in Piaui, Brazil. Am. J. Phys. Anthropol. 138(2). Pgs:
210-220.
Mannu, M. and Ottoni, E. B. 2009. The enhanced tool-
kit of two groups of wild bearded capuchin monkeys in
the Caatinga: tool making, associative use, and secondary
tools. Am. J. Prim. 71(3). Pgs: 242-251.
Marcili, A., Valente, V. C., Valente, S. A., Junqueira,
A. C. V., Maia da Silva, E, Pinto A. Y. N., Maiff, R. D.,
Campaner, M., Coura, J. R., Camargo, E. P., Miles,
M. A. and Teixeira, M. M. G. 2009. Trypanosoma cruzi
in Brazilian Amazonia: lineages TCI and TCIIa in wild
primates, Rhodnius spp. And in humans with Chagas
disease associated with oral transmission. Int. J. Parasitol-
ogy. 39(5). Pgs: 615-623.
Menescal, L. A., Goncalves, E. C., Silva, A., Ferrari, S. F
and Schneider, M. P. C. 2009. Genetic diversity of red-
bellied titis (Callicebus moloch) from Eastern Amazonia
based on microsatellite markers. Biochem. Gen. 47(3-4).
Pgs: 235-240.
Milton, K., Loizer, J. D. and Lacey, E. A. 2009. Genetic
structure of an isolated population of mantled howler
monkeys (Alouatta palliata) on Barro Colorado Island,
Panama. Cons. Gen. 10(2). Pgs: 347-358.
Peker, S., Kowalewski, M. M., Pave, R. E. and Zunino,
G. E. 2009. Births in wild black and gold howler mon-
keys (Alouatta caraya) in northern Argentina. Am. J. Prim.
71(3). Pgs: 261-265.
Perini, E. S., Pessoa, V. F and Pessoa, D. M. A. 2009. De-
tection of fruit by the Cerrado's marmoset (C
penicillata): modeling color signals for different back-
ground scenarios and ambient light intensities. J Exp.
Zool. On line 1-14.
Pesendorfer, M. B., Gunhold, T., Schiel, N., Souto, A.,
Huber, L. and Range, E 2009. The maintenance of tra-
ditions in marmosets: individual habit, not social confor-
mity? A field experiment. Plos one. 4(2). Pgs: e4472(online
1-9).
Porter, L. M., Garber, P. A. and Nacimento, E. 2009. Exu-
dates as a fallback food for Callimico goeldii. Am. J. Prim.
71(2). Pgs: 120-129.
Silva, S. S. B. and Ferrari, S. E 2009. Behavior patterns of
southern bearded sakis (Chiropotes satanas) in the frag-
mented landscape of eastern Brazilian Amazonia. Am. J.
Prim. 71(1). Pgs: 1-7.
Slater, K. Y., Schaffner, C. M. and Aureli, E 2009. Sex dif-
ferences in the social behavior of wild spider monkeys
(Ateles ..o.., yucatanensis). Am. J. Prim. 71(1). Pgs:
21-29.





Neotropical Primates 16(1), June 2009


Van Belle, S., Estrada, A., Ziegler, T. E. and Strier, K. B.
2009. Sexual behavior across ovarian cycles in wild black
howler monkeys (Alouattapigra): male mate guarding and
female mate choice. Am. J. Prim. 71(2). Pgs: 153-164.
Visalberghi, E., Spagnoletti, N., Ramos da Silva, E. D.,
Andrade, F. R. D., Ottoni, E., Izar, P. and Fragaszy, D.
2009. Distribution of potential suitable hammers and
transport of hammer tools and nuts by wild capuchin
monkeys. Primates. 50(2). Pgs: 95-104.
Visalberghi, E., Addessi, E., Truppa, V., Spagnoletti, N.,
Ottoni,E., Izar, P. and Fragaszy, D. 2009. Selection of
effective stone tools by wild bearded capuchin monkeys.
Current Biol. 19(3). Pgs: 213-217.


ABSTRACTS

Selected abstracts from the 31" Meeting of the Ameri-
can Society of Primatologists. West Palm Beach, Flor-
ida, June 18-21, 2008 http://www.asp.org/asp2008/
showConfSchedule.cfm

Amendola-Pimenta, M., Rico-Gray, V. and Pifiero-
Dalmau, D. Habitat disturbance and genetic variability
of populations of black howler monkey (Alouattapigra)
in Campeche, Mexico: Implications for conservation.
Bonilla-Sanchez, Y. M., Serio-Silva, J. C., Pozo-Montuy,
G. and Bynum, N. Demography of Alouatta pigra in
threated habitat in south-eastern Mexico.
Bustos, C. A., Corkum, L. D., Slater, K. Y. and Men-
nill, D. J. Acoustic characteristics of the vocalizations
of mantled howler monkeys (Alouatta palliata) in the
fragmented low-land forests of Honduras.
Dampier, S. M. To see or not to see: factors affecting cap-
tive capuchin visibility (Cebus apella robustus).
Depeine, C. D., Rotundo, M., Juarez, C. P. and Fernan-
dez-Duque, E. Hoot calling in owl monkeys (Aotus
azarai) of Argentina: Sex differences and function.
Field, M. Y. Nursing behavior in a group of human-
commensal white-fronted capuchins (Cebus, dlb. on,) in
Misahualli, Ecuador.
Gibson, S. V., Tustin, G. W., Williams, L. E., Schuler,
A. M., Brady, A. G. and Abee, C. R. Reproduction in
an owl monkey breeding colony (Aotus sp.).
Hooff, S. B. and Wolovich, C. K. Captive owl monkeys
respond to novel flavors with neophobia, discrimina-
tion, and food sharing.
Hores, R. M., Wolovich, C. K. and Evans S. Is it worth
the risk? Novel food presentation affects behavior in
captive owl monkeys (Aotus spp.).
lonica, C. S., Robbins, K. L., Novak, M. F S. X. and
Suomi, S. J. Multimodal data input using touchscreen
technology, voice recording and speech recognition in
adverse field conditions.
Jarcho, M. R., Mason, W. A., Mendoza, S. P. and Bales,
K. L. Intranasal vasopressin administration effects on
pair-bonding and gene expression in monogamous titi
monkeys (Callicebus cupreus).


Jasso, C. and Estrada, A. Tropical rain forest fragmentation
and social interactions in young howler monkeys (Alouat-
ta palliata).
Juarez, C. P., Berg, W. J. and Fernandez-Duque, E. An eval-
uation of the potential long-term effects of radio-collars
on the reproduction and demography of owl monkeys
(Aotus azarai) in Formosa, Argentina.
Kitzmann, C. D., Main, D. E., Mendoza, S. P. and Bales, K.
L. Vocal behavior of adult titi monkeys (Callicebus cupreus)
in a separation paradigm.
Matthews, S. A. and French, J. A. Parental care influences
on pubertal timing in female wied's black tufted-ear mar-
moset (C .- kuhlii).
Parr, N., Campos, F., Childers, A., Fedigan, L. and Jack, K.
Dry season ranging behavior and intergroup relations in
white-faced capuchins (Cebus capucinus) at Santa Rosa na-
tional park, Costa Rica.
Paukner, A., Huntsberry, M. E., Ferrari, P. E and Suomi,
S. J. Imitation recognition in capuchin monkeys.
Perea-Rodriguez, J. P, Milano, A. M., Fernandez-Duque,
E. and Osherov, B. E. Gastrointestinal parasites of owl
monkeys (Aotus azarai) living in edge and non-edge ter-
ritories in a gallery forest in northern Argentina.
Phillips, K. A. and Liu, S. T. Sylvian fissure asymmetries in
capuchin monkeys (Cebus apella).
Pokorny, J. J. and de Waal, E B. How capuchin monkeys
(Cebus apella) categorize visual images of themselves: in-
group vs. out-group.
Pozo-Montuy, G., Serio-Silva, J. C. and Bonilla-Sanchez,
Y. M. The effects of anthropogenic pressure on the behav-
iour and demography of the black howler monkey (Alouat-
tapigra) in south-eastern Mexico.
Ross, C. N., Tardif, S., Davis, K., Dobek, G. and Brasky, K.
Relations among body composition, activity, hematology,
and age in male common marmosets: Toward a model of
frailty.
Rutherford, J. N. Placental insulin-like growth factor ii (igf-
ii) and its relation to litter size and placental weight in
captive common marmosets (C .-('. jacchus).
Saltzman, W., Boettcher, C. A., Crosno, K. A. and Abbott,
D. H. Effects of lactation on pituitary-adrenal responses
to stress in laboratory-housed common marmosets (Cal-
lithrix jacchus).
Savage, A., Thomas, L., Leighty, K., Soto, L., Causado, J.
and Medina, F. The development of a census technique
for cotton-top tamarins (Saguinus oedipus) in Colombia.
Smith, A. S. and French, J. A. Maternal androgen levels
during pregnancy are associated with early-life growth and
aggressive behavior of offspring in geoffroy's marmosets
(C- .. .4 .. .., ,
Smucny, D. A. When primatologists go public: applying
"best practices" for informal science education to teaching
the general public about primates.
Stone, B. W., Menzel, C. R., Evans, T. A., Benoit, J. and
Fragaszy D. M. Capuchin monkeys (Cebus apella) learn to
point with a laser.
Trejo-Macias, G., Estrada, A. and Mosqueda-Cabrera,
M. A. Preliminary study of gastrointestinal helminths in





Neotropical Primates 16(1), June 2009


howler monkeys (Alouattapalliata) living in a cacao plan-
tation in southern Mexico.
Van Belle, S., Estrada, A., Ziegler, T. E. and Strier, K. B.
Behavioral and endocrine characteristics of the ovarian
cycle in black howler monkeys (Alouattapigra).
Wolovich, C. K., Hooff, S. and Evans, S. Owl monkeys
don't just give a hoot: Preferred food elicits trills.







2009

Meeting cancelled: Neotropical Primate Husbandry, Re-
search and Conservation Conference. October 13-15. The
Neotropical Primate Husbandry, research and conservation
conference, that was going to be held at the Brookfield Zoo
was canceled.

IV Congress Mexicano de Primatologia. Junio 24-26,
Villahermosa, Tabasco. La Asociaci6n Mexicana de Prima-
tologia A.C. y la Universidad Juirez Aut6noma de Tabasco,
convocan. Para mayor informaci6n visit: http://www.
tierradeideas.com/amp/

The 3rd Congress of the European Federation for Prima-
tology. August 12-15, Irchel campus of the University of
Ziirich, Switzerland. The EFP is a federation of all national
primatological societies and groups in Europe. The bien-
nial meetings strive to bring together primatologists and
biological anthropologists from all over Europe to encour-
age interdisciplinary and international exchanges. The
registration and abstract submission deadline is April 15',
2009. For more information visit the web site: www.aim.
uzh.ch/EFP.html

The 32nd Meeting of the American Society of Primatolo-
gists. September 18-21, Bahia Resort Hotel, San Diego,
California, USA. For further information check the web
site: www.asp.org/asp2009/index.htm

The 7th International Conference on Behavior, Physiology
and Genetics of Wildlife. September 21-24, Conference
Centre BfR-Bundesinsitut fur Risikobewertung, Berlin,
Germany. The Leibniz Institute for Zoo and Wildlife Re-
search and the European Association of Zoos and Aquaria
invites. The main topics are: behavioral ecology, stress
and disturbance, reproduction biology, conservation genet-
ics, and conservation biology. The conference language is
English. For more information and registration go to www.
izw-berlin.de/de/flink/7thlZW-Conference.html


VI Congress Brasileiro de Unidades de Conservaoio.
Septembro 20-24, Expo Unimed Curitiba, Curitiba-PR,
Brasil. A fundacao 0 Boticario de Protegao a Natureza
convida. Para mais informa6oes visite:http://www.itarget.
com.br/newclients/fundacaoboticario.org.br /cbuc2009//

II Iberian Primatological Conference. September 30-
October 3, Residencia "la Cristalera" in Miraflores de la
Sierra, Madrid, Espafia. During the second edition of the
Iberian Primatological Conference, the Asociaci6n Prima-
tol6gica Espanola (APE) is responsible for organizing and
hosting the congress in straight co-operation with the As-
sociagao Portuguesa de Primatologia (APP). Deadlines for
abstract submission June 30, 2009. For more information
go to http://www.uam.es/otros/ape/congresos/CIP2.html

2010

The 23rd Congress of the International Primatological
Society. September 12-18, Kyoto University, Japan. The
theme of the conference will be 'Quest for Coexistence
with Nonhuman Primates.' In line with IPS policy, the
committee welcomes suggestions for symposia on any of
the disciplines of primatology. The Symposium submission
deadline is October 15th, 2009. The presentation submis-
sion deadline is January 15', 2010. For more information
go to: www.ips2010.jp/.






CONSERVATION INTERNATIONAL
Marmosets
and
Tamarins
Pocket Identflication Guide











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Jo s de S. e Sllv Jr. M. CefIf M. KLru.I
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Marmosets and Tamarins Pocket Identification Guide

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Marmosets and Tamarins Pocket Identification Guide by
Anthony B. Rylands, Russell A. Mittermeier, Adelmar F.
Coimbra-Filho, Eckhard W. Heymann, Stella de la Torre,
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the continental United States)


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Scope
The journal/newsletter 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, primatologi-
cal society information and suchlike.

Submissions
Please send all English and Spanish contributions to: Erwin Palacios,
Conservaci6n Internacional-Colombia, Carrera 13 # 71-41 Bogota
D.C., Colombia, Tel: (571) 345-2852/54, Fax: (571) 345-2852/54,
e-mail: , and all Portuguese contribu-
tions to: Jdlio Cesar Bicca-Marques, Departamento de Biodiversidade
e Ecologia, Pontificia Universidade Cat6lica do Rio Grande do Sul,
Av. Ipiranga, 6681 Pridio 12A, PortoAlegre, RS 90619-900, Brasil,
Tel: (55) (51) 3320-3545 ext. 4742, Fax: (55) (51) 3320-3612,
e-mail: .

Contributions
Manuscripts may be in English, Spanish or Portuguese, and should
be double-spaced and accompanied by the text on CD for PC com-
patible text-editors (MS-Word, WordPerfect, Excel, and Access),
and/or e-mailed to (English, Spanish)
or (Portuguese). Hard copies should be supplied
for all figures (illustrations and maps) and tables. The full name and
address for each author should be included. Please avoid abbreviations
and acronyms without the name in full. Authors whose first language
is not English should please have their English manuscripts carefully
reviewed by a native English speaker.

Articles. Each issue of Neotropical Primates will include up to three
full articles, limited to the following topics: Taxonomy, Systemat-
ics, Genetics (when relevant for systematics and conservation),
Biogeography, Ecology and Conservation. Text for full articles
should be typewritten, double-spaced with no less than 12 cpi font
(preferably Times New Roman) and 3-cm margins throughout,
and should not exceed 25 pages in length (including references).
Please include an abstract in the same language as the rest of the
text (English, Spanish or Portuguese) and (optional) one in Portu-
guese or Spanish (if the text is written in English) or English (if the
text is written in Spanish or Portuguese). Tables and illustrations
should be limited to six, except in cases where they are fundamen-
tal for the text (as in species descriptions, for example). Full articles
will be sent out for peer-review. For articles that include protein
or nucleic acid sequences, authors must deposit data in a publicly
available database such as GenBank/EMBL/DNA Data Bank
of Japan, Brookhaven, or Swiss-Prot, and provide an accession
number for inclusion in the published paper.
Short articles. These manuscripts are usually reviewed only
by the editors. A broader range of topics is encouraged, includ-
ing such as behavioral research, in the interests of informing on
general research activities that contribute to our understanding
of platyrrhines. We encourage reports on projects and conserva-
tion and research programs (who, what, where, when, why, etc.)
and most particularly information on geographical distributions,
locality records, and protected areas and the primates that occur in
them. Text should be typewritten, double-spaced with no less than
12 cpi (preferably Times New Roman) font and 3-cm margins
throughout, and should not exceed 12 pages in length (including
references).


Figures and maps. Articles may include small black-and-
white photographs, high-quality figures, and high-quality maps.
(Resolution: 300 dpi. Column widths: one-column = 8-cm wide;
two-columns = 17-cm wide). Please keep these to a minimum. We
stress the importance of providing maps that are publishable.
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, field sites,
courses, Thesis or Dissertations recently defended, recent publica-
tions, awards, events, activities of Primate Societies, etc.
References. Examples of house style may be found throughout
this journal. In-text citations should be first ordered chronologi-
cally and then in alphabetical order. For example, "...(Fritz, 1970;
Albert, 1980, 2004; Oates, 1981; Roberts, 2000; Smith, 2000;
Albert etal., 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"). This 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. The black-tailed mar-
moset (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.
Thesis/Dissertation
Wallace, R. B. 1998. The behavioral 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. 0. 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, Scientific, 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 Span-
ish respectively.
"Doctoral thesis" changes to "Tese de Doutoramento" and "Tesis de
Doctorado" for articles in Portuguese and Spanish respectively.
"MSc Thesis" changes to "Dissertacao de Mestrado" and "Tesis de
Maestria" for articles in Portuguese and Spanish respectively.
"Unpublished report" changes to "Relat6rio T6cnico" and "Reporte
no publicado" for articles in Portuguese and Spanish respectively.

































































































































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