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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: December 2007
Frequency: quarterly
regular
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Subject: Primates -- Periodicals -- Latin America   ( lcsh )
Primates -- Periodicals   ( lcsh )
Wildlife conservation -- Periodicals   ( lcsh )
Genre: review   ( marcgt )
periodical   ( marcgt )
Spatial Coverage: Brazil
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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).
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Volume ID: VID00054
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 103
        Page 104
        Page 105
        Page 106
        Page 107
        Page 108
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    Back Matter
        Back Matter 1
        Back Matter 2
    Back Cover
        Back Cover
Full Text

ISSN 1413-4703


NEOTROPICAL


PRIMATES



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



Volume 14


Number
December


3
2007


Editors
Erwin Palacios
Liliana Cort6s-Ortiz
JOlio C6sar Bicca-Marques
Eckhard Heymann
Jessica Lynch Alfaro
Liza Veiga
News and Book Reviews
Brenda Sol6rzano
Ernesto Rodriguez-Luna
PSG Chairman
Russell A. Mittermeier
PSG Deputy Chairman
Anthony B. Rylands


SPECIES SURVIVAL
COMMISSION


CONSERVAC16~N
INTERNATIONAL
___COLOMBIA









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
Liliana Cort6s Ortiz, Museum of Zoology, University of Michigan, Ann Arbor, MI, USA
Jflio C6sar Bicca-Marques, Pontificia Universidad Cat6lica do Rio Grande do Sul, Porto Alegre, Brasil
Eckhard Heymann, Deutsches Primatenzentrum, Gattingen, Germany
Jessica Lynch Alfaro, Washington State University, Pullman, WA, USA
LizaVeiga, Museu Paraense Emflio Goeldi, Belem, Brazil

News and Books Reviews
Brenda Sol6rzano, Instituto de Neuroetologfa, UniversidadVeracruzana, Xalapa, Mexico
Ernesto Rodrfguez-Luna, Instituto de Neuroetologfa, Universidad Veracruzana, Xalapa, M6xico

Founding Editors
Anthony B. Rylands, Center for Applied Biodiversity Science Conservation International, Arlington VA, USA
Ernesto Rodrfguez-Luna, Instituto de Neuroetologfa, Universidad Veracruzana, Xalapa, Mexico
Editorial Board
Hannah M. Buchanan-Smith, University of Stirling, Stirling, Scotland, UK
Adelmar E Coimbra-Filho, Academia Brasileira de Ciencias, Rio de Janeiro, Brazil
Carolyn M. Crockett, Regional Primate Research Center, University of Washington, Seattle, WA, USA
Stephen F Ferrari, Universidade Federal do ParA, Belem, Brazil
Russell A. Mittermeier, Conservation International, Arlington, VA, USA
Marta D. Mudry, Universidad de Buenos Aires, Argentina
Horicio Schneider, Universidade Federal do Padr, Belem, Brazil
Karen B. Strier, University of Wisconsin, Madison, WI, USA
Maria Emilia Yamamoto, Universidade Federal do Rio Grande do None, 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

PSG General Coordinator/Website Manager, John M. Aguiar

Layout: Kim Meek, Center for Applied Biodiversity Science, Conservation International, Arlington, VA, USA
Editorial Assistance: John M. Aguiar, Center for Applied Biodiversity Science, Conservation International, Arlington, VA, USA

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

Front cover: A bald uakari, Cacajao calvus calvus, from the Brazilian Amazon. Photo by Russell A. Mittermeier.

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.
fM1mMMsItl -M 1





Neotropical Primates 14(3), December 2007


FLORA BACTERIANA DE LA CAVIDAD ORAL DEL MONO TITI (SAIMIRI OERSTEDII) Y SU
PERFIL DE SENSIBILIDAD A ANTIBIOTICS

Carlos E. Rodriguez-Rodriguez1, Evelyn Rodriguez-Cavallini1, Maria del Mar Gamboa-Coronado1,
Silvia Jimenez-Cuadra1, Ronald Sainchez-Porras2 y Gustavo A. Gutierrez-Espeleta3

1Laboratorio de Investigacidn en Bacteriologia Anaerobia y Centro de Investigacidn en Enfermedades Tropicales, Facultad de
. I cL ob.olo,'; i. Universidad de Costa Rica.
2Programa de Investigaciones del Bosque Premontano, Sede de Occidente, Universidad de Costa Rica.
3Escuela de Biologia, Universidad de Costa Rica.


Resumen

Se estudi6 la flora bacteriana y su patr6n de sensibilidad antimicrobiana en la cavidad oral de 33 monos Saimiri oerstedii:
31 silvestres y 2 en cautiverio. Con torunda est&ril se rasparon los dientes y la cavidad bucal de cada mono y se resuspendi6
en 2 mL de soluci6n salina esteril (0.85%); se prepararon tubos de transport para cultivos aerobics y anaerobios y una vez
en el laboratorio, se inocularon places de agar sangre que se incubaron en aerobiosis y anaerobiosis. Los aislamientos se iden-
tificaron con sistemas miniaturizados API (20NE, Staph y 20A); las determinaciones de la sensibilidad a los antibi6ticos se
realizaron con galerias ATB (G5, Staph y ANA). Se aislaron 137 cepas bacterianas: 106 aerobias (77.4%) y 31 anaerobias
(22.6%). El predominio fue de bacilos Gram negativos aerobics (100 cepas), siendo Enterobacter el gdnero mais frecuente
(42%), seguido de Burkholderia y Aeromonas (27% c/u); los anaerobios mas comunes fueron Clostridium (36%) y Fuso-
bacterium (12%). Estos resultados revelan semejanzas y diferencias con respect a la flora oral humana y la de otros monos
costarricenses; la alta frecuencia de algunos gdneros sugiere que son parte de la flora oral de monos y no contaminaci6n
secundaria de bacteria del suelo. El 90% de los bacilos Gram negativos aerobics fue resistente a cefalotina y el 89% a cefoxi-
tina; altas tasas de resistencia se presentaron tambidn ante otras drogas; solamente ceftriaxone y pefloxacina fueron efectivos
contra todas las cepas analizadas; s6lo dos cepas fueron sensibles a todos los antibi6ticos evaluados. El mayor porcentaje de
resistencia en anaerobios ocurri6 ante el metronidazole (26 a 35%) seguido por cefotetin (26%) y clindamicina (23%); el
39% de los aislamientos fue sensible a todos los antibi6ticos evaluados. La resistencia multiple fue menor en los anaerobios
(26%) que en los aerobics (77%). Este studio contribute al conocimiento y a la preservaci6n del mono titi, especie ame-
nazada, y muestra que pocas barreras son capaces de contener los genes de resistencia y sus hospederos bacterianos, aun en
animals silvestres.

Palabras Clave: Saimiri oerstedii, Costa Rica, flora bacteriana oral, resistencia antimicrobiana


Abstract

The bacterial microflora present in the oral cavity of 33 squirrel monkeys (Saimiri oerstedii, 31 wild and 2 captive) and its an-
timicrobial sensibility was studied. A sterile swab was used to scratch the teeth and oral cavity of every monkey; each sample
was resuspended in 2 mL sterile saline solution (0.85%). Transport tubes for aerobic and anaerobic cultures inoculated with
these samples were sent to the laboratory. Each sample was inoculated in blood agar plates that were incubated in aerobic
and anaerobic conditions. Isolates obtained were identified with API- galleries (20NE, Staph and 20A) and the sensibility
determinations were done using ATB galleries (-G5, -Staph and -ANA). A total of 137 strains were isolated: 106 aerobes
(77.4%) and 31 anaerobes (22.6%). Gram negative bacilli were predominant, with Enterobacter the most frequent genus
(42%), followed by Burkholderia and Aeromonas (27% each). The most frequent anaerobes were Clostridium (36%) and
Fusobacterium (12%). These results show similarities and differences with the bacteria of the oral cavity of humans and of
other Costa Rican monkeys. The high frequency of some genera suggests that they are part of the oral flora of the monkeys
and not contaminants from the soil. Ninety percent of the Gram negative aerobe bacilli were resistant to cephalotin and 89%
to cefoxitine. High resistance rates were obtained with other agents; only two strains were sensitive to every antibiotic tested.
In anaerobes the higher antibiotic resistance was observed with metronidazole (26-35%), cefotetan (20%) and clindamicyn
(23%), 39% of the strains were sensitive to every antibiotic tested; multiple resistance was lower in the anaerobes (26%) than
in the aerobes (77%). This study contributes to the knowledge and preservation of the squirrel monkey, a threatened species,
and demonstrates that there are few barriers to the spread of resistant genes in bacteria, even in wild animals.

Key Words: Saimiri oerstedii, Costa Rica, antimicrobial resistance, oral bacterial flora





Neotropical Primates 14(3), December 2007


Introducci6n

El mono titi (Saimiri oerstedii) habitat en los bosques de
Costa Rica y Panami (Wong, 1990), y es considerada
una especie amenazada (IUCN, 2007). Otras species del
gdnero se encuentran en America del Sur, en un irea limi-
tada por Colombia al oeste y la cuenca del Amazonas y las
Guyanas al este (Wong, 1990). En Costa Rica existen dos
subespecies de este gdnero: S. oerstedii oerstedii y S. oerste-
dii citrinellus; ambas se consideran en peligro de extinci6n,
principalmente por la p&rdida de su habitat, el desarrollo
de infraestructura hotelera y por su capture y venta como
mascotas (Carrillo et al., 2000). S. oerstedii es el mono de
menor tamafio de Costa Rica y se encuentra en bosques
primaries, secundarios y en ireas cultivadas; los Parques
Nacionales Manuel Antonio y Corcovado son los reservo-
rios mais importantes. Es de conduct arboricola y diurna
y se alimenta durante las primeras horas de la mafiana,
principalmente de insects (75-80% de la dieta) y frutas
(Campbell et al., 2003).

La cavidad oral de los animals, al igual que la de los hu-
manos, es uno de los habitats microbiol6gicos mais com-
plejos y heterog6neos. La flora bacteriana incluye tanto
anaerobios estrictos como Bacteroides sp., Fusobacterium
sp., Actinomyces sp. y aerobics facultativos como Coryne-
bacterium sp., Haemophilus sp., Moraxella sp. y Neisseria
sp. (Sorum y Sunde, 2001). Dicha flora indigena contiene
genes de resistencia a antibi6ticos, incluso en individuos sin
historic de exposici6n a antimicrobianos preparados comer-
cialmente (Sorum y Sunde, 2001). Son necesarios nuevos
studios en la flora normal de animals para determinar si
su resistencia esti directamente relacionada con el drami-
tico incremento en la resistencia de pat6genos (Sorum y
Sunde, 2001). Las escasas investigaciones relacionadas con
la flora normal de monos se han llevado a cabo principal-
mente en el mono rhesus (Macaca mulatta) (Bowers et al.,
2002), mientras que en Costa Rica se efectu6 un studio
relacionado con la flora oral de los monos congo (Alouatta
palliata) y colorado (Ateles. .r ..'i I (Gamboa-Coronado et
al., 2004). En el present trabajo se describe la flora bacte-
riana de la cavidad oral de S. oerstedii asi como su patron de
sensibilidad, para compararlos con los de otros monos de
Costa Rica y establecer la possible influencia del hombre en
la adquisici6n de resistencia antimicrobiana.

MWtodos

Se estudiaron 33 muestras de la cavidad oral de monos de la
especie Saimiri oestedii; 31 monos se capturaron en estado
silvestre de cuatro zonas de Costa Rica: Parque Nacional
Manuel Antonio (09023'N, 8407'0), Parque Nacional
Corcovado (0828'N, 8335'0), Isla Damas (0930'N,
8415'0) y Golfito (08036'N, 8304'0), utilizando una
cerbatana para el lanzamiento de dardos (Pneudart, Inc.)
que contenian cada uno 0.3-0.4 mL de Zolazepam, co-
nocido comercialmente como Zoletil. Las muestras de los
dos monos restantes fueron obtenidas de individuos que


permanecian en cautiverio desde hace dos afios en un zoo-
16gico. Con una torunda est&ril se rasparon los dientes y
la cavidad bucal de cada uno de los monos previamente
sedados, y se resuspendi6 la muestra en un tubo con 2 mL
de soluci6n salina est&ril (SSE). Asepticamente y con jerin-
ga est&ril se inocul6 0.5 mL de la suspension en un tubo
con medio came cocida (CC) prerreducido. Durante el
transport hasta el laboratorio los tubos con la suspension
en SSE se mantuvieron en frio, mientras que los de CC
se mantuvieron a temperature ambiente. A cada uno de
los tubos con SSE se les agreg6 2 mL de caldo tripticasa
soya (CTS) y se incubaron a 35C por 24 horas; los tubos
con CC prerreducidos se incubaron a 35C por 48 horas.
A partir de cada tubo con CTS se ray6 una placa de agar
sangre (AS) y se incub6 a 35C por 24 horas para el aisla-
miento de bacteria aerobias. A partir de cada tubo con CC
prerreducido se ray6 una placa de AS y se incub6 a 35C
por 48 horas en jarra de anaerobiosis para el aislamiento de
bacteria anaerobias. Se seleccionaron los diferentes mor-
fotipos coloniales de cada placa, se les realize tinci6n de
Gram y se subcultivaron en places de AS para obtener cul-
tivos puros. Se determine la tolerancia al oxigeno de cada
cepa aislada a trav5s de la inoculaci6n de dos places de AS,
una incubada en atm6sfera incrementada de CO2 y otra en
jarra de anaerobiosis (35C por 48 horas). Se seleccionaron
como bacteria anaerobias aquellas cuyo crecimiento fue
exclusive o mejor en condiciones de anaerobiosis.

A las cepas bacterianas aerobias se les realizaron pruebas de
Gram, oxidasa y catalasa, con el objetivo de agrupar las bac-
terias como enterobacterias, bacilos Gram negativos no en-
terobacterias, estafilococos y estreptococos. Con base en los
resultados se seleccion6 la galeria miniaturizada de pruebas
bioquimicas apropiada para la identificaci6n; se emplearon
los sistemas API 2 "E API 20NE, y API Staph, mientras
que para las bacteria anaerobias se utilizaron las galerias API
2, Las identificaciones se realizaron con el program
API-Plus. Para determinar la sensibilidad a los antibi6ticos
se emplearon galerias comerciales ATB de acuerdo con el
tipo de bacteria aerobia (ATB-G5 y ATB-Staph); en el caso
de las bacteria anaerobias se utiliz6 el sistema ATB-ANA.
Todas las galerias se incubaron y leyeron de acuerdo con las
recomendaciones de la casa fabricante (bioMrieux).

Resultados

A partir de 33 muestras de la cavidad oral de los monos titi
se aislaron 137 cepas; 106 de bacteria aerobias (77.4%) y
31 de anaerobias (22.6%), lo que equivale a un promedio de
3.2 aerobics y 0.9 anaerobios por muestra. En las bacteria
aerobias predominaron los bacilos Gram negativos (100 de
106 cepas aerobias), donde el gdnero mris frecuente fue En-
terobacter (20 cepas), que se aisl6 del 42% de las muestras e
incluy6 las species E. aerogenes, E. cloacae y E. sakazakii. En
frecuencia le siguieron los gdneros Burkholderia (19 cepas)
y Aeromonas (10 cepas), los cuales se aislaron del 27% de las
muestras. Se identificaron cepas de otros 20 gdneros de ba-
cilos Gram negativos (Tabla 1). Las seis cepas de bacteria





Neotropical Primates 14(3), December 2007


aerobias Gram positivas fueron de los gdneros Staphylococ-
cus (tres cepas: S. sciuri, S. xylosus y S. auricularis) y Bacillus
sp. (tres cepas). En las 31 bacteria anaerobias (Tabla 2)
se identificaron 17 bacilos Gram positivos (generos Clos-
tridium y Propionibacterium), ocho bacilos Gram negativos
(generos Fusobacterium, Bacteroides y Prevotella), cuatro
cocos Gram positivos (generos Gemella y Peptostreptococcus)
y dos cocos Gram negativos (genero Veillonella). El gdnero


Tabla 1. Bacilos Gram negativos aerobics aislados de la cavidad
oral de 33 monos titi (Saimiri oerstedii) de Costa Rica.

Total de cepas Frecuencia de
Genero e cepas aislamiento(%)
n= 100
n=33
Enterobacter 20 42
Burkholderia 19 27
Aeromonas 10 27
Serratia 8 18
Klebsiella 6 15
Citrobacter 6 12
Pseudomonas 4 12
Acinetobacter 3 9
Chryseomonas 3 9
Vibrio 3 9
Brevundimonas 2 6
Morganella 2 6
Pantoea 2 6
Ralstonia 2 6
Flavimonas 2 3
Agrobacter 1 3
A .", .". .*. 1 3
Chromobacterium 1 3
Kluyvera 1 3
Leclercia 1 3
Ochrobacter 1 3
Pasteurella 1 3
Stenotrophomonas 1 3



Tabla 2. Bacterias anaerobias aisladas de la cavidad oral de
33 monos titi (Saimiri oerstedii) de Costa Rica.
Frecuencia de
Genero Total de cepas aislamiento (%)
n=31
n=33
Clostridium 16 36
Fusobacterium 4 12
Bacteroides 2 6
Gemella 2 6
Peptostreptococcus 2 6
Prevotella 2 6
Veillonella 2 6
Propionibacterium 1 3


anaerobio mris cominmente aislado fue Clostridium (16
cepas), a partir del 36% de las muestras, con representantes
de las species C bifermentans, C clostridioforme, C per-
fringens, C sporogenes y C tyrobutyricum.

En las pruebas de sensibilidad a los antibi6ticos (Fig. 1), el
90% de los bacilos Gram negativos fue resistente a la cefa-
lotina y el 89% a la cefoxitina, cefalosporinas de primera y
segunda generaci6n respectivamente. Otras cefalosporinas
presentaron menores porcentajes de resistencia microbia-
na: cefuroxima (69%, 2 generaci6n), ceftazidima 1 mg.L-1
(61%, 3 generaci6n), cefepima (10%, 4 generaci6n) y ce-
fotaxima, ceftazidima 8-16 mg.L-1 y ceftriaxone, todas de
tercera generaci6n, con porcentajes inferiores al 10%. Altas
tasas de resistencia se presentaron tambidn ante amoxicili-
na, tobramicina y amoxicilina + icido clavulinico (Fig. 1).
Ocho de los antimicrobianos demostraron porcentajes de
resistencia de 10-40%, mientras que nueve estuvieron por
debajo del 10%, dentro de los cuales solamente ceftriaxone
y pefloxacina fueron efectivos contra todas las cepas anali-
zadas. Por su parte, las tres cepas de Staphylococcus fueron
resistentes a penicilina, cefalotina, ampicilina + sulbactam,
eritromicina, clindamicina, nitrofurantoina, rifampicina,
vancomicina y teicoplanina.

En las cepas anaerobias tambidn se present resistencia a
various antibi6ticos (Fig. 2); el mayor porcentaje de resis-
tencia ocurri6 ante el metronidazole, 26 a 35% segin su
concentraci6n, seguido por cefotetin (26%), clindamicina
(23%) y penicilina (19%). Se present un bajo porcentaje de
resistencia ante antibi6ticos como amoxicilina, cefoxitina,
ticarcilina y amoxicilina + icido clavulinico (4/8 mg.L-1).
De las 16 concentraciones de antibi6ticos evaluadas, seis
(37.5%) fueron efectivas contra todas las cepas identifica-
das: amoxicilina + icido clavulinico (16/2 mg.L-1), cloran-
fenicol, imipenem, piperacilina, piperacilina + tazobactam
y ticarcilina + icido clavulinico.

Se presentaron casos de cepas multirresistentes tanto en
bacteria aerobias como anaerobias. De los bacilos Gram
negativos aerobics, el 3% fue resistente a 16-19 antibi6-
ticos, el 3% a 13-15, el 13% a 10-12, el 21% a 7-9, el
37% a 4-6, el 21% a 1-3, y s6lo dos cepas fueron sensibles
a todos los antibi6ticos evaluados. La multirresistencia del
gdnero Staphylococcus fue alta, ya que las tres cepas fueron
resistentes a entire 10 y 12 de los 15 antibi6ticos evalua-
dos; la pefloxacina, ciprofloxacina y tetraciclina fueron los
inicos antibi6ticos efectivos contra todas las cepas. En el
caso de las bacteria anaerobias, la resistencia multiple fue
menor pues el 35% fue resistente s6lo a uno 6 dos antimi-
crobianos, el 10% present resistencia a 3-4 y el 16% a
5-7 antibi6ticos, mientras que el 39% fue sensible a todos
los antibi6ticos evaluados.

Discusi6n

Actualmente es escaso el conocimiento disponible sobre
la flora bacteriana oral de monos y en particular de la




Neotropical Primates 14(3), December 2007


100-

90-
80-
70-

60-

a 50-
40-

30-


10....








Figura 1. Resistencia antimicrobiana de 100 bacilos Gram negatives aerobios aislados de la cavidad oral de 33 monos titi (Saimiri oerstelii)
de Costa Rica.


S 25
U* 20

is
10
5
g, ,," +


0 I




./
1/ 6


S.0 -- '54

cVP
< ,
+o


Figura 2. Resistencia antimicrobiana de 31 bacteria anaerobias aisladas de la cavidad oral de 33 monos titi (Saimiri oerstedlii) de Costa
Rica.





Neotropical Primates 14(3), December 2007


especie Saimiri oerstedii. Investigaciones previas en Costa
Rica fueron realizadas en Alouatta palliata (mono congo)
y Ateles ." .. .., (mono colorado) (Gamboa-Coronado et
al., 2004), por lo que el present studio permit realizar
comparaciones entire la flora oral de diferentes species de
monos, asi como comparaciones con la flora humana.

Se logr6 aislar un promedio de 4.1 cepas por muestra, sin
embargo se encontr6 mayor cantidad de aerobics (3.2 por
muestra) que de anaerobios (0.9 por muestra), a diferen-
cia de los patrons esperados en la cavidad oral humana,
donde la proporci6n favorece a las bacteria anaerobias.
Este resultado pudo deberse a factors relacionados con
las dificultades de la toma de muestras para anaerobios y
el transport de las mismas al laboratorio. Para tomar la
muestra se emple6 una torunda que se suspendi6 en so-
luci6n salina y posteriormente dicha suspension se in6-
culo en tubos prerreducidos, es decir con atm6sfera libre
de oxigeno; los anaerobios mais sensibles pudieron haber
perdido su viabilidad durante dicho procedimiento. Como
los muestreos fueron realizados en zonas alejadas, debi6
transcurrir un tiempo prolongado (generalmente de 24 a
48 horas) antes de que las muestras fueran procesadas en el
laboratorio. Durante el transport los tubos en anaerobiosis
debieron mantenerse a temperature ambiente, con el obje-
tivo de disminuir la solubilidad del oxigeno en el medio,
que aumenta al bajar la temperature; es por esto que no se
transportaron en refrigeraci6n como las muestras para aero-
bios. Dicha prictica pudo perjudicar la viabilidad de las es-
pecies de anaerobios con ambitos estrechos de temperature
permisivos para el crecimiento, cercanos a las condiciones
de la cavidad oral de los monos. Tales inconvenientes pu-
dieron provocar la disminuci6n en la recuperaci6n de cepas
de bacteria anaerobias.

Flora aerobia
El gdnero mais frecuentemente aislado fue Enterobacter, que
esti descrito como uno de los predominates en la cavidad
oral humana (Isenberg y D'Amato, 1995) y que fue tam-
bidn descrito como el mais abundante en la cavidad bucal
de los monos congo y colorado (Gamboa-Coronado et al.,
2004). Otras enterobacterias encontradas fueron Serratia,
Klebsiella y Citrobacter con frecuencias de aislamiento entire
el 12% y el 18%; si bien todas han sido aisladas de la cavidad
bucal de los monos congo y colorado (Gamboa-Coronado
et al., 2004), Serratia no se ha descrito como habitante de
la flora oral humana, sino que esti asociada a superficies de
plants, suelo, semillas y agua (Grimont y Grimont, 2005),
lo que podria explicar su presencia en el mono titi.

El segundo gdnero de aerobics mais frecuentemente aislado
fue Burkholderia (todas las cepas identificadas como B. cepa-
cia), no descrito como habitante comin de la boca humana
ni encontrado en los monos congo y colorado. Esta bacte-
ria se ha aislado de suelo, plants, superficie de animals,
rizosfera y aguas (Coenye y Vandamme, 2003; Ramette et
al., 2005). Aeromonas fue el tercer genero aerobio en abun-
dancia y aunque no se asocia a la boca humana, si se ha


informado en bajas frecuencias en monos congo y colorado
(Gamboa-Coronado et al., 2004) y se ha aislado principal-
mente de fuentes de agua y aguas negras (Martin-Carnahan
y Joseph, 2005). Los gdneros Pseudomonas y Acinetobacter
estuvieron presents, respectivamente, en el 12% y 9% de
las muestras y han sido aislados de otros monos (Gamboa-
Coronado et al., 2004), pero no se consideran flora normal
de la cavidad oral humana. Ambos incluyen muchas espe-
cies ubicuas, aisladas de suelos, rios, plants y animals,
entire otros (Juni, 2005; Palleroni, 2005).

Chryseomonas fue aislado en un 9% de las muestras y
aunque su presencia en el ambiente es dudosa, este gdnero
es aparentemente sapr6fito o comensal de humans y algu-
nos animals de sangre caliente (Palleroni, 2005). Con igual
frecuencia se aisl6 Vibrio, siendo todas las cepas identifica-
das como V. parahaemolyticus; esta especie se encuentra en
ambientes acuaticos, pero parece estar limitada a estuarios o
dreas costeras debido a su requerimiento de 1-8% de NaCl.
Se asocia a animals marines (Carnahan y Andrews, 2000),
por lo que su aparici6n en el mono podria estar asociada a
hibitos alimenticios o de consumo de agua, tomando en
cuenta que los sitios de muestreo estin localizados cerca de
zonas maritimas. Este genero ha sido descrito como parte
de la microbiota subgingival de la especie Saimiri sciureus
(Beem etal., 1991).

En cuanto a los cocos Gram positives aerobics, los gdneros
Staphylococcus y Streptococcus son los mas frecuentes en la
cavidad oral humana (Isenberg y D'Amato, 1995) y se han
descrito en el 6% y el 2%, respectivamente, de la micro-
biota subgingival de otras species de monos ardilla (Beem
et al., 1991), ademis de que Staphylococccus se ha aislado
hasta en un 67% de los monos congo y colorado (Gam-
boa-Coronado et al., 2004). En este studio, sin embargo,
se aislaron s6lo tres cepas de cocos Gram positivos, perte-
necientes todas al gdnero Staphylococcus; los estreptococos
no pudieron ser detectados probablemente debido a que
son un gdnero nutricional y fisiol6gicamente mais exigen-
te. Adicionalmente, se aislaron tres cepas de Bacillus sp.,
gdnero que constitute hasta el 12% de la flora subgingival
de otros monos ardilla (Beem et al., 1991).

Otros gdneros menos frecuentes en estos monos y no des-
critos como pertenecientes a la cavidad oral humana fueron
Brevundimonas, VIo agl.c'//. Pantoea, Ralstonia y Flavimo-
nas (6% cada uno) y Agrobacterium, Alcaligenes, Chromo-
bacterium, Kluyvera, Leclercia, Ochrobacter, Pasteurella y
Stenotrophomonas (3% cada uno). De &stos, s6lo Chromo-
bacterium fue aislado previamente de los monos congo y
colorado, tambidn con baja frecuencia (Gamboa-Coronado
et al., 2004). Brevundimonas, Pantoea, Ralstonia, Flavimo-
nas, Agrobacterium, Alcaligenes, Chromobacterium, Kluyve-
ra, Leclercia y Stenotrophomonas se encuentran ampliamen-
te distribuidos en el ambiente, en suelos y aguas, lo que
podria explicar su aparici6n en el mono titi, mientras que
loIgIpa'Illi. Flavimonas, Alcaligenes y Pasteurella son consi-
derados comensales de mamiferos, entire otros vertebrados





Neotropical Primates 14(3), December 2007


(Busse y Auling, 2005; Janda y Abbott, 2005; Mutters et
al., 2005; Palleroni, 2005).

Flora anaerobia
Las bacteria anaerobias mais usuales en la cavidad oral del
hombre son Actinomyces, Bacteroides, Eubacterium, Fuso-
bacterium, Peptostreptococcus, Prevotella y Veillonella (Isen-
berg y D'Amato, 1995). De ellos Fusobacterium fue el mais
frecuentemente aislado en el mono titi (12% de las mues-
tras), seguido por Bacteroides, Peptostreptococcus, Prevotella
y Veillonella (6% cada uno). Estudios anteriores en monos
informan de frecuencias que van desde el 4% al 50% para
estos organismos (Clark et al., 1988; Beem et al., 1991;
Gamboa-Coronado et al., 2004). B. gingivalis y B. inter-
medius han sido encontrados como posibles pat6genos de
enfermedad periodontal, lo que podria correlacionar con el
aislamiento de Bacteroides en S. oerstedii (Clark et al., 1988).
Debido a que no se encontraron Actinomyces ni Eubacterium
siguiendo el mismo protocolo de muestreo, es possible que
no esten presents en S. oerstedii, aunque si se han aislado
de otros monos de Costa Rica. Con respect a Gemella, su
habitat natural no ha sido completamente establecido, sin
embargo su aparici6n en un 6% de las muestras, asi como
en la cavidad oral de otros monos (Gamboa-Coronado et
al., 2004), podria sugerir que constitute parte de la flora
normal del tracto respiratorio superior de estos animals.
Con una frecuencia menor se aisl6 Propionibacterium (3%),
gdnero encontrado principalmente en derivados licteos y
en la piel humana (Holt et al., 2000).

El gdnero de anaerobios mis frecuente fue Clostridium, ais-
lado del 36% de las muestras. Dicho gdnero tambidn se
describi6 como el anaerobio mis abundante en los monos
congo y colorado (48%: Gamboa-Coronado et al., 2004),
aunque en otras species de mono ardilla se sefiala como
constituyente de s6lo el 0.5% de la flora subgingival (Beem
et al., 1991). A pesar de que en los humans no se con-
sideran flora indigena oral, los clostridios son habitantes
normales del suelo y todas las species identificadas (C bi-
fermentans, C clostridiiforme, C. perfringens, C. sporogenes y
C. tyrobutyricum) se han logrado aislar de suelos de Costa
Rica con frecuencias que van del 21% al 50% (Rodriguez
et al., 1993; Gamboa et al., 2005), lo que explica la posibi-
lidad de que estas bacteria se ubiquen en la cavidad bucal
de los monos, a partir de la ingesta de alimentos y agua
contaminados con esporas de clostridios. Sin embargo, su
alta frecuencia sugiere que este gdnero podria ser verdadera-
mente parte de la flora normal de la boca de los monos.

Resistencia antimicrobiana en bacteria aerobias
Gran parte de las cepas bacterianas aisladas presentaron
resistencia antimicrobiana ante various agents quimiotera-
p6uticos, donde sobresale la alta resistencia de los bacilos
Gram negativos aerobics y de los cocos Gram positivos.
Para el primer grupo, un 90% de las cepas fue resistente a
cefalotina, cefalosporina de primera generaci6n, mientras
que un 89% a cefoxitina y un 69% a cefuroxima, cefalos-
porinas de segunda generaci6n. Este resultado es similar al


obtenido para las cepas aisladas de otros monos de Costa
Rica, donde la mayor resistencia dentro de las cefalospori-
nas se present para la cefalotina, aunque en menor porcen-
taje (63%: Gamboa-Coronado et al., 2004). La menor re-
sistencia a la cefepima (12.7%) era de esperar, debido a que
es una cefalosporina de cuarta generaci6n, con el mayor
espectro de actividad de las cefalosporinas disponibles ac-
tualmente (Gomis et al., 1998). La cefepima es mais stable
y menos afin ante las beta lactamasas, por lo que el hallazgo
de bacteria de la flora normal de los monos (particular-
mente cepas de Enterobacter, tipicamente sensibles) (Gomis
et al., 1998) resistentes a esta droga es preocupante, dado
que su uso es muy limitado al ambiente hospitalario. Por
su parte, el 65% de las cepas de bacilos Gram negativos
present resistencia a amoxicilina, similar a las cepas de los
monos congo y colorado (71%: Gamboa-Coronado et al.,
2004). Dicho resultado correlaciona con el hecho de que
la amoxicilina es uno de los antibi6ticos mas empleados
en el sistema de salud del pals, debido a su bajo precio y su
amplio espectro.

Los resultados muestran una important resistencia de
los bacilos Gram negativos ante los aminoglic6sidos: to-
bramicina (52%), gentamicina (32%), netilmicina (28%)
y amikacina (25%). La menor resistencia a la amikacina
puede explicarse debido a que por diferencias estructurales,
este antibi6tico no es inactivado por las enzimas intrace-
lulares comunes que inactivan gentamicina y tobramicina
(Gonzilez y Spencer, 1998). A pesar de esto, la resistencia
es mayor en las cepas aisladas del mono titi, si se le compa-
ra con los patrons de otros monos de Costa Rica, donde
dichos antimicrobianos fueron efectivos contra todos los
bacilos Gram negativos aislados (Gamboa-Coronado et al.,
2004). La resistencia de bacilos Gram negativos aerobics
aislados de animals ha sido descrita previamente; studios
han demostrado la presencia de cepas de Escherichia coli en
mandriles salvajes con niveles de resistencia menores que
los presentados por cepas provenientes de humans con-
temporineos, pero similares a los de cepas obtenidas en la
era previa a los antibi6ticos (Routman et al., 1985). Por
otro lado, se ha encontrado que bacteria entericas aisla-
das de mandriles en contact con el ser human presentan
niveles significativamente mayores de resistencia, en com-
paraci6n con las cepas de mandriles sin contact con el
hombre (Rolland et al., 1985); ambos hallazgos favorecen
la hip6tesis de que el amplio uso de antimicrobianos por
parte del ser human ha promovido la distribuci6n de los
genes de resistencia entire las bacteria.

Los cocos Gram positivos aerobics, correspondientes todos
al gdnero Staphylococcus, presentaron una multirresistencia
important ante los antibi6ticos evaluados. Las tres cepas
fueron resistentes a nueve de las 15 concentraciones de
antimicrobianos probadas (60%): penicilina, cefalotina,
ampicilina + sulbactam, eritromicina, clindamicina, nitro-
furantoina, rifampicina, vancomicina y teicoplanina. Sola-
mente la pefloxacina, ciprofloxacina y tetraciclina fueron
efectivas contra todos los aislamientos. Estos resultados





Neotropical Primates 14(3), December 2007


son alarmantes si se comparan con los obtenidos para los
monos congo y colorado de Costa Rica, donde el 67%
de los antibi6ticos fueron efectivos contra las 21 cepas de
cocos Gram positivos aislados (Gamboa-Coronado et al.,
2004). La resistencia creciente a antibi6ticos por parte de
los estafilococos se conoce desde hacevarios afos. Lavanco-
micina todavia se consider como el mej or antimicrobiano
disponible para el tratamiento de infecciones por estafilo-
cocos resistentes a las penicilinas que no son inhibidas por
las penicilinasas; sin embargo, ya se report una resistencia
incipiente a este firmaco por parte de los estafilococos (No-
darse, 2001), como se observa en este studio (todas las
cepas resistentes) y en caso de aumentar representaria una
verdadera catistrofe en la quimioterapia.

Resistencia antimicrobiana en bacteria anaerobias
La resistencia antibacteriana que presentaron las bacteria
anaerobias fue considerablemente menor con respect a la
de las otras bacteria. El mayor porcentaje de resistencia
se present ante metronidazole (35%), al igual que ocu-
rri6 en otros monos del pals (49%: Gamboa-Coronado et
al., 2004). Ademis de presentar excelente actividad ante
Bacteroides fragilis, Fusobacterium sp. y Clostridium perfrin-
gens (Chow, 2000), este agent es utilizado tambidn para
el tratamiento de infecciones por protozoarios, por lo que
su difundida aplicaci6n ha favorecido la aparici6n de cepas
resistentes aisladas de animals y del ser human (Diniz
et al., 2000). La resistencia se present en el 52.4% de
los anaerobios Gram positivos y abarc6 todos los gdneros,
mientras que la droga fue efectiva contra todos los Gram
negativos. Este hallazgo es similar al 3% de resistencia en
Gram negatives y el 53.6% en Gram positives encontrado
por Boyanova y colaboradores (2000) en aislamientos de
muestras clinics, pero contrast con el 44% de resistencia
presentado por Gram negativos en el caso de los monos
congo y colorado (Gamboa-Coronado et al., 2004).

La clindamicina es un antibi6tico muy dtil para el trata-
miento de anaerobios y su amplio uso favorece la aparici6n
de cepas resistentes, principalmente por la alteraci6n no
enzimitica del sitio de acci6n (Falagas y Siakavellas, 2000).
Asi por ejemplo, se han observado recientemente porcen-
tajes de resistencia entire 5 y 15% para Bacteroidesfragilis y
entire 15 y 30% para otros miembros del grupo B. fragilis,
organismos para los cuales se ha considerado tipicamen-
te este agent como una excelente opci6n de tratamiento
(Lorber, 1995; Falagas y Siakavellas, 2000). En el presen-
te studio se obtuvo un 23% de resistencia a clindamicina
(29% en Gram positivos y 10% en Gram negativos, inclu-
yendo una cepa de Bacteroides distasonis) y es similar al 28%
mostrado por los anaerobios de otros monos de Costa Rica.
Estos resultados son preocupantes, si se consideraba que
de los aislamientos clinics, menos del 10% de los Gram
negativos y el 19.6% de los Gram positives son resistentes
(Engelkirk et al., 1992) y mas adn si se compare con la
ausencia de resistencia obtenida para clindamicina en cepas
aisladas de saliva humana (Stark et al., 1993). De las cefa-
losporinas, la cefoxitina es probablemente la mais efectiva


(Murdoch, 1998), lo que concuerda con los hallazgos en
el mono titi; sin embargo, hubo una mayor resistencia que
la obtenida para las cepas de los monos congo y colorado
(Gamboa-Coronado et al., 2004). Los informes relaciona-
dos con el incremento continue en la resistencia ante estas
cefalosporinas por parte de algunos grupos de anaerobios
(Behra-Miellet et al., 2003) refuerza la importancia de la
b6squeda de nuevas estrategias para combatirlos.

La resistencia de los anaerobios alas penicilinas fue de 19%
para la penicilina y 16% para la amoxicilina; sin embar-
go, como era de esperar de acuerdo con su mecanismo de
acci6n, fue mayor en Gram negativos (30% penicilina; 20%
amoxicilina) que en Gram positivos (14% para ambos an-
tibi6ticos). La resistencia informada para las cepas de otros
monos de Costa Rica es mayor para penicilina (31%) y
menor para amoxicilina (10%) (Gamboa-Coronado et al.,
2004). Numerosos studios revelan un aumento creciente
en la resistencia a penicilina por parte de various grupos de
anaerobios: Clostridium (Engelkirk et al., 1992), Bacteroides
(Engelkirk et al., 1992) y Prevotella (Hecht, 1999), mien-
tras que otros como Propionibacterium, Peptostreptococcus y
Gemella tienden a ser susceptibles (Murdoch, 1998; Hecht,
1999). En el caso de la ticarcilina se obtuvo una resistencia
del 10%, mayor que la descrita para los monos congo y
colorado (2%: Gamboa-Coronado etal., 2004); sin embar-
go, la susceptibilidad aument6 hasta el 100% al probar este
antibi6tico conjuntamente con Acido clavulknico como in-
hibidor de beta lactamasas.

Multirresistencia
Dentro de todos los grupos bacterianos estudiados se pre-
sent6 multirresistencia, principalmente en los bacilos Gram
negativos aerobics y en los estafilococos, y en menor media
en los anaerobios. Sobresale el hecho de que un 6% de los
bacilos Gram negativos aerobics fueron resistentes a 13 o
mais de las 24 concentraciones de antibi6ticos evaluadas,
mientras que las tres cepas de Staphylococcus fueron re-
sistentes a 10 o hasta 12 de los 16 agents probados. En
los anaerobios la resistencia multiple es apreciablemen-
te menor, ya que 39% de las cepas fueron sensibles a las
16 concentraciones de antimicrobianos, el 35% fue resisten-
te a uno 6 dos, mientras que s6lo el 26% mostr6 resistencia
desde tres hasta siete agents; sin embargo, dicho hallazgo
no deja de ser alarmante, pues tradicionalmente se ha creido
que la resistencia multiple no es un problema comin en
anaerobios (Gamboa-Coronado et al., 2004). Las sustancias
antimicrobianas pueden estar presents de manera natural
en suelos, ya que constituyen un mecanismo utilizado por
los microorganisms en sus habitat naturales; la resistencia
contra estos agents juega un papel important en la dini-
mica poblacional de estos ambientes (Kiimmerer, 2004).
Por otro lado existe la resistencia intrinseca hacia ciertos
agents, debido a la fisiologia natural de algunos microor-
ganismos (Kiimmerer, 2004). Estos factors permiten con-
cluir que no es de extrafar la presencia de ciertos niveles de
resistencia en los organismos aislados de la cavidad oral de
S. oerstedii; sin embargo, estos niveles son altos y similares





Neotropical Primates 14(3), December 2007


a los encontrados en poblaciones humans, lo que sugiere
la influencia de una presi6n selective generada por el uso
excesivo de antibi6ticos. Millones de ,l.. rd ... de agents
antimicrobianos son usados cada afio en la profilaxis y trata-
miento de personas, animals y en agriculture, favoreciendo
la generaci6n de resistencia al eliminar cepas susceptibles y
seleccionar las resistentes (Levy y Marshall, 2004).

Los ambientes naturales no estin libres de contaminaci6n
con antibi6ticos; se han encontrado en efluentes de centros
mddicos, aguas municipales, tanques de aireaci6n, tanques
de digesti6n anaerobia, aguas superficiales, sedimentos y
suelo (Kiimmerer, 2003, 2004). Muchos de los compuestos
utilizados en medicine son s6lo parcialmente metabolizados
por los pacientes y son descargados en los efluentes hospita-
larios o en las aguas de desecho municipales si se utilizan en
casa (Kiimmerer, 2004), mismo destino que tienen muchos
de los antibi6ticos descartados por vencimiento (Hartmann
et al., 1999; Kiimmerer, 2003). Asi, estos compuestos ter-
minan en el ambiente, principalmente en el compartimen-
to acuoso, donde se encuentran cada vez con mayor fre-
cuencia (Levy y Marshall, 2004) y eventualmente podrian
ingresar en la cadena alimentaria. Los antimicrobianos son
tambidn utilizados para el tratamiento de enfermedades en
criaderos de peces, donde son adicionados directamente al
agua (Kiimmerer, 2004), mientras que otros son utilizados
con fines veterinarios o como promotores de crecimiento,
por lo que al ser excretados terminan siendo redistribuidos
como abono (Kiimmerer, 2003).

En Costa Rica actualmente los hospitals no cuentan con
sistemas de tratamiento de aguas residuales y el pals carece
de la legislaci6n adecuada para la regulaci6n del uso de an-
tibi6ticos en agriculture y ganaderia (Tzoc et al., 2002). Se
cree que la exposici6n de las bacteria a estas concentracio-
nes antimicrobianas subterap6uticas, incrementa la veloci-
dad de selecci6n de cepas resistentes (Kiimmerer, 2003), lo
que aunado a la transferencia de determinantes gen6ticos
de resistencia presents en el ambiente, podria explicar en
parte los patrons de resistencia encontrados en los monos
titi, aunque estos tengan poco contact director con el ser
human. Este studio contribute al conocimiento y al
mismo tiempo a la preservaci6n del mono titi, animal en
peligro de extinci6n, y muestra que pocas barreras son ca-
paces de contener los genes de resistencia y sus hospederos
bacterianos en nuestro mundo estrechamente relacionado.

Agradecimientos

Queremos agradecer al Dr. Misael Chinchilla por su apoyo
logistico en la investigaci6n. Este trabajo fue realizado gra-
cias al soporte econ6mico de la Vicerrectoria de Investiga-
ci6n de la Universidad de Costa Rica.

Referencias

Beem, J. E., Hurley, C. G., Magnusson, I., McArthur, W. P.
y Clark, W.B. 1991. Subgingival microbiota in squirrel


monkeys with naturally occurring periodontal diseases.
Infect. Immun. 59: 4034-4041.
Behra-Miellet, J., Calvet, L., Mory, E, Muller, C., Cho-
marat, M., B&zian, M.C., Bland, S., Juvenin, M.E.,
Fosse, T., Goldstein, E, Jaulhac, B. y Dubreuil, L. 2003.
Antibiotic resistance among anaerobic Gram-negative
bacilli: Lessons from a French multicentric survey. An-
aerobe 9: 105-111.
Bowers, L., Purcell, J., Plauch6, G., Denoel, P., Lovet, Y.
y Philipp, M. 2002. Assesment of the nasopharyngeal
bacterial flora of rhesus macaques: Moraxella, Neisseria,
Haemophilus, and other genera. J. Clin. Microb. 40:
4340-4342.
Boyanova, L., Petrov, D., Osmanliev, D., Mitov, I., Usuno-
va, I., Minchev, T., Goranov, E., Plochev, M. y Dimitrov,
J. 2000. Anaerobic bacteriology in 75 cases of thoracic
empyema in Sofia, Bulgaria. Anaerobe 6: 81-85.
Busse, H.J. y Auling, G. 2005. Genus I. Alcaligenes. In:
Bergey's Manual of Systematic Bacteriology, 2a Edici6n,
Vol. 2, D.J. Brenner; N.R. Krieg y J.T. Staley (eds.),
pp.653-658. Springer, USA.
Campbell, N., Clow, D., Crane, A. y MacDonald, A.
2003. "Squirrel Monkeys". En: Southern Kings Con-
solidated School ( sqmonkey.htm>).
Carnahan, A.M. y Andrews, G. 2000. Vibrio, Aeromonas,
Plesiomonas and Campylobacter species. En: Textbook of
Diagnostic _11. ..' '.. i. 2a Edici6n, C.R. Mahon and
G. Manuselis (ed.), pp.515-538. W.B. Saunders Com-
pany, Philadelphia.
Carrillo, E., Wong, G. y Sienz, J.C. 2000. Mamiferos de
Costa Rica. INBio, Heredia.
Chow, A.W. 2000. Anaerobic infections: Management of
anaerobic infections. En: Infectious Disease, V Anaerobic
Infections, ACP Medicine Online, D.C. Dale and D.D.
Federman (eds.). WebMD Inc., New York.
CITES. 2003. "Saimiri oerstedii". En: Base de datos de es-
pecies de la CITES species.html>. Consultado el 20 de octubre de 2007.
Clark, W. B., Magnusson, I., Abee, C., Collins, B., Beem,
J.E. y McArthur, W.P. 1988. Natural occurrence of
black-pigmented Bacteroides species in the gingival
crevice of the squirrel monkey. Infect. Immun. 56:
2392-2399.
Coenye, T. y Vandamme, P. 2003. Diversity and signifi-
cance of Burkholderia species occupying diverse ecologi-
cal niches. Environ. Microbiol. 5: 719-729.
Diniz, C.G., Santos, S.G., Pestana, A.C.N.R., Farias,
L. M. y Carvalho, M. A. R. 2000. Chromosomal breakage
in the B. fragilis group induced by metronidazole treat-
ment. Anaerobe 6: 149-153.
Engelkirk, P.G., Engelkirk, J.D. y Dowell, V.R. 1992.
Principles and Practice of Clinical Anaerobic Bacteriology,
Susceptibility Testing. Star Publishing Co., Belmont.
Falagas, M. E. y Siakavellas, E. 2000. Bacteroides, Prevotella
and Porphyromonas species: A review of antibiotic resis-
tance and therapeutic options. Int. J. Antimicrob. Agents
15: 1-9.





Neotropical Primates 14(3), December 2007


Gamboa-Coronado, M.M., Rodriguez-Cavallini, E., Ro-
jas-Contreras, G., S&nchez-Porras, R. y Gutikrrez-Espele-
ta, G. 2004. Flora bacterial oral y su perfil de sensibilidad
a antibi6ticos en monos de Costa Rica (Alouattapalliata y
Ateles '.. r.,, i Neotrop. Primates 12(1): 24-30.
Gamboa, M. M., Rodriguez, E. y Vargas, P. 2005. Diversity
of mesophilic clostridia in Costa Rican soils. Anaerobe
11: 322-326.
Gomis, M., Barberin, J., Ferrnndez, A. y S&nchez, B. 1998.
Cefepima en el paciente neutropenico febril. Rev. Esp.
Quimioterap. 11: 12-16.
Gonzilez, L. S. y Spencer, J.P. 1998. Aminoglycosides: a
practical review. Am. Fam. Physician. 58: 1811-1820.
Grimont, F. y Grimont, P.A.D. 2005. Genus XXXIV. Ser-
ratia. En : Bergey's Manual of Systematic Bacteriology, 2a
Edici6n, Vol. 2, D.J. Brenner, N.R. Krieg y J.T. Staley
(eds.), pp.799-811. Springer, New York.
Hartmann, A., Golet, E.M. y Gartiser, S. 1999. Primary
DNA damage but not mutagenicity correlates with cip-
rofloxacin concentrations in German hospitals' waste
waters. Arch. Environ. Contam. Toxicol. 36: 115-119.
Hecht, D.W. 1999. Susceptibility testing of anaerobic bac-
teria. En: Manual of Clinical -V. ..'...' .. 7a Edici6n,
P. R. Murray (ed.), pp.1555-1565. ASM Press, Washing-
ton, DC.
Holt, J.G., Krieg, N.R., Sneath, P.H.A., Staley, J.T. y
Williams, S.T. 2000. Bergey's Manual of Determinative
Bacteriology, 9q Edici6n. Williams & Wilkins, Baltimore,
Maryland.
Isenberg, H.D. y D'Amato, R.E 1995. Indigenous and
pathogenic microorganisms of humans. En: Manual of
Clinical M1. ..' .'..' 6a Edici6n, P.R. Murray (ed.),
pp.5-18. ASM Press, Washington, DC.
IUCN. 2007. 2007 IUCN Red List of Threatened Species.
. Consultado el 20 de octu-
bre de 2007.
Janda, J.M. y Abbott, S.L. 2005. Genus XXI. Mol:gme/lla.
En: Bergey's Manual of Systematic Bacteriology, 2a Edici6n,
Vol. 2, D.J. Brenner; N.R. Krieg and J.T. Staley (eds.),
pp.707-709. Springer, New York.
Juni, E. 2005. Genus II. Acinetobacter. En: Bergey's Manual
of Systematic Bacteriology, 2a Edici6n, Vol. 2, D.J.
Brenner, N.R. Krieg y J.T. Staley (eds.), pp. 425-437.
Springer, New York.
Kiimmerer, K. 2004. Resistance in the environment. J. An-
timicrob. Chemother. 54: 311-320.
Kilmmerer, K. 2003. Significance of antibiotics in the envi-
ronment. J. Antimicrob. Chemother. 52: 5-7.
Kilmmerer, K. 2001. Drugs in the environment: emission
of drugs, diagnostic aids, and disinfectants into wastewa-
ter by hospitals, in relation to other sources a review.
Chemosphere 45: 957-69.
Levy, S. B. y Marshall, B. 2004. Antibacterial resistance
worldwide: Causes, challenges and responses. Nat. Med.
Suppl. 10: 122-129.
Lorber, B. 1995. Bacteroides, Prevotella and Fusobacte-
rium species (and other medically important anaero-
bic gram-negative bacilli). En: Mandell, Douglas and


Bennett' Principles and Practice of Infectious Diseases,
4a Edici6n, G. L. Mandell, J. E. Bennett y R. Dolin (eds.),
pp.2195-2204. Churchill Livingston, New York.
Martin-Carnahan, A. y Joseph, S.W. 2005. Genus I. Aero-
monas. In: Bergey's Manual of Systematic Bacteriology,
2a Edici6n, Vol. 2, D.J. Brenner, N. R. Krieg y J.T. Staley
(eds.), pp.557-578. Springer, New York.
Murdoch, D.A. 1998. Gram-positive anaerobic cocci.
Clin. Microbiol. Rev. 11: 81-120.
Mutters, R., Christensen, H. y Bisgaard, M. 2005. Genus
I. Pasteurella. En: Bergey's Manual of Systematic Bacteri-
ology, 2a Edici6n, Vol. 2, D.J. Brenner, N.R. Krieg y
J.T. Staley (eds.), pp.857-866. Springer, New York.
Nodarse, R. 2001. Estafilococos multirresistentes: uso del
disco de oxacillin como marcador de resistencia a anti-
bi6ticos. Rev. Cub. Med. Mil. 30: 7-10.
Palleroni, N. 2005. Genus I. Pseudomonas. En: Bergey's
Manual of Systematic Bacteriology, 2a Edici6n, Vol. 2, D.J.
Brenner, N.R. Krieg y J.T. Staley (eds.), pp.323-379.
Springer, New York.
Ramette, A., LiPuma, J.J. y Tiedje, J.M. 2005. Species
abundance and diversity of Burkholderia cepacia com-
plex in the environment. Appl. Environ. Microbiol. 71:
1193-1201.
Rodriguez, E., Gamboa, M.M. y Fernandez, B. 1993.
Clostridios mes6filos en suelos de la Meseta Central de
Costa Rica. Rev. Biol. Trop. 41: 365-369.
Rolland, R., Hausfater, G., Marshall, B. y Levy, S.B. 1985.
Antibiotic-resistant bacteria in wild primates: Increasing
prevalence in baboons feeding on human refuse. Appl.
Environ. Microbiol. 49: 791-794.
Routman, E., Miller, R.D., Phillips Conroy, J. y Hard,
D.L. 1985. Antibiotic resistance and population struc-
ture in Escherichia coli from free-ranging African yellow
baboons. Appl. Environ. Microbiol. 50: 749-754.
Sorum, H. y Sunde, M. 2001. Resistance to antibiotics in
the normal flora of animals. Vet. Res. 32: 3-4.
Stark, C.A., Edlund, C., Sjostedt, S., Kristensen, G. y
Nord, C.E. 1993. Antimicrobial resistance in human
oral and intestinal anaerobic microfloras. Antimicrob.
Agents Chemother. 37: 1665-1669.
Tzoc, E., Arias, M.L. y Valiente, C. 2004. Efecto de las
aguas residuales hospitalarias sobre los patrons de resist-
encia a antibi6ticos de Escherichia coli y Aeromonas sp.
Rev. Biomed. 15: 165-172.
Wong, G. 1990. Uso del habitat, estimaci6n de la composi-
ci6n y densidad poblacional del mono titi (Saimiri oerstedi
citrinellus) en la zona de Manuel Antonio. Quepos, Costa
Rica. Tesis de Maestria, Universidad Nacional, Programa
Regional en Manejo de Vida Silvestre para Mesoam&rica
y el Caribe.





Neotropical Primates 14(3), December 2007


BEHAVIORAL FLEXIBILITYAND TOOL SELECTION
IN A TUFTED CAPUCHIN MONKEY (CEBUS
APELLA)

Euphly Jalles-Filho
Rogerio Grassetto Teixeira da Cunha
Rodolfo Aureliano Salm

Introduction

Capuchin monkeys use a variety of tools in many differ-
ent contexts in captivity (Visalberghi, 1987, 1990, 1993;
Ritchie and Fragaszy, 1988; Westergaard and Suomi, 1994;
Tomasello and Call, 1997; Fragaszy et al., 2004b), in semi
free-ranging conditions (Ottoni and Mannu, 2001) and
in the wild (Fragaszy et al., 2004a; Moura and Lee, 2004;
Mannu and Ottoni, 2005; but see Panger, 1998). In terms
of tool variety and the multiple contexts in which tools
are used, capuchins are similar to great apes in tool-using
behavior (Anderson, 1996). Some argue that the abil-
ity to use tools requires the cognitive ability to establish
a relationship between the object and the environment in
order to implement anticipated external effects (Reynolds,
1982; Ingold, 1987). Research on tool-using behavior in
non-human primates has often described tool-use perform-
ance without analyses of the underlying cognitive processes
(Visalberghi and Limongelli, 1996), although noteworthy
exceptions are found in the classic works of Kbhler (1925)
and Yerkes (1927, 1943). In terms of the relationship of
cognition and intelligence to tool use, there may be little
similarity between capuchins and the great apes. There is
growing evidence that apes understand what they are doing
when using tools (e.g. Boesch, 1992; McGrew, 1992), but
this has not been shown for capuchins. To compare, in a
context of tool use, the cognitive abilities of chimpanzees
(or other primate species) and those of capuchin monkeys,
we must look for the underlying mental program that both
guides and is expressed in tool-using behavior.

In this study, we do not assume a priori that capuchins are
less, more or equally intelligent than other primate spe-
cies. Capuchins, just like chimpanzees, humans, whales or
any other species, possess a particular and limited suite of
cognitive capacities. Here we describe the results of an ex-
periment that evaluated the ability of a capuchin monkey
to select appropriate tools in a nut-cracking task. We also
speculate on the possible factors involved in tool selection.

Materials and Methods

Subjects
A group of capuchin monkeys (Cebus apella sp.) were housed
on a small island within a zoo setting (Parque Ecol6gico
Municipal Eng Cid Almeida Franco, Americana, Sao


Paulo, Brazil). The alpha male was the experimental sub-
ject. He was an adult, wild-born and raised in captivity. He
monopolized almost every new object in the small home
island and prevented regular access to them by the other
animals, leaving us without much choice regarding experi-
mental subjects. It was not possible to remove the alpha
male from the island. As the other monkeys had only un-
predictable access to the objects, it was not possible to apply
the experimental protocol to them in any regular or reliable
manner. However, a juvenile male and an adult female that
used tools on some occasions were included for qualita-
tive comparisons. All three monkeys had been observed
to spontaneously use tools (see below) and/or took part in
other tool use experiments (Jalles-Filho et al., 2001), and
were thus proficient in the use of tools.

Test phase
In each trial the subject was offered one of three stones
(cobbles of quartzite) of similar shape but different sizes
(large: 1,565 g; medium: 915 g; small: 110 g), and one
nut. Twenty trials were performed per stone (17 for the
small stone). A trial began when the subject held the stone
in his hands to give the first blow, and ended when the nut
was broken. The time and the number of blows required
to complete the task were recorded. Here, "nut" actually
refers to the fruits of Terminalia spp. (Combretaceae), a
species that is found in the zoo. Monkeys were observed
to crack these fruits spontaneously with the assistance of
stones naturally available on the island. This fruit has a soft
external layer and, underneath it, a second fibrous and hard
layer, which has to be broken in order to reach the edible
seed, something the monkeys could do only with the as-
sistance of tools. We draw attention to the fact that the test
phase was not designed to give the subjects experience with
the different stones. Instead, it was conceived to guide us in
evaluating the magnitude of the effect of stone size on the
efficiency of accomplishing the task.

Experimentalphase
The same three stones of different sizes were simultaneously
presented to the subject, and a single nut was offered. Cri-
teria for the starting and ending of the trials were the same
as in the test phase, unless the nut was left undisturbed
for three minutes, in which case the trial ended. In each
trial, the order of lateral placement of the stones was al-
tered. A total of 50 trials were performed. Both phases were
videotaped for subsequent analysis.

Qualitative analysis
The two comparison subjects were videotaped in situations
of tool use identical to those performed by the experimen-
tal subject.

Results

During the test phase, there was a significant effect of stone
size on the number of blows required to complete the task
(Kruskal-Wallis ANOVA X2 (17, 2)=36.95, p<0.0001,





Neotropical Primates 14(3), December 2007


Table 1. Summary of tool-using activities in the test phase. (Trials:
LS and MS, n= 20; SS, n= 17.) LS (large stone); MS (medium
stone); SS (small stone).

Type of Number Mean Mean
stone of blows per trial Time (s) per trial
(x + SE) (x + SE)
Large 67 3.35 + 0.43 135.52 6.78 + 1.12
Stone
Medium 82 4.1 + 0.34 157.91 7.9 + 0.9
Stone
Small 381 22.41 + 1.9 739.04 43.47 + 6.44
Stone


Monte Carlo method; see Table 1). Post-hoc tests re-
vealed that use of the small stones required significantly
more blows than the medium or large stones (Nemenyi-
Dunn multiple comparisons test, for samples of unequal
size, p < 0.0001). However, there was no significant differ-
ence in number of blows required between the large and
medium stones (Mann-Whitney Test: U= 144.0; p = 0.134
- exact test, two-tailed). Since the assumption of spheric-
ity required for a repeated measures ANOVA was violated
(Mauchly's sphericity test, w= 26.72, p< 0.0001), we com-
pared the duration data across conditions with a repeated
measures MANOVA, which showed a significant differ-
ence across the different stone sizes (R (2, 15) = 18.62,
p < 0.0001). The values associated with the small stone were
again responsible for the difference (Spjotvoll-Stoline test
for unequal sample sizes, p < 0.001). The large and medium
stones did not differ significantly in time to task comple-
tion (Student's t-test for independent samples, t =-1.54,
p > 0.05, two-tailed). In the analysis of the experimental
phase, the subject excluded the small stone as an opera-
tive tool, but did not differentiate between the other two,
using the large stone during 28 trials and the medium one
during the other 22 trials (two-tailed binomial test, n = 50,
p > 0.5).

Discussion

When given the choice between three different stone sizes,
the experimental subject rejected the small stone as a useful
tool, but did not differentiate between the other two. The
subject's use of the large and medium stones did not differ
with regard to the number of blows or in relation to the
time necessary to complete the task, and the movements
executed by the subject were exactly the same in both cases.
Thus, the only differential factor, in terms of metabolic ex-
penditure and muscular cost involved, was the magnitude
of the load. Note that a weight difference of 650 g (between
the medium and large stones) is probably a quite consider-
able one given the range of adult male weights for the spe-
cies (4.0-4.5 kg: Rowe, 1996). If the subject was choosing
tools in order to minimize energetic costs, a preference for
the medium category should be expected, but this predic-
tion was not confirmed by the experimental data. Please


note that in our analyses, there is an assumption of a dif-
ference in energetic expenditure between the medium and
large stones, and an assumption that energetic efficiency,
not time efficiency, is what the monkey should maximize.
These assumptions are based on the conditions of the ex-
periment, with a large weight difference between the stones,
and the captive setting, where animals are usually freed
from time constraints. However, until detailed measures of
energetic expenditure under different conditions are car-
ried out, our first assumption remains speculative. If there
is no significant difference in energetic expenditure and/or
if time is the variable being minimized, then one should
expect the observed lack of preference between the medium
and large stones as tools.

Bearing the above caveat in mind, the choices made by the
subject (exclusion of the small stone) could be credited to
an interaction between persistence of behavioral patterns
and physical features of the tool. During the test phase, the
individual repeatedly picked up the small stone bimanually
(like he did with the other stones), a cumbersome tech-
nique that proved very ineffective. The small stone's per-
formance as a tool was about five to six times worse than
the other tools, even though it was eight and 14 times
smaller than the medium and large stones respectively.
One might expect that the subject would adapt his manual
behaviour to best fit the tool in question (e.g., by picking
it up with only one hand), but this did not happen. We
speculate that, if the subject had changed his behavior, the
small stone could have been a reasonable choice in terms of
energetic expenditure. It is relevant that he did not change
his behaviour even once over the course of 17 test trials, nor
try to explore the small stone further as a potential tool over
the 50 experimental trials. The two comparative subjects
were also resistant to any change of established patterns of
manipulative behaviour. The juvenile male engaged in a
similar sequence of movements to the alpha male and, when
presented with the small stone, persisted in this behavioral
pattern, incurring the same difficulties as the experimental
subject. The adult female employed a different technique to
break the nuts. However, like the others, she never varied
her movement pattern regardless of the conditions of the
task. Her behavioral pattern, which was already less ef-
ficient when compared to the one exhibited by the males,
made the technique absolutely ineffective with the small
stone because of the reduced magnitude of the load.

These findings suggest that the choices made by the ca-
puchins do not spring from a more detailed means-end
analysis, but seemingly from gross physical limitations or
restrictions only, in a context of behavioral persistence.
That is, the experimental subject only rejected the very
inefficient tool, but did not choose the most energeti-
cally efficient of the other two. Furthermore, the rejection
seems to result from behavioral inflexibility, which made
the small stone a very inefficient implement, although it
seemed to have the potential to be the opposite. This re-
inforces previous doubts of capuchin behavioral flexibility





Neotropical Primates 14(3), December 2007


and other cognitive capacities, as shown in Jalles-Filho et
al. (2001). We observed the continuous reactivation of
previous manipulative action patterns, with the monkeys
always applying one and the same set of movements, ap-
parently blind to the changes in the external conditions,
even when a change was needed. In terms of the concept
of tool mentioned above, we suggest that the mental pro-
gram used by the individual to implement the operations
over the environment was lacking in complexity from the
outset. A sufficiently complex program would permit new
elements to be incorporated, and also the selection and
combination of previous elements, producing completely
new arrangements of whole motor patterns.

Previous studies of tool selection or modification (partly re-
viewed in Fragaszy et al., 2004b) have yielded mixed results
when compared the present study. In all cases, there are dif-
ferences in experimental design, some of them subtle, which
may explain the discrepancies. For example, Antinucci and
Visalberghi (1986) have shown that a capuchin monkey
was able to use three different kinds of objects (a stone,
a piece of wood, and a plastic container) as hammers to
crack open hazelnuts and walnuts. More importantly here,
they reported that the monkey showed a strong preference
for the stone, followed by the wood, with near rejection
of the plastic container. The authors did not analyze the
time or the number of blows required by each tool to fulfil
the task. They noted qualitatively that the stone was much
more effective, the piece of wood less so, and the plastic
container was completely ineffective. Thus, the monkeys
were selecting only for effectiveness, not effectiveness and
energetic efficiency, as in our case. Their subject, similar to
ours, showed rejection of a useless tool (although he still
attempted to use it a few times). However, we believe that
due to its very small weight (40 g), this tool was so ineffec-
tive that no change in behavior would make it valuable, in
contrast to the small stone in our study.

Visalberghi and Trinca (1989) have shown that capuchin
monkeys were able to solve three conditions of a tube task
in which the tools required modification before use, but
that the monkeys kept performing errors throughout the
course of those experiments. Note that, in order to be effec-
tive, the monkeys had to modify the tools, not their motor
patterns when using them-an approach which was not
possible in our test phase, since the tool could not be modi-
fied. Behaviorally, their monkeys made various different at-
tempts, but always by performing the same general action
(trying to insert something in the tube), which was abso-
lutely useless in some cases. Thus, there was some rigid-
ity in behavioral patterns as well, since they kept repeating
motor patterns with ineffective tools.

In another tube task experiment (Visalberghi, 1993), the
same capuchins selected the correct tool out of a group of
four. The other three tools in this choice experiment were
completely ineffective, whereas in our experimental phase
the comparison was between two equally effective tools


with different energetic requirements and an inefficient
one that could still be used to accomplish the task. In a dif-
ferent experimental set-up, Cummins-Sebrae and Fragaszy
(2005) showed that capuchins chose correctly positioned
canes to pull out pieces of food, but they also repositioned
canes to pull the food, and improved at the task with prac-
tice, thus discovering affordances of the tool according to
the authors. In the vast majority of their pairings, the tools
did not differ in effectiveness, only in the ease to accom-
plish the task and/or the familiarity of the animals with
them. Also, the required change in behavior for reposition-
ing might be regarded as involving a simpler mental opera-
tion (comprehension of a spatial relation) than the creation
of whole new motor patterns that would be necessary to
make the small stone an effective choice (in our case) or to
understand that splinter and tapes cannot be used to push
food out of a tube (as in the case of Visalberghi and Trinca,
1989).

Although very preliminary, our results may suggest cru-
cial differences between the tool-using behavior displayed
by chimpanzees (or other great ape species) and capuchin
monkeys, at least regarding behavioral flexibility involving
stone tools; this agrees with a growing body of literature
expressing similar doubts. The possibility that capuchins
are limited in their capacity to select appropriate tools, and
show much less flexibility in behavior than the great apes,
should at least be regarded as a working hypothesis, testable
both with similar experiments (but a larger sample size),
and also with different experimental paradigms, ideally
contrasting the aspects which varied between and within
studies (e.g. effective vs. ineffective tool; more vs. less effi-
cient tool; requiring tool modification vs. requiring behav-
ioral modification). Only through more experimentation
we will be able to fully comprehend capuchins' range of
cognitive capacities, their physical knowledge of the world,
and the relation of both to their ecology.

Acknowledgements

We thank the staff and director of the Parque Ecol6gico
Municipal de Americana Engo Cid Almeida Franco for
their logistical support and general cooperation during
our work at the zoo. R. G.T. C. received a mastership grant
CNPq 139649/96-4. Five anonymous reviewers provided
insightful comments to the manuscript.

Euphly Jalles-Filho, Rua Thomas Nogueira Gaia, 83 Jd.
Sao Luiz-Ribeirao Preto 14020-290, SP, Brazil, e-mail:
, Rog6rio Grassetto Teixeira da
Cunha, e-mail: and Rodolfo
Aureliano Salm, e-mail: .

References

Anderson, J.R. 1996. Chimpanzees and capuchin mon-
keys: Comparative cognition. In: Reaching into Thought:
The Minds of the Great Apes, A. E. Russon, K.A. Bard,





Neotropical Primates 14(3), December 2007


and S.T. Parker (eds.), pp.23-56. Cambridge University
Press, Cambridge.
Antinucci, E and Visalberghi, E. 1986. Tool use in Cebus
apella: A case study. Int. J Primatol. 7(4): 351-363.
Boesch, C. 1992. Aspects of transmission of tool-use
in wild chimpanzees. In: Tools, Language and Cogni-
tion in Human Evolution, K. R. Gibson and T. Ingold
(eds.), pp.171-183. Cambridge University Press,
Cambridge.
Cummins-Sebree, S.E. and Fragaszy, D.M. 2005. Choos-
ing and using tools: Capuchins (Cebus apella) use a dif-
ferent metric than tamarins (Saguinus oedipus). J. Comp.
Psychol. 119(2): 210-219.
Fragaszy, D.M., Izar, P., Visalberghi, E., Ottoni, E.B. and
Gomes de Oliveira, M. 2004a. Wild capuchin monkeys
(Cebus libidinosus) use anvils and stone pounding tools.
Am. J Primatol. 64: 359-366.
Fragaszy, D., Visalberghi, E. and Fedigan, L. 2004b. The
Complete Capuchin: The Biology of the Genus Cebus.
Cambridge University Press, Cambridge.
Ingold, T. 1987. The Appropriation of Nature: Essays on
Human Ecology and Social Relations. University of Iowa
Press, Iowa City.
Jalles-Filho, E., da Cunha, R.G.T. and Salm, R.A.
2001. Transport of tools and mental representation:
Is capuchin monkey tool behaviour a useful model of
Plio-Pleistocene hominid technology? J Hum. Evol.
40(5): 365-377
Kbhler, W. 1925. The Mentality of Apes. Routledge and
Kegan Paul, London.
Mannu, M. and Ottoni, E.B. 2005. Sazonalidade na uti-
lizagao de ferramentas ente esta6oes seca-chuvosa em dois
grupos livres de macacos-prego na caatinga: Dados par-
ciais. In: XXIII Encontro Anual de Etologia. Sociedade
Brasileira de Etologia, Assis, SP, Brazil.
McGrew, W.C. 1992. Chimpanzee Material Culture: Im-
plications for Human Evolution. Cambridge University
Press, Cambridge.
Moura, A.C. de A. and Lee, P. C. 2004. Capuchin stone
tool use in caatinga dry forest. Science 306: 1909.
Ottoni, E. B. and Mannu, M. 2001. Semifree ranging tufted
capuchin monkeys (Cebus apella) spontaneously use tools
to crack open nuts. Int. J Primatol. 22: 347-358.
Panger, M.A. 1998. Object-use in free ranging white-faced
capuchins (Cebus capucinus) in Costa Rica. Am. J Phys.
Anthropol. 106: 311-321.
Reynolds, P.C. 1982. The primate constructional system:
The theory and description of instrumental tool use in
humans and chimpanzees. In: The Analysis of Action,
M. Van Cranach and R. Harrd (eds.), pp. 243-385.
Cambridge University Press, Cambridge.
Ritchie, B. G. and Fragaszy, D. M. 1988. Capuchin monkey
(Cebus apella) grooms her infant's wound with tools. Am.
J Primatol. 16: 345-348.
Rowe, N. 1996. The Pictorial Guide to the Living Primates.
Pogonias Press, Charlestown, Rhode Island.
Tomasello, M. and Call, J. 1997. Primate Cognition. Oxford
University Press, Oxford.


Visalberghi, E. 1987. Acquisition of nut-cracking behav-
iour by two capuchin monkeys (Cebus apella). Folia Pri-
matol. 49: 168-181.
Visalberghi, E. 1990. Tool use in Cebus. Folia Primatol. 54:
154-64.
Visalberghi, E. 1993. Tool use in a South American monkey
species: An overview of the characteristics and limits of
tool use in Cebus apella. In: The Use of Tools by Human
and Non-human Primates, A. Berthelet and J. Chavaillon
(eds.), pp. 118-131. Oxford University Press, New York.
Visalberghi, E. and Limongelli, L. 1996. Acting and un-
derstanding: Tool uses revisited through the minds
of capuchin monkeys. In: Reaching into Thought: The
Minds of the Great Apes, A.E. Russon, K.A. Bard and
S.T. Parker (eds.), pp.57-79. Cambridge University
Press, Cambridge.
Visalberghi, E. and Trinca, L. 1989. Tool use in capuchin
monkeys: Distinguishing between performing and un-
derstanding. Primates 30: 511-521.
Westergaard, G. C. and Suomi, S.J. 1994. Stone-tool bone-
surface modification by monkeys. Current A..- .'
35: 468-470.
Yerkes, R. M. 1927. The mind of a gorilla. Genetic Psychol-
ogy Monographs 2: 1-193.
Yerkes, R.M. 1943. Chimpanzees: A Laboratory Colony.
Yale University Press, New Haven, CT.


DISTRIBUTION AND CONSERVATION STATUS
OF THE YELLOW-TAILED WOOLLY MONKEY
(OREONAX FLAVICAUDA, HUMBOLDT 1812) IN
AMAZONAS AND SAN MARTIN, PERU

Sam Shanee
Noga Shanee
Angela M. Maldonado

Introduction

The yellow-tailed woolly monkey (Oreonax flavicauda) is
one of the largest and rarest Neotropical primates. First
discovered in 1802 by Alexander von Humboldt (Hum-
boldt and Bonpland, 1812), since then only a few field
studies have been conducted on this species (Leo Luna,
1980, 1982; Butchart et al., 1995a; DeLuycker, 2007) and
it remains one of the least known of all primate species.
0. flavicauda is restricted to a small area of pre-montane
cloud forest between 1,400 and 2,500 m a.s.1. in the de-
partments of San Martin and Amazonas in northern Peru
(Leo Luna, 1980, 1982; DeLuycker, 2007). The species
probably also occurs in small areas of Cajamarca, Hua-
nuco, Loreto and La Libertad departments (Mittermeier
et al., 1975; Graves and O'Neil, 1980; Leo Luna, 1980,
1982, 1989; Parker and Barkley, 1981; DeLuycker, 2007;
Rolando Aquino, pers. com.). 0. flavicauda is endemic
to the tropical Andes biodiversity hotspot (Myers et al.,
2000), and its habitat is characterized by rugged terrain of
steep mountain sides and deep river gorges, with canopy





Neotropical Primates 14(3), December 2007


height of about 20-25 m, with a thick understory and lush
vegetation cover. Low reproductive rates, long inter-birth
intervals, low population densities, restricted habitat and
limited geographic range all increase this species' vulner-
ability to extinction from human activities affecting the Pe-
ruvian Andes (Leo Luna, 1989; IUCN, 2006). Although
no accurate census data exist, Nowak (1999) cites a popu-
lation estimate of less than 250 individuals surviving in the
wild. 0. flavicauda is listed as Critically Endangered by the
IUCN (2006) and currently featured as one of the 25 most
endangered primate taxa (Mittermeier et al., 2007).

The main threat to this species' survival is habitat loss from
deforestation (Macedo Ruiz and Mittermeier, 1979; Leo
Luna, 1980; Butchart et al., 1995b; DeLuycker, 2007).
Currently the species is present in several protected areas:
Rio Abiseo National Park, Alto Mayo Protected Forest, Cor-
dillera Colan Reserved Zone, Cordillera Escalera Regional
Conservation Area, and the Laguna de los Condores Re-
served Zone. Hunting and logging are still known to occur
in all of these reserves (e.g. Parks Watch Peru, 2003). Built
in the 1980s, the Lima-Tarapoto highway runs through the
departments of San Martin and Amazonas and brought
with it many settlers from coastal and high mountain sierra
departments (DeLuycker, 2007). Overpopulation and en-
vironmental degradation have caused continued immigra-
tion, giving San Martin and Amazonas some of the high-
est immigration levels in Peru (INEI, 2006). As a result,
since the last field survey of 0. flavicauda (Leo Luna, 1980)
the area has undergone high levels of deforestation and
many populations of the species now exist in isolated forest
fragments. Hunting is also a major threat to the survival
of the species (Macedo Ruiz and Mittermeier, 1979; Leo
Luna, 1980, 1989; Butchart et al., 1995a). In this study
we aimed to gather up-to-date information on the status of
0. flavicauda and to evaluate the current threat levels facing
it; this also serves as a preliminary study for the implemen-
tation of a larger conservation study.

Methods

Between March and June 2007 we conducted a prelimi-
nary survey of 0. flavicauda at 11 sites in Amazonas and
San Martin departments. We also collected secondary data
on a further six sites in Amazonas, Huanuco, La Libertad,
Loreto and San Martin departments. Sites listed in previ-
ous studies (Mittermeier et al., 1975; Graves and O'Neil,
1980; Leo Luna, 1980, 1982, 1989; Parker and Barkley,
1981; DeLuycker, 2007) as areas of this species' occurrence
were surveyed for the continued presence of 0. flavicauda.
Other areas where habitat and climatic requirements could
be met were also surveyed. All areas covered in this inves-
tigation were in the pre-montane cloud forest belt in the
two eastern branches of the Andean Cordillera between
05034' and 0613'S and 77001' and 7631'W (Fig. 1), at
altitudes ranging from 1,400 to 2,500 m a.s.l. Average
temperatures for these areas are approximately 14-15C,
with average monthly rainfall between 15 mm in the dry


season and 120 mm in the wet season. Primary data were
collected during forest walks along existing trail systems
accompanied by local residents. The location of all sites was
recorded with GPS, as were points of encounter with the
species. Additional data were also collected on threats to
habitat in areas where this species occurs. Incidental data
were collected on an ad libitum basis. Secondary data on
species occurrence were collected from local informants
and researchers. Additional data were collected on hunt-
ing practices, environmental problems and forest resource
uses.

Results

Groups of 0. flavicauda were found in three locations
during this study. On 13 April 2007, near the village of
Santa Rosa (0540'13.5"S, 7755'08.0"W), Amazonas
department (Fig. 1), we encountered a group of eight
0. flavicauda, consisting of five adults and three young,
accompanied by a female white-bellied spider monkey
(Ateles belzebuth; see Shanee et al., 2007). The group was
found in a fragment of forest adjoining pasture at an
altitude of 1,875 m a.s.l. Throughout the encounter the
group displayed aggressive behaviours such as branch
shaking, "mooning" of the scrotal tuft and the short
barking call characteristic of the species (Leo Luna,
1980; DeLuycker, 2007). On 2 May 2007, near the vil-
lage of Shipasbamba, (0554'35.3"S, 7758'50.3"W),
Amazonas department (Fig. 1), we encountered a group
of nine 0. flavicauda, consisting of two adult males,
three adult females, one sub-adult and three juveniles.
This group was found in an area of regenerating second-
ary forest within a larger forest fragment at an altitude of
2,305 m a.s.l., and again this group was detected aurally.
We were able to approach the group and stand directly
beneath them. Initial aggressive behaviours quickly gave
way to more relaxed foraging.

On 27 April 2007, near the village of Paitoja (0621'42.0"S,
77004'52.1"W), San Martin department (Fig. 1), we heard
the calls of two groups but were unable to locate them.
This encounter took place in an area of contiguous pri-
mary forest at an approximate altitude of 1,787 m a.s.l.
During this study we also found evidence of the presence
of 0. flavicauda in two additional sites: the private reserve
of the Peruvian NGO Associaci6n de Ecosistemas Andinas
(ECOAN), Abra Patricia (05041'52.3"S, 7748'38.6"W), in
Amazonas department on the border with San Martin, and
near the Gocta waterfalls (06001'18.4"S, 77053'12.4"W),
also in Amazonas department (Fig. 1). Abra Patricia covers
an area of mixed primary and regenerating secondary forest
adjoining the Alto Mayo Protected Forest, which is known
to contain this species (DeLuycker, 2007). At the Gocta
waterfall we found half-eaten fruit (Ficus spp.) showing
bite marks of a large bodied primate, and the presence of
0. flavicauda was confirmed by local residents who told us
of the species' occurrence in the small patch of forest sur-
rounding the waterfall.





Neotropical Primates 14(3), December 2007


We were unable to directly observe 0. flavicauda in any of
the other six sites visited in this study. However, through
informal interviews with local informants, and the use
of photographic depictions and verbal descriptions of
O.flavicauda, we were able to gather additional information


on these sites. Results from these interviews confirmed
the presence of 0. flavicauda at Colca (0553'40.9"S,
7723'15.2"W) and Nuevo Mendoza (0627'06.7"S,
77005'46.3"W) in San Martin department and La Perla
de Limasa (0534'20.1"S, 7758'53.7"W) in Amazonas


Loreto


Amazonas


- -4%


Zon da
.- Cmagadnae los
C4ndores


San Martin


'I

9
1Le
L
|

/

/ Loreto


La Libertad


Figure 1. Map of sites visited during the study, showing the presence and absence of Oreonaxflavicauda.


* City/Town
A O.flawcauda absent
E O. flavicauda present
- River
Referred to by other researcher
S- Protected area
S. Regional boundary
--. Road/Highway


.1~

9'
St -. -


-' P


** 1


40"-





Neotropical Primates 14(3), December 2007


department (Fig. 1). All other areas visited during this
study showed no evidence of the continued presence of
0. flavicauda. These included the site of the "rediscovery"
of the species in 1974 (Mittermeier et al., 1975), Pedro
Ruiz Gallo (0556'36.3"S, 7758'42.3"W) where the
area was found to be completely deforested for several ki-
lometres in all directions. The area around the town of
Yambrasbamba (0544'06.9"S, 7755'30.0"W), listed by
Leo Luna (1980) as 0. flavicauda habitat, is almost com-
pletely deforested within several kilometres of the town.
Reports from local informants and our own observations
suggest that the species does not occur in either the Gira-
Sisa Reserve (0617'34.3"S, 7654'24.7"W) or around the
town of Shimbayacu (0620'41.9"S, 7631'58.4"W) in
San Martin department. We were told of the confirmed
presence of 0. flavicauda in additional sites by researchers
working in or involved with projects there. These site were
in the Los Chilchos Valley (Hans Dignum, pers. com.),
north of the Rio Abiseo National Park in San Martin de-
partment and around the Rio Metal river valley near To-
cache in the far south of San Martin along the borders
with La Libertad and Huanuco departments (Rolando
Aquino, pers. com.).

Key informant questionnaires and ad libitum data collec-
tion showed that most people in these areas are depen-
dent on income from timber extraction. Many people
also showed concern about the level of deforestation and
its implications for the future. Almost all informants said
that they had noticed environmental problems affecting
their lives and pointed to deforestation as the main cause
of problems such as landslides, soil erosion, changes in the
local climate and the disappearance of wildlife. The migrant
populations in the area do not generally consume primate
meat but opportunely hunt 0. flavicauda with the inten-
tion of selling young animals as pets: in fact 8% of inter-
viewees targeted primates whilst hunting, but only in the
indigenous community of Shimbayacu did respondents say
that primates were hunted for meat. Unfortunately no pre-
cise data could be collected on the percentage of primate
off-take rates represented by 0. flavicauda, as hunting was
opportunistic and hunters indiscriminate in their choice
of species. During the period of this study we collected in-
cidental data on illegal trade in 0. flavicauda. We found
two recently caught 0. flavicauda for sale and heard reports
of several more. Prices ranged from 30-250 soles (about
10-70 US dollars).

Discussion

Determining population sizes and distributions for a
species such as the yellow-tailed woolly monkey is made
harder by its fragmented distribution, occurrence in moun-
tainous terrain and by the fact that it has never been the
subject of a full census. Nowak's (1999) estimate of less
than 250 individuals was probably too low; however, we
must conclude that the true population size will not now
be much higher than this, with a continuing downward


trend. The species' large body size, low reproductive rate
and the need for large home ranges, as suggested by their
low densities (Leo Luna, 1987; DeLuycker, 2007), makes
it especially vulnerable to anthropogenic hunting pressures,
and habitat destruction and its fragmented distribution will
reduce the effective population size far below that of a single
contiguous population (Purvis et al., 2000). Therefore the
largest, most secure, individual population should be used
to determine the species' level of endangerment. We wit-
nessed large areas within the boundaries of the Alto Mayo
Protected Forest being cleared for agriculture and cattle
ranching and new areas are being settled constantly. How-
ever, group sizes reported by DeLuycker (2007) within the
boundaries of the Protected Forest are appreciably greater
then those found during this study and in previous studies
(Leo Luna, 1980; Parker and Barkley, 1981; Butchart et
al., 1995b), all of which were outside protected areas. This
could possibly be due to relatively lower hunting pressures
within the reserve.

We conclude that the main threats to this species con-
tinue to be land clearance and habitat degradation, and,
contrary to recent reports (EDGE, 2007), hunting by
both indigenous and immigrant communities for subsis-
tence and trade is also a major threat to the survival of the
species. Trade in 0. flavicauda seems to be of a very local
nature, but even such small levels of trade in a species as
endangered as this could be disastrous. Leo Luna (1987)
estimates that 600 individuals were killed by opportunis-
tic hunters over a 10-year period, and our experience leads
us to believe that similar numbers are being hunted today.
During this study at least three infants were removed
from the population, and presumably their mothers were
killed in the process. Previous recommendations for the
conservation of this species have concentrated on habitat
protection and public awareness to reduce hunting pres-
sure (Mittermeier et al., 1975; Graves and O'Neil, 1980;
Leo Luna, 1980, 1982; Parker and Barkley, 1981; Rios
and Ponce del Prado, 1989; DeLuycker, 2007). Much has
been achieved in recent years, and currently there are sev-
eral projects in place for the conservation of this and other
endemic species in the area for example, the communi-
ty-based conservation project in the Los Chilchos valley,
supported by Apenheul Primate Conservation Trust,
IUCN Netherlands and the RABO Foundation, and also
the ecosystem protection initiatives of Asociaci6n Eco-
sistemas Andinos (ECOAN) and the Asociaci6n Peruana
para la Conservaci6n de la Naturaleza (APECO). We
recommend urgent conservation efforts throughout the
distribution of 0. flavicauda, concentrating on habitat
protection. To best achieve this we feel that work should
take place on four different levels: 1) increased protection
and connectivity between protected areas, 2) better en-
forcement of conservation laws, 3) coordinated local and
regional scale education and public awareness programs,
and 4) investment in development of alternative income
sources for rural populations.





Neotropical Primates 14(3), December 2007


Acknowledgements

For the funding we thank Aap, International Primate Pro-
tection League and the Monkey Sanctuary Trust. Thanks
to our amazing field assistant Fernando Guerra, and
to Carlos and Helen Palomino of IKAMA Peru, Karen
Bendezd Aguilar, Rolando Aquino, Anneke DeLuycker,
Mariella Leo and APECO, Willy Palomino and ECOAN,
Fanny Cornejo, Jan Vermeer, Hans Dignum, Liz Cooke,
Liz Tyson, Noam Shany, Lily Rodriguez, Arnon Datner,
Thomas R. Defler and Mika R. Peck for their contribu-
tions to this work. We also thank the Gobierno Regional
de San Martin, Ministerio de Agricultura, PROCRELL,
PETT, IIAP and INRENA. Finally we thank the villages of
Colca, Pitoja, Shimbayacu, San Pedro, La Esperanza, Perla
de Limasa, Santa Rosa, Shipasbamba and Yambrasbamba,
and of course the yellow-tailed woolly monkeys.

Sam Shanee, Noga Shanee, Neotropical Primate Con-
servation, 36D Brondesbury Villas, London, UK, e-mail:
and Angela M. Maldonado,
Fundaci6n Entropika, Leticia, Colombia and School of
Social Sciences and Law, Department of Anr-...p..1..;_,,
Oxford Brookes University, Oxford, UK.

References

Butchart, S.H.M., Barnes, R., Davies, C.W.N., Fernan-
dez, M. and Seddon, N. 1995a. Observations of two
threatened primates in the Peruvian Andes. Primate Con-
serv. (16): 15-19.
Butchart, S.H.M., Barnes, R., Davies, C.W.N., Fernan-
dez, M. and Seddon, N. 1995b. Threatened mammals of
the Cordillera de Colin, Peru. Oryx 29: 275-281.
DeLuycker, A. 2007. Notes on the yellow-tailed woolly
monkey (Oreonax flavicauda) and its status in the pro-
tected forest of Alto Mayo, northern Peru. Primate Con-
serv. (22): 41-47.
EDGE. 2007. Evolutionarily Distinct and Globally En-
dangered (EDGE), London. Website: edgeofexistence.org/species/species_info.asp?id=79>. Ac-
cessed 1 August 2007.
Graves, G.R. and O'Neill, J.P. 1980. Notes on the yel-
low-tailed woolly monkey (Lagothrixflavicauda) of Peru.
J. Mammal. 61: 345-347.
Humboldt, A. and Bonpland, A. 1812. Recueil d'Obser-
vations de Zoologie et d'Anatomie Comparde faites dans
l'Odcan Atlantiques, dans l'Intrieur du Nouveau Continent
et dans la Mer du Sud. 1. F Schoell and G. Dufour and
Co., Paris.
Institute Nacional de Estadistica e Informitica (INEI).
2006. Website: . Accessed
1 August 2007.
IUCN. 2006. Red list of threatened Species. International
Union for the Conservation of Nature (IUCN). Website:
. Accessed 1 August 2007.
Leo Luna, M. 1980. First field study of the yellow-tailed
woolly monkey. Oryx 15: 386-389.


Leo Luna, M. 1982. Estudio preliminary sobre la biologia y
ecol6gica del mono choro de cola amarilla Lagothrixfla-
vicauda (Humboldt, 1812). Tesis, Universidad Nacional
Agraria La Molina, Lima.
Leo Luna, M. 1987. Primate conservation in Peru: A case
study of the yellow-tailed woolly monkey. Primate Con-
serv. (8): 122-123.
Leo Luna, M. 1989. Biologia y conservaci6n del mono
choro de cola amarilla (Lagothrix flavicauda), especie en
peligro de extinci6n. In: La Primatologia en Latinoam-
drica, C.J. Saavedra, R.A. Mittermeier and I.B. Santos
(eds.), pp.23-30. World Wildlife Fund-US, Washing-
ton, DC.
Macedo Ruiz, H. de and Mittermeier, R.A. 1979. Redes-
cubrimiento de primate peruano Lagothrix flavicauda
(Humboldt 1812) y primeras observaciones sobre su
biologia. Rev. Cienc. Universidad Nacional Mayor San
Marcos 71: 78-92.
Mittermeier, R.A., Macedo Ruiz, H. de and Luscombe, A.
1975. A woolly monkey rediscovered in Peru. Oryx. 13:
41-46.
Mittermeier, R. A., Ratsimbazafy, J., Rylands, A. B., Wil-
liamson, E., Oates, J. F, Mbora, D., Ganzhorn, J. U.,
Rodriguez-Luna, E., Palacios, E., Heymann, E. W.,
Kierulff, M. C. M., Long Yongcheng, Supriatna, J.,
Roos, C., Walker, S. and Aguiar, J. M. 2007. Primates
in Peril: The World's 25 Most Endangered Primates
2006-2008. Unpublished report, IUCN/SSC Primate
Specialist Group (PSG), International Primatological
Society (IPS), and Conservation International (CI), Ar-
lington, VA.
Myers, N., Mittermeier, R.A., Mittermeier, C. G., Fonseca,
G.A.B. da and Kent, J. 2000. Biodiversity hotspots for
conservation priorities. Nature 403: 853-858.
Nowak, R.M. 1999. Mammals of the World. 6th
Ed. The Johns Hopkins University Press, Baltimore.
Parker, T.A. and Barkley, L.J. 1981. New locality for the
yellow-tailed woolly monkey. Oryx 26: 71-72.
Parks Watch Peru. 2003. Perfil Area Protegida-Perd
Bosque de Protecci6n Alto Mayo. Website: parkswatch.org>. Accessed 1 August 2007.
Purvis, A., Gittleman, J. L., Cowlishaw, G. and Mace,
G.M. 2000. Predicting extinction risk in declining spe-
cies. Proc. R. Soc. Lond. 267: 1947-1952.
Rios, M. and Ponce del Prado, C. E 1989. El status de las
dreas de conservaci6n propuestas para choro de cola ama-
rilla (Lagothrix flavicauda): Una investigaci6n sobre la
planificaci6n regional de dreas naturales protegidas. En:
La Primatologia en Latinoamerica, C.J. Saavedra, R.A.
Mittermeier and I. B. Santos (eds.), pp.31-65. World
Wildlife Fund-US, Washington, DC.
Shanee, N., Shanee, S. and Maldonado, A. M. 2007. Inter-
specific association between Oreonax and Ateles, Amazo-
nas, Peru. Neotrop. Primates 14(1): 34-35.





Neotropical Primates 14(3), December 2007


GRANDMATERNAL INFANT CARRYING IN
WILD NORTHERN MURIQUIS (BRACHYTELES
HYPOXANTHUS)

Maira de Lourenfo Assundao
Sergio L. Mendes
Karen B. Strier

Introduction

Opportunities for grandmothers and other older matrilin-
eal kin to invest in their grandchildren or younger mater-
nal relatives are affected by whether females remain and
reproduce in their natal groups. They may also be mediated
by the trade-offs between investing in their own offspring
versus those of their relatives. Indeed, the evolution of post-
reproductive life spans in human females has been attribut-
ed to the fitness benefits that older matrilineal kin may gain
by investing in their relatives' offspring instead of their own
(Hrdy, 1981; Hawkes et al., 1998). Some types of alloma-
ternal investment, such as agonistic support or babysitting,
can be provided irrespective of the female's own reproduc-
tive condition, while other types, such as infant carrying
during travel or feeding, may be more limited if the female
is already carrying an infant of her own (Paul, 2005). In
Hanuman langurs (Semnopithecus entellus), experienced
females with weaning infants or no infants accounted for
roughly 10% of all allomothering attempts (Hrdy, 1977:
210), and in Japanese macaques (Macacafuscata), the sur-
vivorship of infants to 12 months was significantly higher
if their post-reproductive grandmothers were present than
if their grandmothers were still reproducing or no longer
alive (Pavelka et al., 2002). In captive vervet monkeys
(Chlorocebus aethiops), grandmothers without infants had
significantly higher rates of caring for grandchildren than
grandmothers with infants (Fairbanks, 1988: 437).

Northern muriquis (Brachyteles .'i;.... .-.'... i live in patri-
focal societies in which allomaternal care of any type is rare
(Odalia-Rimoli, 1998; Guimaraes and Strier, 2001; Mar-
tins et al., 2007). Grandmothers rarely have opportunities
to interact with maternal grandchildren because daughters
typically disperse from their natal groups prior to the onset
of puberty (Printes and Strier, 1999; Strier and Ziegler,
2000). The only previous known muriqui grandmother
of two daughters that reproduced in their natal group was
caring for her own infants when her grandchildren were
born, and was never observed to carry them. In this paper,
we present data on infant-carrying by a second grandmoth-
er that did not have her own infant at the time.

Methods

The study was conducted at the Reserva Particular do
Patrim6nio Natural-Feliciano Miguel Abdala (RPPN-
FMA) in Caratinga, Minas Gerais, Brazil. The 957-ha
forest supports four groups of northern muriquis, and has


been described in detail elsewhere (Strier et al., 2006). We
focus on two adult females in the Matao group, which had
81 members during this study period: DD, a grandmother
who was carrying an infant when long-term monitoring
on this group was initiated in 1982, and is therefore esti-
mated to have been at least 30 years old during the pres-
ent study; and her daughter, DB, who was born in 1996
and was the third of three natal females (out of 38 natal
females that have survived to dispersal age) to remain and
reproduce in this group (Martins and Strier, 2004; Strier et
al., 2006). DB's first infant, a son, DN, was born in early
June 2005.

On 2 September 2005, DD was first seen traveling with
her three-month-old grandson (DN) on her back. DD was
observed carrying DN on subsequent occasions in 2005.
From January to July 2006, instantaneous scan samples
(Altmann, 1974) were conducted at 15-minute intervals
on all females visible, to assess the proportion of time that
DD carried her grandson relative to the proportion of time
that he was carried by his mother. At the onset of each
scan sample, the females' activities (e.g., resting, traveling,
feeding, socializing, drinking water, and undetermined)
and all individuals within a five-meter radius were recorded
(Strier, 1987). DD and DB were the only females observed
carrying DN (i.e., both transporting him while active and
resting in contact with him). We calculated the monthly
proportion of scan samples in which either DD or DB
was carrying or in contact with DN, and in which DB was
among her mother's nearest neighbors when DD was car-
rying or in contact with her grandson. We also examined
whether the monthly distribution of both females' activities
differed when they were carrying versus not carrying DN.
We present descriptive statistics without analyses because
of our small sample sizes.

Results

One or both females were observed in 332 of the 2,162 scan
samples conducted during the present study period. This
resulted in a total of 171 observations of DD (median = 23,
range = 6-46, n= 7 months), and 184 observations of DB
(median = 23, range = 7-73, n = 7 months). The percentage
of monthly observations in which DD was seen carrying
her grandson ranged from 0-60.8% (median= 31.1%,
n= 7 months), while those in which DB was carrying her
son ranged from 4.4-62.5% (median = 12.5%). From
April through July, DD carried DN proportionately more
often than DB (Fig. 1). DD was rarely in proximity to her
daughter during the study period. On average, DB was
among her mother's nearest neighbors in 14.4 11.8%
of the scan samples when DD was carrying her grandson
(median= 18.2%, range: 0-25.0%; n= 6 months) and
in 9.6 7.7% of the scan samples in which DD was not
carrying him (median = 11.1%, range= 0-17.6%, n= 7
months). Both females exhibited similar activity patterns
whether or not they were carrying or in contact with DN.
DD was twice as likely to be feeding when not carrying her





Neotropical Primates 14(3), December 2007


grandson, and DB was seven times more likely to be feed-
ing when not carrying her son (Fig. 2).

Discussion

We do not know why DD began carrying her grandson in
the first place, or why her care of DN increased during the
last four months of the study period. However, neither of
the other two females (maternal sisters) that have repro-
duced in their natal group received any help with carry-
ing from their mother-who, unlike DD, was caring for
her own infants when her grandchildren were born. DD's
interest in or ability to carry her grandson may have been
possible because she was not encumbered with an infant of
her own. Based on her reproductive history and the aver-
age three-year birth interval (Strier et al., 2006), DD was
expected to have conceived during the 2005-06 mating
season. Although her last observed copulation was on 2 De-
cember 2005, she did not subsequently give birth. Muriqu-
is do not exhibit visible signs of early pregnancy, and the
cessation of cycling and mating during the mating season is
usually indicative of conception (Strier and Ziegler, 1997,
2005). We do not know, however, whether DD's pregnan-
cy failed, or whether she failed to conceive at all this year.
Seven years earlier, during the 1998-1999 mating season,


70
60- %DD


40 -
30


Figure 1. Grandmaternal versus maternal infant-carrying and
contact. Percentages are based on scan samples in which DD and
DB were carrying or in contact with DN.


80- Rest
70_ Travel
Sso


50


10

ODDwith DDw/o DBwilh DBwVo
Female with and without (wlo) DN

Figure 2. Distribution of DD's and DB's main activities relative
to their contact with or without DN. Resting with DN involved
physical contact; traveling and feeding with DN involved carry-
ing him.


DD also cycled and copulated, but did not subsequently
give birth. Her much lower cycling estradiol levels and
higher corresponding androgen levels relative to other fe-
males that conceived that year were hypothesized to have
contributed to her reproductive failure (Strier and Ziegler,
2005). Although she has reproduced in the intervening
years, it is possible that during the present study, she ex-
perienced similar conception difficulties to those when she
was seven years younger.

Although DD and DB were rarely in close proximity, DB
was more likely to be among DD's nearest neighbors when
DD was carrying her grandson than when she was not. We
do not know whether DD initiated proximity with DB to
gain access to her grandson, or whether DB initiated prox-
imity with DD to solicit her help or to monitor her while
she was carrying DN. Both DD and DB were less likely to
feed when they were carrying DN than when they were not.
It is tempting to infer that by carrying her grandson, DD
liberated her daughter to feed unencumbered, but muriqui
mothers often "park" their infants in the canopies of the
trees in which they are feeding (Strier, 1999, p. 84). If DN
was parked nearby when either his mother or grandmother
were feeding, neither was scored as carrying him.

Extended allomaternal care by northern muriquis has pre-
viously been observed on only one other occasion during
our long-term monitoring of this group, and curiously, the
same female (DD) was also involved. On that occasion,
DD carried her own and another female's similarly aged
infant for 11 2 days before relinquishing one of the infants
to the other mother. In the process, however, the infants
were exchanged, and both mothers successfully weaned and
reared their adopted infants (Martins et al., 2007). In the
present case, however, DD focused her attention exclusive-
ly on her maternal grandson, despite the presence of other
infants in the group at the time. Moreover, none of the
other adult females, including those that were not carrying
infants of their own, were observed carrying or attempting
to carry DN. Although we cannot yet assess whether DD's
care of her grandson will have any direct or indirect fit-
ness benefits, our observations of persistent investment by a
grandmother in her maternal grandson indicate that grand-
maternal care can occur within a patrilocal society when a
daughter atypically reproduces in her natal group and the
grandmother is not carrying an infant of her own.

Acknowledgements

We thank CNPq and the Abdalla family for permission
to conduct this field research, J. Gomes, C. B. Possamai,
and F. P. Tabacow for their help during this field study, and
E P. Tabacow for calling our attention to her observation
of DD carrying DN the first time and for her comments
on an earlier version of this manuscript. The research re-
ported here was financed with grants to KBS from the
National Geographic Society, the Margot Marsh Biodi-
versity Foundation, the Liz Claiborne and Art Ortenberg


Jan Feb Mar Apr
Month


May Jun Jul





Neotropical Primates 14(3), December 2007


Foundation, and the Graduate School of the University of
Wisconsin-Madison. The Sociedade para a Preservacao do
Muriqui and CI-Brasil provided additional support. We
thank E. M. Veado, J. Gomes, F. Mendes, J. Rimoli, A. 0.
Rimoli, F. Neri, P. Coutinho, A. Carvalho, L. Oliveira,
C. Nogueira, S. Neto, W. Teixeira, R. Printes, M. Maciel,
C. Costa, A. Oliva, L. Dib, D. Carvalho, N. Bejar, L.G.
Dias, W. P. Martins, V. O0. Guimaraes, J. C. da Silva, C. B.
Possamai, R. C. Romanini, E. P. Paim, M. F. lurck, K. To-
lentino, V. Souza, J. Fidelis, D. Guedes, and F. P. Tabacow
for their contributions to the long-term demographic data
on the Matao group. We also thank Sarah Hrdy and Paul
Garber for their comments on an earlier version of this
manuscript.

Maira de Lourenco Assungio, Pontificia Universidade
Cat61lica de Minas Gerais-Betim, R. do Rosirio, 1.081
Bairro Angola-Betim, MG, Brazil, e-mail: hotmail.com>, Sergio L. Mendes, Departamento de Ci-
encias Biol6gicas, Universidade Federal do Espirito Santo,
Av. Mal. Campos, 1468, Vit6ria, ES, Brazil, e-mail:
and Karen B. Strier, Depart-
ment of An-i r..p. .1..;,, University of Wisconsin-Madison,
1180 Observatory Drive, Madison, WI 53706, USA,
e-mail: .

References

Altmann, J. 1974. Observational study of behavior: Sam-
pling methods. Behaviour 49: 227-267.
Fairbanks, L.A. 1988. Vervet monkey grandmothers: In-
teractions with infant grandoffspring. Int. J Primatol. 9:
425-441.
Guimaraes, V. 0. and Strier, K. B. 2001. Adult male-infant
interactions in wild muriquis (Brachyteles arachnoides hy-
poxanthus). Primates 42: 395-399.
Hawkes, K., O'Connell, J. F., Blurton-Jones, N. G., Alvar-
ez, H. and Charnov, E. L. 1998. Grandmothering, meno-
pause, and the evolution of human life histories. Proc.
Natl. Acad. Sci. USA 95: 1336-1339.
Hrdy, S.B. 1977. The Langurs of Abu: Female and Male
Strategies of Reproduction. Harvard University Press,
Cambridge, MA.
Hrdy, S.B. 1981. The Woman That Never Evolved. Harvard
University Press, Cambridge, MA.
Martins, W. P. and Strier, K. B. 2004. Age at first reproduc-
tion in philopatric female muriquis (Brachyteles arach-
noides '..' -'.. Primates 45: 63-67.
Martins, W.P., Guimaraes, V.O. and Strier, K.B. 2007.
Infant swapping in northern muriquis (Brachyteles hypo-
xanthus). Primates 48(4): 324-326.
Odalia-Rimoli, A. 1998. Desenvolvimento comporta-
mental do muriqui (Brachyteles arachnoides) na Estagao
Biol6gica de Caratinga, Minas Gerais. Tese de Doutora-
mento, Universidade de Sao Paulo, Sao Paulo, Brasil.
Paul, A. 2005. Primate predispositions for human grandma-
ternal behavior. In: Grandmotherhood: The Evolutionary
Significance of the Second Half of Female Life, E. Voland,


A. Chasiotis and W. Schiefenhovel (eds.), pp.21-37. Rut-
gers University Press, New Brunswick, New Jersey.
Pavelka, M.S.M., Fedigan, L.M. and Zohar, S. 2002.
Availability and adaptive value of reproductive and
postreproductive Japanese macaque mothers and grand-
mothers. Anim. Behav. 64: 407-414.
Printes, R.C. and Strier, K.B. 1999. Behavioral correlates
of dispersal in female muriquis (Brachyteles arachnoides).
Int. J. Primatol. 20: 941-960.
Strier, K. B. 1987. Activity budgets of woolly spider mon-
keys, or muriquis. Am. J. Primatol. 13: 385-395.
Strier, K.B. 1999. Faces in the Forest: The Endangered
Muriqui Monkeys of Brazil. Harvard University Press,
Cambridge, MA.
Strier, K.B. and Ziegler, T.E. 1997. Behavioral and en-
docrine characteristics of the reproductive cycle in wild
muriqui monkeys, Brachyteles arachnoides. Am. J Prima-
tol. 42: 299-310.
Strier, K. B. and Ziegler, T. E. 2000. Lack of pubertal influ-
ences on female dispersal in muriqui monkeys, Brachyte-
les arachnoides. Anim. Behav. 59: 849-860.
Strier, K.B. and Ziegler, T.E. 2005. Variation in the re-
sumption of cycling and conception by fecal andro-
gen and estradiol levels in female northern muriquis
(Brachyteles ',.. .-'. Am. J Primatol. 67: 69-81.
Strier, K. B., Boubli, J. P., Possamai, C. B. and Mendes, S. L.
2006. Population demography of Northern muriquis
(Brachyteles I'i,.. -..' at the Estagao Biol6gica de
Caratinga / Reserva Particular do Patrim6nio Natural
Feliciano Miguel Abdala, Minas Gerais, Brazil. Am. J
Phys. Anthropol. 130: 227-237.


CARACTERIZACI6N DE LA POBLACI6N DEL
MONO AULLADOR (ALOUATTA PALLIATA PALLIATA)
EN EL REFUGIO NATIONAL DE VIDA SILVESTRE
ISLA SAN LUCAS, COSTA RICA

Marta Marleny Rosales-Meda

Introducci6n

Los studios realizados con monos aulladores en sitos con
aislamiento geogrifico se han desarrollado principalmente
en las islas de Barro Colorado (Milton 1990), Orquidea
(Froehlich y Thorington, 1982, 1992) y Coiba (Milton y
Mittermeier, 1977) en Panami, donde predomina la ve-
getaci6n de bosque tropical. Dichos studios han sido de
utilidad para conocer la ecologia y comportamiento de los
aulladores en estos habitats. Hasta la fecha no existe infor-
maci6n acerca del estado de estos primates en ambientes
aislados geogrificamente, estacionales y reducidos. Este es
el caso del Refugio Nacional deVida Silvestre Isla San Lucas
(RNVSISL) en Costa Rica, en donde habitat una poblaci6n
introducida de monos aulladores (Alouattapalliatapalliata)
desde hace 40 afios (Costa Rica, MINAE, 2005). Se ha re-
portado que dicha especie juega un papel determinante en
la regeneraci6n y restauraci6n de habitats, principalmente





Neotropical Primates 14(3), December 2007


en bosques secos del pals (Howe, 1980; Morera, 1996), lo
cual podria ser el caso del RNVSISL, donde en los 61timos
30 afios la cobertura del bosque caducifolio ha aumentado
en un 55% (Castro y Carvajal, 2006). Por otro lado, en la
actualidad, las poblaciones de monos aulladores estin con-
sideradas en peligro de extinci6n para Costa Rica (UICN-
ORMA-WWF, 1999) y su studio en ambientes aislados
geograficamente es important para formular e implemen-
tar acciones de manejo que puedan mejorar la viabilidad
de dicha especie. La present investigaci6n constitute el
primer aporte para conocer el estado de los monos aullado-
res en el RNVSISL y tuvo como objetivos: 1) caracterizar
la poblaci6n existente (composici6n por sexo-edad y carac-
teristicas particulares) y 2) identificar algunos de los Arboles
utilizados como alimento y descanso en 6poca seca.

MWtodos

Area de studio
El RNVSISL se ubica en el golfo de Nicoya, al occi-
dente de Costa Rica, entire las coordenadas 09057'N y
8454'0. Su extension es de 462 ha y la altitude varia entire
los 0 y 220 m.s.n.m. Segdn Bolafos y Wattson (1993) la
isla se encuentra dentro de la zona de vida Bosque Seco
Tropical y present dos estaciones definidas: lluviosa
(mayo-noviembre) y seca (diciembre-abril). La precipita-
ci6n media annual es de 1,600 mm y la temperature media
es de 27C. La isla se encuentra a 800 metros al oeste de
la peninsula de Nicoya y a 7 km al este de la provincia de
Puntarenas (Costa Rica, MINAE, 2005). Para el afo 2006,
la isla contaba con 366 ha de bosque caducifolio en suce-
si6n, 46.89 ha de bosque siempre verde, 6.9 ha de manglar
y 6.8 ha de pastos arbolados (Castro y Carvajal, 2006). En
1873 el gobierno de Costa Rica declar6 la creaci6n de un
centro penitencial en la Isla San Lucas, con lo cual se da la
introducci6n de species ex6ticas de fauna y flora al drea,
asi como la degradaci6n de la vegetaci6n existente a causa
de actividades ganadera y agricola. En 1967 se introdujeron
en la isla algunas species de fauna silvestre, entire ellas los
monos aulladores, pero se carece de informaci6n acerca de
la cantidad de individuos y su origen. En 1991 se clausur6
el centro penitencial y empez6 un process de regeneraci6n
vegetal principalmente del bosque caducifolio, ya que hasta
entonces predominaban las areas de pasturas. En 2001 la
isla fue declarada Refugio Nacional de Vida Silvestre por
el Ministerio de Ambiente y Energia y desde entonces ha
sufrido poca intervenci6n humana. En la actualidad es visi-
tada por pobladores de areas aledafas con fines recreativos,
principalmente en las playas, pero tambidn se han regis-
trado pesca y caceria furtiva (Costa Rica, MINAE, 2005;
obs. pers.).

Caracterizacidn del mono aullador
El registro de la poblaci6n de monos aulladores existente en
el RNVSISL se realize mediante recorridos en la manana
(05:00-10:00 hr) y tarde (15:00-17:30 hr) durante 10 dias,
en 6poca seca (18 al 27 de abril de 2006). Se visitaron al
menos dos veces todos los remanentes de bosque siempre


verde donde podian habitar los monos, y tambidn se reali-
zaron recorridos en los otros tipos de cobertura vegetal. Los
monos fueron observados con binoculars por un minimo
de 40 minutes, con el fin de determinar el sexo (macho
o hembra, mediante la presencia o ausencia de escroto de
color blanco a partir de la etapa sub-adulta; Neville et al.,
1988) y edad de los integrantes de la tropa. La edad se di-
ferenci6 en adulto (individuo grande e independiente), ju-
venil (individuo que se mueve independientemente de su
madre, de tamafo medio, muy activo), infante (individuo
pequefo que se agarra del pelaje dorsal de la madre, de-
pende de ella pero se separa frecuentemente para jugar o
explorer por poco tiempo) y cria (individuo pequefo que se
agarra del pelaje dorsal o ventral de la madre, es totalmente
dependiente de ella y se separa esporidicamente para ex-
plorar). Se identificaron caracteristicas particulares de cada
individuo cicatricess y coloraci6n del pelaje) y algunas espe-
cies de arboles utilizadas para alimento y descanso durante
el tiempo de observaci6n. La ubicaci6n de las tropas fue
registrada en un mapa con la ayuda de un GPS. Se uti-
liz6 estadistica descriptive para el anAlisis de la composi-
ci6n de tropas existentes y su organizaci6n social machoss
adults / hembras adults y hembras-inmaduros).

Resultados

Durante 75 h de esfuerzo de b6squeda y observaci6n se
detect un total de 112 individuos distribuidos en nueve
tropas y un macho adulto solitario. Las tropas estuvieron
compuestas por 31 machos adults (28%), 38 hembras
adults (34%), 21 juveniles (19%), seis infants (5%) y
15 crias (14%) (Tabla 1). La media del tamafo de tropas
fue de 12.33 + 6.5 y la median fue de 11, con un intervalo
de 3 a 23 individuos. La tasa sexual promedio en adults
fue de 1.48 + 1.03 hembras por macho, mientras que las
proporciones de inmaduros infantss + crias) por hembra
y de crias por hembra fueron de 0.53 0.43 y 0.36 0.17
respectivamente. Todos los individuos fueron detectados en
remanentes de bosque siempre verde (Fig. 1), en Arboles de
20 m o mris de altura. La densidad estimada de monos au-
lladores en el RNVSISL fue de 0.24 ind/ha y en el bosque
siempre verde en 6poca seca fue de 2.29 ind/ha. Los Arboles
utilizados como alimento fueron Mangifera indica y Spon-
dias purpurea (fruto); Cassia grandis, Bursera simarouba,
Ficus benjamin, Anacardium excelsum, Pseudobombax sep-
tenatum, Albizia saman, Tamarindus indica, Acacia centralis,
Desmopsis bibracteata, Melicoccus .._ .-.. Maytenus sego-
viarum (hojas). Frecuentemente se les observ6 descansan-
do en Arboles de Bombacopsis quinata, Sideroxylon capiri,
Enterolobium cyclocarpum, CdllycvIopl/'y// candidissimun y
Lonchocarpus spp.

Nueve por ciento (n= 10) de los individuos observados
presentaron una despigmentaci6n (mancha blanca) en el
pelaje, la cual variaba en tamafo y forma entire los dife-
rentes individuos, pudiendo ser continue o discontinue,
y se observ6 principalmente en las extremidades y cola de
adults y juveniles (Tabla 1 y Fig. 2). Las observaciones






Neotropical Primates 14(3), December 2007


"T1 S Tropas de A. palliata

T9 TBosque siempreverde


L" Bosque caducifolio
en sucesi6n
T6
PN oyecci6nicdca vonform

Datum Ocompequc Cona Rica
Fuenic: Fowgmlaa CARTA 2M
Intepretaci4:6 J. Castro y J. Camsial
435500 436000 436500 437000 437500 438000 438500
0 0.5 1 Kil6metros


Figura 1. Distribuci6n geogrifica de las tropas (n= 9) y de un macho adulto solitario (IS) de Alouattapalliatapalliata en el Refugio Na-
cional de Vida Silvestre Isla San Lucas, Costa Rica.


Tabla 1. Composici6n de las tropas del mono aullador, Alouattapalliatapalliata, en el Refugio Nacional de Vida Silvestre Isla San Lucas,
Costa Rica. MA = macho adulto, HA= hembra adulta, J= juvenile, I= infante, C= cria.

No. Tropa MA HA J I C Total Individuos con manchas Lugar
1 1 4 0 0 2 7 0 Administraci6n
2 4 5 2 0 1 12 0 Hacienda Vieja
3 2 3 5 0 1 11 2 BellaVista
4 4 3 3 0 1 11 1 Administraci6n
5 3 6 1 1 2 13 1 El Ingles
6 7 6 5 1 3 22 0 Limoncito
7 6 8 3 2 4 23 4 Cirialito
8 3 2 1 2 1 9 0 El Coco
9 1 1 1 0 0 3 1 Tumbabote
Total tropas 31 38 21 6 15 111 9
Mediana 3 4 2 0 1 11
Media 3.44 4.22 2.33 0.67 1.67 12.33
Desv.Est. 2.07 2.22 1.80 0.87 1.22 6.50
Ind. solos 1 1 1 Central
Total general 32 112 10





Neotropical Primates 14(3), December 2007


particulares de las manchas de cada individuo por tropa se
especifican en la Tabla 2.

Discusi6n

El intervalo del tamano de tropas detectado en el present
studio se encuentra entire el rango reportado para la Isla
de Barro Colorado (IBC, 3-45 individuos: Milton, 1990)
y la isla Coiba (2-9 individuos: Milton y Mittermeier,
1977) en Panami, asi como para el bosque seco estacional
del Parque Nacional Santa Rosa (PNSR, 3-40: Fedigan et
al., 1985) y la finca La Toboga (3-39: Heltne et al., 1975)
en Costa Rica. El tamano medio de tropas observado en
el RNVSISL es similar al reportado para la finca La Paci-
fica, en Guanacaste (11.9 individuos: Heltne et al., 1975;
17 individuos: Glander, 1980) y mais alto que el reportado
en la isla Coiba (5 individuos: Milton y Mittermeier, 1977).
Si se excluye del analisis a la tropa incipiente (No.9), el
tamano medio de tropas (13.50+ 5.86) es un valor cercano
al reportado para el bosque seco estacional (14 individuos:
Fedigan, 1986), pero mas bajo que el reportado para la IBC
(19 individuos: Milton, 1990). Se desconoce el tiempo de
formaci6n de cada tropa en el RNVSISL. No obstante, el
mismo podria afectar su tamano, y es possible que las tropas
mais antiguas sean las mayores.

La cantidad media de machos, hembras e inmaduros es
congruente con lo reportado para la especie (Neville et al.,
1988), cercana a los valores reportados para el bosque seco
en el PNSR (Fedigan et al., 1985), La Pacifica y La Toboga
(Neville etal., 1988) y relativamente menor a los reportados
en el bosque tropical de la IBC en 1980 (Milton, 1990).
Asi, el tamano, composici6n y patron de distribuci6n de las
tropas observado en los bosques siempre verdes del RNV-
SISL no difiere de los valores reportados en otros habitats
y probablemente s6lo depend de la abundancia, calidad y
disponibilidad de recursos (Milton, 1990). Como se espe-
raba, se observ6 que las tropas mais grandes (de 22 y 23 in-
dividuos) habitaban en los remanentes de bosque mas gran-
des y antiguos (7.5 y 5.85 ha respectivamente) mientras que
la tropa mais pequefia (tres individuos) se observ6 en uno de


los remanentes mais pequenos y j6venes (3.16 ha). Es posi-
ble que esto refleje una mejor adaptaci6n de los aulladores
en el RNVSISL, debido a la disponibilidad de alimento
de mejor calidad y con menor cantidad de compuestos
secundarios vegetables t6xicos (Milton, 1979). Durante el
muestreo, se observ6 cualitativamente una tendencia a un
mayor tamano corporal de los monos adults en uno de los
remanentes mais antiguos (tropa No. 6) y de individuos con
menor tamano corporal en remanentes de bosque mis re-
cientes (tropas No. 4 y 9), lo cual podria apoyar la hip6tesis
de que los aulladores alcanzan mayor tamano y peso corpo-
ral en lugares donde tienen acceso a bosque mais maduro y
divers (Froehlich y Thorington, 1990). Esto fue descrito
anteriormente para la IBC y la isla aledana Orquidea, la
cual posee un airea menor (16 ha) y cuenta con recursos
alimenticios limitados ya que su tiempo de regeneraci6n
vegetal es menor al de la IBC (Froehlich y Thorington,
1982, 1990). No obstante, para verificar si esta tendencia se
present en el RSVSISL, es necesario realizar studios que
proporcionen informaci6n sobre mediciones corporales de
los individuos y su relaci6n con la abundancia y diversidad
de alimento.


Figura 2. Macho adulto Alouattaipalliatapalliata con despigmen-
taci6n en el pelaje de la cola y de la pata derecha. (Foto por M. M.
Rosales-Meda.)


Tabla 2. Descripci6n de las manchas de color blanco en piel o pelaje observadas en individuos de las tropas de monos aulladores que
habitan en el Refugio Nacional de Vida Silvestre Isla San Lucas, Costa Rica.
No. Tropa Observaciones
3 Un macho adulto con manchas de color blanco en el pelo de ambas patas traseras y en la parte inferior de la cola (en forma de
anillo). Un juvenile con manchas de color blanco en la parte inferior de la cola (en forma de anillo).
4 Un macho adulto con parte inferior de la cola de color blanco.
5 Un macho adulto con la punta de la cola de color blanco.
7 Un macho adulto y un juvenile con manchas de color blanco en parte del pelo y piel de la pata trasera izquierda. Un macho
adulto con manchas de color blanco en la piel de la pata delantera izquierda. Un juvenile con manchas de color blanco en el pelo
de ambas patas traseras.
9 Una hembra adulta con pelo y piel de la pata trasera izquierda y parte inferior de la cola (s6lo de un lado) de color blanco.
La coloraci6n blanca de la piel de la pata es discontinue.
Ind. solo Macho adulto con parte del pelo y piel de la pata trasera derecha y parte de la cola (en forma de anillo) de color blanco.
La coloraci6n blanca del pelo de la pata es discontinue.





Neotropical Primates 14(3), December 2007


La densidad de aulladores en el RNVSISL, concentrada
principalmente en la reducida cobertura de bosque siem-
pre verde, y la proporci6n media de inmaduros por hembra
indican que la poblaci6n podria tener un crecimiento por
natalidad constant. El ndmero mayor de juveniles que de
infants y crias parece indicar que la supervivencia de los
inmaduros es alta, aunque se deben realizar studios de
monitoreo de la poblaci6n a lo largo del afo para verificar
dicha informaci6n. La baja cantidad de individuos solita-
rios encontrados en el RNVSISL es similar a lo reportado
en otros ambientes aislados geograficamente como la isla
Coiba (s6lo un macho adulto solitario: Milton y Mitter-
meier, 1977) y la IBC (cero individuos solitarios: Froehlich
etal., 1981; Milton, 1990).

Con respect a la despigmentaci6n en el pelaje 6 piel ob-
servada en algunos individuos, no existe hasta la fecha in-
formaci6n documentada acerca de las causes de ello. Esta
despigmentaci6n ha sido tambidn observada en individuos
de A. palliata palliata en otras areas no insulares del pals
como el Pacifico Central (Rosales-Meda, 2007), en Piro,
Peninsula de Osa (Bustamante, com. pers.) y en individuos
de A. palliata mexicana en M6xico (Crist6bal-Azkarate,
2003; Cortes Ortiz, com. pers.). Las posibles causes de la
despigmentaci6n pueden obedecer a alguna o el conjunto
de las siguientes hip6tesis: a) Endogamiay herencia: ya que
la migraci6n de aulladores queda restringida a la isla, es
factible que exista una alta tasa de endogamia en la pobla-
ci6n y que la proporci6n de loci heterozig6ticos sea extre-
madamente baja. Como consecuencia de ello, es possible
que la coloraci6n blanca se deba, a) a alelos recesivos que
estin siendo expresados fenotipicamente en algunos indi-
viduos y se puedan estar transmitiendo de generaci6n en
generaci6n; en la IBC, Froehlich y Thorington (1990) re-
portaron que existe una proporci6n de loci heterocig6ticos
por individuo muy inferior a lo que se consider normal
y dicho fen6meno es mayor en la isla Orquidea, b) caren-
cia de algin requerimiento nutritional esencial o desnu-
trici6n: causado por cambios estacionales en y entire afos
que conduzca a una baja calidad de alimento disponible o
a competencia inter e intra especifica, lo cual puede afec-
tar en mayor grado a los individuos mais d6biles (Milton,
1990; Froehlich et al., 1981) 6 c) carencia de algdn polime-
ro esencial que pueda afectar la producci6n de melanina
en algunos individuos.

Se observ6 el uso frecuente del dosel y arboles emergentes
en el RNVSISL, tal como ha sido reportado por Chapman
(1988) y Neville et al. (1988); la mayor proporci6n de ar-
boles utilizados para alimentarse o descansar tenian una
altura de 20 m o mais. El bosque caducifolio, el manglar y
algunos cables eldctricos antiguos fueron de utilidad para el
desplazamiento de individuos en la isla en la b6squeda de
alimento. Los frutos de Mangifera indica y Spondias pur-
purea fueron consumidos por los aulladores (obs. direct
o en heces), tal como ha sido reportado para la isla Coiba
(Milton y Mittermeier, 1977). Es evidence que dichas espe-
cies son un recurso alimenticio important en 6poca seca,


tanto para los aulladores como para otros mamiferos y aves
que habitan en la isla (obs. pers.).

Recomendaciones para el manejo, conservaci6n y
monitoreo de los monos aulladores en el RNVSISL

A la brevedad possible, es necesario realizar studios gend-
ticos y de salud de los individuos que permitan entender
el origen de la despigmentaci6n en el pelaje o piel, asi
como evaluar la condici6n general actual de la poblaci6n.
Es tambidn important monitorear la proporci6n relative
de las categories de sexo-edad, total de individuos, tasas
de natalidad, mortalidad y sobrevivencia a largo plazo, asi
como m6tricas corporales de los individuos. Dichos aspec-
tos deben ser estudiados en ambas 6pocas del afo, utili-
zindose los mismos criterios de apreciaci6n con respec-
to al sexo-edad y a las caracteristicas particulares de cada
individuo. Por otro lado, la evaluaci6n de la abundancia,
distribuci6n, calidad del alimento y la capacidad de carga
de la isla es esencial para entender aspects relacionados
con la salud de la poblaci6n. Puesto que en RNVSISL se
empieza a promover el turismo, se recomienda que esta
actividad sea regulada para que tenga un impact minimo
en los bosques de la isla; las condiciones de aislamiento y
de possible estr&s ambiental de la poblaciones de monos
aulladores, exige que sean desarrolladas medidas para su
manejo y conservaci6n.

Agradecimientos

Al Servicio de IntercambioAcademicoAlemin (DAAD) por
la beca de studios de postgrado en Costa Rica. Al Instituto
International en Conservaci6n y Manejo de Vida Silvestre
(ICOMVIS) de la Universidad Nacional por el financia-
miento, equipo, transport y demis facilidades brindadas
para la realizaci6n de la "Linea Base de los Componentes
de Flora y Fauna en el RNVSISL", del cuil form parte esta
investigaci6n. A Jos6 Castro por la clasificaci6n de cober-
turas vegetables en la foto Carta 2005, la identificaci6n de
arboles y su compania durante los muestreos. A Aida Bus-
tamante por su colaboraci6n en la identificaci6n de Arbo-
les. Al los funcionarios del MINAE en la isla por su ayuda
brindada durante el trabajo en el campo. A Maria Susana
Hermes por la elaboraci6n del mapa y su compania en los
muestreos. A Jos6 Carvajal por la clasificaci6n de las cober-
turas en la foto area Carta 2005. A Oscar Rangel por su
compania en los muestreos. A Liliana Cortes, Jorge Erwin
L6pez y Karenina Morales por las valiosas sugerencias rea-
lizadas al present manuscrito. Al Smithsonian Tropical
Research Institute, Pedro Mendez y Karenina Morales por
facilitarme literature.

Marta Marleny Rosales-Meda, Instituto Internacional en
Conservaci6n y Manejo de Vida Silvestre, Universidad Na-
cional, Heredia, Costa Rica, Campus Omar Dengo, Apdo.
Postal 1350-3000, e-mail:
y .





Neotropical Primates 14(3), December 2007


Referencias

Bolafos, R. y Wattson, V. 1993. Mapa de Zonas de Vida de
Costa Rica, Hoja San Jose CR2CM-5, Escala 1:200,000.
Centro Cientifico Tropical, San Jose, Costa Rica.
Castro, J. y Carvajal, J. 2006. Cambio de uso del suelo
en el Refugio Nacional de Vida Silvestre Isla San Lucas.
En: Linea Base de los Componentes de Flora y Fauna en
el Refugio Nacional de Vida Silvestre Isla San Lucas, Costa
Rica, Promocin XVII, 2006, pp.9-22. ICOMVIS/UNA,
Heredia, Costa Rica.
Chapman, C. 1988. Patterns of foraging and range use
by three species of Neotropical primates. Primates 29:
177-194.
Crist6bal-Azkarate, J. 2003. Determinaci6n de la capaci-
dad de carga de un habitat y evaluaci6n de la capacidad
de adaptaci6n conductual y social de los monos aulla-
dores (Alouatta palliata mexicana). Tesis de Doctorado,
Universidad de Barcelona, Espafa.
Fedigan, L. 1986. Demographic trends in the Alouatta
palliata and Cebus capucinus populations of Santa Rosa
National Park, Costa Rica. In: Primate Ecology and Con-
servation, J. Else y P. Lee (eds.), pp.285-293. Cambridge
University Press, Cambridge.
Fedigan, L., Fedigan, L. y Chapman, C. 1985. A census of
Alouatta palliata and Cebus capucinus monkeys in Santa
Rosa National Park, Costa Rica. Brenesia 23: 309-322.
Froehlich, J.W. y Thorington Jr., R.W. 1982. Food limi-
tation on a small island and the regulation of population
size in mantled howling monkeys (Alouattapalliata). Am.
J Phys. Anthrop. 57: 190.
Froehlich, J.W. y Thorington Jr., R.W. 1990. Estructura
genetica y socioecologia de los monos aulladores (Alou-
atta palliata) de la isla de Barro Colorado. En: Ecologia
de un Bosque Tropical: Ciclos Estacionales y Cambios a
Largo Plazo, E. Leigh, A. Stanley y D. Windsor (eds.),
0. Londofo (trad.), pp.375-389. Smithsonian Tropical
Research Institute, Panami.
Froehlich, J.W., Thorington Jr., R.W. y Otis, J.S. 1981.
The demography of howler monkeys on Barro Colorado
Island, Panama. Int. J Primatol. 2: 207-236.
Glander, K. 1980. Reproduction and population growth
in free-ranging mantled howling monkeys. Am. J Phys.
Anthrop. 53: 25-36.
Heltne, P., Turner, D. y Scott, N. 1976. Comparison of
census data on Alouatta palliata from Costa Rica and
Panami. En: Neotropical Primates: Field Studies and Con-
servation: Proceedings of a Symposium on the Distribution
andAbundance of .J'.....- ..': 'Primates, R. W. Thorington
Jr. y P. G. Heltne (eds.), pp.10-19. Committee on Con-
servation of Nonhuman Primates, Institute of Laboratory
Animal Resources, Assembly of Life Sciences, National
Research Council, Washington, DC.
Howe, H. 1980. Monkey dispersal and waste of a neotro-
pical fruit. Ecology 61: 944-959.
Milton, K. 1979. Factors influencing leaf choice by howler
monkeys: A test of some hypotheses of food selection by
generalist herbivores. Am. Nat. 114: 362-378.


Milton, K. 1990. Calidad dietetica y regulaci6n demogrifi-
ca de una poblaci6n de monos aulladores Alouattapallia-
ta. En: Ecologia de un Bosque Tropical: Ciclos Estacionales
y Cambios a Largo Plazo, E. Leigh, A. Stanley y D. Wind-
sor (eds.), 0. Londofo (trad.), pp.357-373. Smithsonian
Tropical Research Institute, Panami.
Milton, K. y Mittermeier, R. 1977. A brief survey of the pri-
mates of Coiba Island, Panama. Primates 18: 931-936.
Costa Rica, MINAE. 2005. Plan Estratigico para elRefugio
Nacional de Vida Silvestre Isla San Lucas. Ministerio de
Ambiente y Energia, Costa Rica.
Morera, R. 1996. Uso de habitats y plants importantes en
la alimentaci6n de los monos aulladores (Alouattapallia-
ta) y carablancas (Cebus capucinus) en el bosque tropical
seco, Costa Rica. Tesis de Maestria, Universidad Nacio-
nal, Costa Rica.
Neville, M., Glander, K., Braza, E y Rylands, A. 1988. The
howling monkeys, genus Alouatta. En: Ecology and Beha-
viour of .'.....- . 'Primates, Vol. 2, R. A. Mittermeier, A.
Rylands, A. Coimbra-Filho y G. A. B. da Fonseca (eds.),
pp.349-454. World Wildlife Fund, Washington, DC.
Rosales-Meda, M. 2007. Uso de tipos de coberturas por
tropas de monos aulladores (Alouatta palliata palliata) y
carablancas (Cebus capucinus) en un agro paisaje, conoci-
miento y percepci6n de habitantes locales con respect a
los primates y propuesta base consensuada de manejo y
conservaci6n para 6stas species en el Pacifico Central,
Costa Rica. Tesis de Maestria, Universidad Nacional,
Costa Rica.
UICN, ORMA, WWF (eds). 1999. Listas de fauna de im-
portancia para la conservacion en Centroamerica y Mexico:
listas rojas, listas oficiales y species en Apendice CITES:
Sistema de integraci6n centroamericana. Direcci6n Am-
biental, Costa Rica.


ASPECTS ECOL6GICOS DE ALOUATTA GUARIBA
CLAMITANS CABRERA, 1940 NA AREA DE
RELEVANT INTERESSE ECOL6GICO FLORESTA
DA CICUTA, RIO DE JANEIRO, BRASIL

Sandro Leonardo Alves
Andre Scarambone Zai

Introduao

0 Brasil 6 considerado o detentor da maior diversidade de
esp6cies de primatas do mundo. Somente na FlorestaAtlan-
tica ocorrem 24 esp6cies, sendo 17 endemicas (Mendes et
al., 2003), entire elas Alouatta guariba (= A. fusca). A subes-
p6cie Alouatta guariba clamitans Cabrera, 1940 ocorre nos
Estados de Minas Gerais, Espirito Santo, Rio de Janeiro,
Sao Paulo, Parand, Santa Catarina e Rio Grande do Sul no
Brasil (Coimbra-Filho, 1990) e no norte da Argentina (Di
Bitteti et al., 1994). Ocupando originalmente cerca de 12%
do territ6rio brasileiro, atualmente a FlorestaAtlantica se en-
contra altamente fragmentada e seus maiores remanescentes
estao localizados principalmente nos Estados do Parand,





Neotropical Primates 14(3), December 2007


Sao Paulo, Minas Gerais, Rio de Janeiro, Espirito Santo e
na regiao sul da Bahia (Zad, 1998). Os primatas do genero
Alouatta Lacepede, 1799, familiar Atelidae, sao considerados
os mais folivoros entire as esp6cies neotropicais, por6m in-
cluem, quando disponiveis, quantidades variiveis de frutos
e flores a dieta (Neville et al., 1988; Queiroz, 1995). Estu-
dos term demonstrado que as diversas esp6cies do genero
ocupam Areas de vida pequenas, geralmente menores que
60 ha (Neville et al., 1988; Bicca-Marques, 2003).

Alouatta guariba clamitans encontra-se enquadrada como
"Quase Ameagada" na revisao da Lista Oficial de Espe-
cies da Fauna Brasileira Ameagada de Extingao (Rylands e
Chiarello, 2003) e "Presumivelmente Ameagada" na Lista
da Fauna Ameagada de Extingao do Estado do Rio de Ja-
neiro (Bergallo et al., 2000). Atualmente, pouco se conhece
sobre a ecologia e demografia de A. g. clamitans nos frag-
mentos de Floresta Atlhntica do Rio de Janeiro. Na regiao
do Mddio Vale do Paraiba do Sul (regiao sul do Estado)
inexistem informacoes acerca da situacao atual desta sub-
esp6cie. Este trabalho apresenta dados sobre a composigao
s6cio-etAria e a dieta de A. g. clamitans na Area de Relevante
Interesse Ecol6gico Floresta da Cicuta, unidade de conser-
vagao federal no Estado do Rio de Janeiro.

Material e MWtodos

Area de estudo
Abrangendo parte dos municipios de Barra Mansa e Volta
Redonda, na regiao do Mddio Vale do Paraiba do Sul,
Estado do Rio de Janeiro, a "Area de Relevante Interesse
Ecol6gico" (ARIE) Floresta da Cicuta (2224'-2238'S,
4409'-4420'W, 300-500 m a.n.m., 131 ha) 6 admin-
istrada pelo Instituto Brasileiro do Meio Ambiente e dos
Recursos Naturais Renoviveis (IBAMA) e pela Compan-
hia Siderdrgica Nacional (CSN). Sua vegetagao 6 caracter-
izada como Floresta Estacional Semidecidual Submontana
(IBGE, 1992), enquanto as areas adjacentes sno compostas
por matas em estigio inicial e intermediario de sucessao,
antigos plantios de E.., ',;.-.. sp. e pastagens. 0 clima 6
mesotermico (Cwa [Kappen]), apresentando duas esta-
goes bem definidas: estagao seca (maio-setembro, period
com pouca precipitagao e temperatures mais baixas) e es-
tagao chuvosa (outubro-abril, com elevadas temperatures
e concentracao das precipitacoes). As temperatures mddias
anuais variam entire 17 (julho) e 24C (fevereiro) e as


precipitao6es entire 1,000 e 1,600 mm/ano (Carauta et al.,
1992). As families com a maior riqueza de esp6cies na area
sao, em ordem decrescente, Myrtaceae, Leguminosae, Ru-
biaceae, Lauraceae e Euphorbiaceae (Faria, 2002; Souza,
2002). Aldm de A. g. clamitans, a ARIE Floresta da Cicuta
tambdm possui uma populagao introduzida de C
jacchus Linnaeus, 1758. A coleta de dados foi realizada em
uma area de 20 ha (aproximadamente 15% da Area total)
na parte nordeste da ARIE, cuja selegao levou em consid-
eracao caracteristicas favoriveis is observagoes, tais como,
ficil acesso, presenga de uma trilha principal (2 km) e di-
versas "picadas", al6m de abranger o limited (borda) entire a
Area florestada e a Area coberta por pastagens.

Metodologia
Entre abril e dezembro de 2002, cerca de tries dias mensais
foram dedicados a coleta de dados populacionais por um
hnico observador. 0 m6todo consistiu em procurar grupos
de A. g. clamitans ao long da trilha principal (2 km) no
period das 06:00 is 18:00 h. Sempre que possivel, cada
grupo localizado era acompanhado at6 a determinacao
confiivel de seu tamanho e composigao etirio-sexual. Uti-
lizou-se a classificacao etAria proposta por Mendes (1989).
0 estudo da dieta foi realizado entire os meses de junho e
novembro de 2003, a excegao de Agosto, durante tries dias
por mes, totalizando cerca de 165 h de esforgo amostral.
Cada event individual de alimentagao foi registrado, in-
cluindo o item consumido (folha madura, folha nova, folha
em estigio de maturacao indeterminado, flor, fruto e broto,
conforme Mendes, 1989) e o hibito (irvore, trepadeira ou
indeterminada) da fonte alimentar.

Resultados e Discussio

Foram encontrados quatro grupos (Tabela 1) e um macho
adulto solitirio, totalizando 24 animals. Cada grupo foi de-
nominado de acordo com alguma caracteristica ambiental
de sua irea de uso. Todos os grupos apresentaram uma es-
trutura social uni-macho (Eisenberg et al., 1972), a semel-
hanga do observado por Mendes (1989: 84% dos grupos)
em Minas Gerais, Steinmetz (2001: 83%) em Sao Paulo e
Limeira (1996: 100%) no Rio de Janeiro. 0 tamanho mddio
dos grupos foi de 5,8 individuos, mesmo valor observado
por Silva (1981) e Steinmetz (2001). Devido ao pequeno
tamanho amostral nao 6 prudent estimar a densidade pop-
ulacional de A. g. clamitans na ARIE Floresta da Cicuta.


Tabela 1. Composiygo dos grupos de Alouatta 7 clamitans encontrados na ARIE Floresta da Cicuta, RJ, Brasil, entire abril e dezem-
bro de 2002.
Macho
Grupo N Macho adulto FRmea adulta subadulto Juvenil Infante Indeterminado

Bambuzal 8 1 3 1 1 2
Vale 8 1 3 1 1 2
Ponte 4 1 1 1 1
Riacho 3 1 2
Total 23 4 9 3 1 1 5





Neotropical Primates 14(3), December 2007


Um total de 60 registros de alimentagao foi obtido, sendo
o item folha responsivel por 81% do consume. Brotos,
frutos e flores foram consumidos em menores proporgoes
(respectivamente, 10%, 7% e 2% dos registros). Esta dieta
principalmente folivora provavelmente foi observada pelo
fato da coleta de dados ter sido realizada apenas durante o
period de transicao entire a estiagem e a estaago chuvosa,
6poca na qual hi uma escassez de frutos e flores comestiveis.
Folhas maduras foram consumidas em maior proporgao
em relagao a folhas novas (respectivamente, 51% e 43%
do total das folhas consumidas) e folhas provenientes de
irvores compuseram 64% dos registros. As folhas de trepa-
deiras, plants abundantes na irea de estudo localizada na
borda da floresta da ARIE, foram responsiveis por 26% dos
registros de consume de folhas. Sua abundancia por todo o
fragmento associada a caracteristica produgao constant de
folhas novas das esp6cies vegetais de hibito trepador, faz das
lianas e trepadeiras importantes recursos alimentares para
A. g. clamitans (Alves, 2004).

Os dados aqui apresentados sao preliminares e estudos de
longa duracao sobre o padrao de atividades, uso do espago
e dieta (quantidade e esp6cies consumidas) sao necessarios
para o entendimento das relagoes entire a populagao de
A. g. clamitans e o fragmento florestal em que habitat. Estu-
dos relatados por Bicca-Marques (2003) demonstram a ca-
pacidade de sobrevivencia das esp6cies do genero Alouatta
em habitats perturbados de variados tamanhos. Por6m,
apesar da existencia de A. g. clamitans nos fragments de
menor tamanho ao redor da ARIE Floresta da Cicuta, se-
gundo informacoes fornecidas por guards que executam
o patrulhamento da airea, nao se observa nenhum tipo de
conectividade entire essas "ilhas" de floresta e a unidade de
conservagao, o que pode reduzir ou eliminar o fluxo de in-
dividuos geneticamente diferentes e a possibilidade de (re)
colonizacao de novas areas. Devido ao process de ocupa-
gao humana ocorrido na regiao do Medio Vale do Paraiba
do Sul, os principals remanescentes de Floresta Atlrntica
se encontram em propriedades particulares, sujeitos a dev-
astagao. Com o acelerado process de fragmentagao nesta
regiao, acoes planejadas para a conservacao de A. g. clami-
tans devem ser realizadas para evitar que as iltimas popu-
lacoes fiquem aqudm do limited de sustentagao gen&tica e
ecol6gica. Sugere-se que areas privadas que ainda preservam
populagoes desta subesp6cie e outras esp6cies de primatas
sejam mantidas e protegidas, se possivel convertendo-as em
unidades de conservagao particulares (RPPNs).

Agradecimentos

Agradecemos a Fundagao CSN pela autorizacao de pes-
quisa e auxilio financeiro. Ao Prof. Dr. Lenicio Gongalves
e ao Prof. Dr. H61io Ricardo da Silva, Universidade Federal
Rural do Rio de Janeiro (UFRRJ), pelas critics e sugest6es
a este trabalho.

Sandro Leonardo Alves, Reserva Biol6gica do Guapord,
Av. Limoeiro, s/n, Centro, Costa Marques, 27320-690,


Rond6nia, Brasil, e-mail: e
Andr6 Scarambone Zaii, Laborat6rio de Ecologia Flor-
estal, Universidade Federal do Estado do Rio de Janeiro
(UNIRIO), Av. Pasteur, 458 Sala 503, Urca, Rio de Janei-
ro, 22290-240, Rio de Janeiro, Brasil, e-mail: unirio.br>.

Referencias

Alves, S. L. 2004. Aspectos ecol6gicos e conservagao de
Alouatta guariba clamitans (Primates, Atelidae) na Area
de Relevante Interesse Ecol6gico Floresta da Cicuta,
Regiao do Mddio Vale do Paraiba do Sul, RJ. Monografia
de Bacharelado, Universidade Federal Rural do Rio de
Janeiro, Seropddica.
Bergallo, H. G., Rocha, C. E D., Alves, M.A. S. e Sluys, M.
van. 2000. A Fauna Ameafada de Extinado do Estado do
Rio deJaneiro. Editora da UERJ, Rio de Janeiro.
Bicca-Marques, J.C. 2003. How do howler monkeys
cope with habitat fragmentation? Em: Primates in Frag-
ments: Ecology and Conservation, L. K. Marsh (ed.),
pp.283-303. Kluwer Academic/Plenum Publishers,
New York.
Carauta, J. P. P., Lima, D. F., Vianna, M.C., Ascencao,
M.R. e Lins, E.A.M. 1992. Vegetagao da Floresta da
Cicuta, Estado do Rio de Janeiro: ObservagCes prelimi-
nares. Albe: roa 3(11): 101-124.
Coimbra-Filho, A. E 1990. Sistemitica, distribuigao geo-
grifica e situacao atual dos simios brasileiros (Platyrrhini
Primates). Rev. Brasil. Biol. 50(4): 1063-1079.
Di Bitteti, M.S., Placci, G., Brown, D. e Rode, D.I. 1994.
Conservation and population status of the brown howl-
ing monkey (Alouatta fusca clamitans) in Argentina.
Neotrop. Primates 2(4): 1-4. 1994.
Eisenberg, J. E, Muckenhirn, N.A. e Rudran, R. 1972. The
relation between ecology and social structure in Primates.
Science 176(4037): 863-874.
Faria, M.J.B. 2002. Caracterizaino e estrutura da vegeta-
gao de um trecho de borda de um fragmento de Mata
Atlhntica (Floresta da Cicuta), no municipio de Volta Re-
donda-Estado do Rio de Janeiro. Monografia de Espe-
cializacao, Universidade Federal Rural do Rio de Janeiro,
Seropddica.
IBGE. 1992. Manual Tlcnico da Vegetacdo Brasileira.
Fundagao Instituto Brasileiro de Geografia e Estatistica
(IBGE), Rio de Janeiro.
Limeira, V.L.A.G. 1996. Comportamento alimentar,
padrao de atividades e uso do espago por Alouattafusca
(Primates, Platyrrhini) em um fragmento degradado de
Floresta Atlhntica no Estado do Rio de Janeiro. Disserta-
gao de Mestrado, Universidade Federal do Rio de Janeiro,
Rio de Janeiro.
Mendes, S. L. 1989. Estudo ecol6gico de Alouatta fusca
(Primates: Cebidae) na Estagao Biol6gica de Caratinga,
MG. Revista Nordestina de Biologia 6(2): 71-104.
Mendes, S. L., Coutinho, B. R. e Moreira, D. 0. 2003. Efe-
tividade das unidades de conservagao da Mata Atlhntica
para a protegao dos primatas ameagados de extingao. Em:





Neotropical Primates 14(3), December 2007


VI Congress de Ecologia do Brasil Anais de Taibal/o,
Completos, pp.286-287. Editora da UFCE, Fortaleza.
Neville, M.K., Glander, K.E., Braza, E e Rylands, A.B.
1988. The howling monkeys, genus Alouatta. Em: Ecolo-
gy and Behavior of .'...... 'Primates, Vol. 2, R.A. Mit-
termeier, A. B. Rylands, A. F Coimbra-Filho e G.A. B. da
Fonseca (eds.), pp.349-453. World Wildlife Fund, Wa-
shington, DC.
Queiroz, H. L. 1995. Preguifas e Guaribas: Os Mamiferos
Folivoros Arboricolas do Mamiraud. CNPq, Brasilia e So-
ciedade Civil Mamiraud, Tef6.
Rylands, A. B. e Chiarello, A. G. 2003. Official list of Bra-
zilian fauna threatened with extinction 2003. Neotrop.
Primates 11(1): 43 -49.
Silva, E.C. 1981. A preliminary survey of brown howler
monkeys (Alouattafusca) at the Cantareira Reserve (Sao
Paulo, Brazil). Rev. Bras. Biol. 41(4): 897-909.
Souza, G. R. 2002. Floristica do estrato arbustivo-arb6reo
da Floresta da Cicuta, um fragmento de Floresta Atlin-
tica no municipio de Volta Redonda, Estado do Rio de
Janeiro. Dissertagao de Mestrado, Universidade Federal
Rural do Rio de Janeiro, Seropddica.
Steinmetz, S. 2001. Densidade e conservagao do bugio
(Alouatta fusca) no Parque Estadual Intervales. Neotrop.
Primates 9(2): 69-73.
Zad, A.S. 1998. Fragmentagao da Mata Atlintica: Aspec-
tos te6ricos. Floresta eAmbiente 5(1): 160-170.


A PRELIMINARY STUDY OF PROXIMITY
PATTERNS AMONG AGE-SEX CLASSES IN A
POPULATION OF CENTRAL AMERICAN BLACK
HOWLERS (ALOUATTA PIGRA)

Lisa C. Corewyn
M. S. M. Pavelka

Introduction

Affiliative interactions reflect the nature of social bonds
within primate social groups, which in turn can reflect
the pattern of dispersal. In female resident societies, re-
lated females tend to affiliate more closely with one an-
other, and the reverse is reported for male resident groups
(Strier, 1994; Strier et al., 2002). Bisexual or female dis-
persal may be associated with stronger bonds between
adult males and females (Printes and Strier, 1999; Di
Fiore and Fleischer, 2005), and weaker bonds between
females (Strier, 1999).

Central American black howler monkeys (Alouatta pigra),
recently upgraded to Endangered by the IUCN (IUCN,
2003), are folivore/frugivores (Silver et al., 1998; Pavelka
and Knopff, 2004) that live in small groups of 2-10 indi-
viduals. Groups are usually comprised of one or more adult
males plus one or more adult females and juveniles (Hor-
wich et al., 2001; Ostro et al., 2001). Preliminary reports
indicate bisexual dispersal (Brockett et al., 2000a; Pavelka,


unpub. data), as seen in other howler monkey species
(Crockett and Eisenberg, 1997; Di Fiore and Campbell,
2007), but long-term data on known individuals is not
yet available. Despite the highly cohesive nature of howler
monkey social groups (Bernstein, 1964; Stevenson et al.,
1998), overt social interactions are few. In black howler
monkeys, less than 4% of time is typically spent in social
interactions such as grooming and hand-holding among
adults (Silver et al., 1998; Brockett et al., 2000b; Pavelka
and Knopff, 2004; Brockett et al., 2005).

Spacing patterns are important indicators of the underlying
social relationships that aid in establishing affiliative con-
tacts, and in avoiding agonistic interactions and predation
(Altmann, 1980; White and Chapman, 1994). Kummer
(1971: 221) argued that "social affinity and spatial proxim-
ity are so highly correlated that the distribution of animals
in space can be used as a first reading of their social struc-
ture". Female social relationships in black howler monkeys
appear to be, like those of other howler monkeys, undif-
ferentiated and egalitarian (Pavelka, unpub. data). Crock-
ett and Eisenberg (1987) have suggested that measures of
inter-individual proximity may be one of the few ways
to quantify affiliative social relationships within howler
monkey groups. In this paper we describe the results of a
preliminary study of proximity patterns to help elucidate
the nature of within-group social bonds in A. pigra.

Methods

This study was conducted at Monkey River in the Toledo
district of Belize. The 52 ha study site is located within
a 100 km2 lowland semi-evergreen riparian forest along
the river. The area exhibits a distinctive dry season, gen-
erally from January to May, and a wet season from June
to December. The average annual temperature in the area
is 260C, with an average annual rainfall of approximately
2,460 mm (Pavelka and Knopff, 2004). Over 160 hours of
focal animal data were collected on 11 adults and juveniles
(infants were not sampled) living in three groups (A, D,
and Q). Each of the three groups contained one adult male
and two adult females, and group Q also had two juveniles
(defined as independent offspring over one year of age).
Ten-minute focal animal samples were collected from each
group member, with no individual sampled more than
once each hour, in order to maintain independence across
sample points. The first individuals were sampled opportu-
nistically and on a rotating basis thereafter. Though indi-
viduals could not always be reliably identified, we used age-
sex class and location relative to other group members to
ensure individuals were as equally represented as possible.
At the start of each focal animal sample, we conducted a
proximity scan to record the age-sex class of each neighbor
within 2 m of the focal animal (following the proximity
categories established for A. pigra [Schneider et al., 1999;
Treves et al., 2001], and other howler monkey species such
as A. palliata [Zucker and Clarke, 1998] and A. seniculus
[Stevenson et al., 1998]). Each group was followed from





Neotropical Primates 14(3), December 2007


dawn to dusk once per week over the wet season study
period of July 2003 to January 2004.

From the 960 proximity scans, we calculated proximity
scores for dyads using a formula adapted from Matsumura
and Okamoto (1997):


another with whom it had been in one meter proximity)
from the focal animal data:


APPa
APPb + APPa


LEA
LEA x 100
LEAb + LEA


fa(A)
b) --x 100
F(A)


Where a) F(A) was the total number of proximity scans for
a given age-sex class A; F(B) was the total number of prox-
imity scans for a given age-sex class B; fA (B) was the total
number of proximity scans in which B was found within
2 m of A when A was scanned; and f, (A) was the total
number of proximity scans in which A was found within
2 m of B when B was scanned. Although this formula was
originally intended for individual dyad analyses, we have
adapted it for age-sex classes. Given that there were differ-
ent numbers of individuals and different numbers of sam-
ples for each age-sex class, for dyads with the same age-sex
class, we b) divided the number of near proximity scans
for that dyad by the total number of proximity scans for
that focal age-sex class. Dyads with an unknown age-sex
class were dropped from this part of the analysis. Proxim-
ity data from the three groups were pooled, with the ex-
ception of dyads involving juveniles, which were calculat-
ed by group, as juveniles were only present in one group.
Chi-square tests were used due to the small sample sizes
and the categorical nature of the data (Siegel and Castellan
Jr., 1988).

Maintenance of proximity was calculated using Hinde's
index (Hinde and Atkinson, 1970) for each of the prox-
imity dyads using the frequency of approaches (when one
individual approached and settled within one meter of
another) and leaves (when one animal moved away from


fA(B) + f,(A)
a) x 100
F(A) + F(B)


65.3


Rf 5


53.3


E AM-AF
* AF-AF
H AF-JV
AM-JV
SJV-JV


Group A Group D Group Q

Figure 1. Proximity score by age-sex dyad for each group. AM adult male; AF= adult female; JV= juvenile.


Where APPa was the number of approaches by age-sex class
a towards age-sex class b; APPb was the number of ap-
proaches by age-sex class b towards age-sex class a; LEA
was the number of leaves by age-sex class a from age-sex
class b; and LEAb was the number of leaves by age-sex
class b from age-sex class a. If the percentage was positive,
then age-sex class a was more responsible than b for main-
taining proximity, and vice versa if the percentage was neg-
ative. Low values of Hinde's index indicated a tendency for
individuals in those dyads to be equally responsible for
maintenance of proximity.

Results

Confirming the cohesive nature of Central American
black howler monkeys, in 70.6% of the 960 proximity
scans (divided into 347, 247, and 366 total scans for each
group respectively) the focal animal had another individ-
ual within 2 m significantly more often than not (29.4%,
or 284 scans with no individual within 2 m; x2= 611.2,
df = 2, p < 0.001). Proximity scores were highest for juve-
niles (80%), followed by adult females (72.5%) and then
males (65.8%). Fig. 1 shows the overall proximity scores
within and across each age-sex class for each group. Adult
females were in close proximity to other adult females as
often as they were to adult males. However, analysis of
the strength of the adult dyads revealed that females as-
sociated with one another more than expected given the
availability of congeners in each group (2 = 6.24, df= 1,
p= 0.01). It is possible that the percentage of time adult
males spent in close proximity to adult females in each





Neotropical Primates 14(3), December 2007


group was artificially low, given that males could have had
both group females in close proximity at once; however,
only dyadic interactions were analyzed as part of this study.
In the only group with juveniles (group Q), the proximity
score for adult females with juveniles was 65.3%, and juve-
niles were in close proximity to other juveniles in 56.9% of
their proximity scans. The least commonly occurring dyad
in this group was adult males and juveniles (49.7%).

Maintenance of proximity was calculated to determine
which age-sex class was responsible for maintaining the
"relationship" within each dyad (Table 1). Between adult
females and adult males, females were slightly more respon-
sible for maintaining proximity (5.5%), although the low
score suggested fairly even responsibility. Juveniles were
15.3% more responsible for maintaining the spatial rela-
tionship with adult females; however, adult males and juve-
niles appeared to be equally responsible.

Discussion

Despite low levels of conspicuous social interaction and
undifferentiated social relationships in A. pigra, the prox-
imity data presented here support the overall impression
that the groups were nonetheless very cohesive. If spatial
proximity is taken as an indication of social affinity, as has
been suggested (Kummer, 1971; Altmann, 1980; White
and Chapman, 1994), the spacing patterns reported here
further revealed variation among age-sex classes in strength
of social bonds. Juveniles exhibited a higher degree of affili-
ation than adults, and females exhibited a higher degree of
affiliation than males. Being smaller in size and less experi-
enced than adults, young monkeys may be more vulnerable
to predation and might spend more time near other indi-
viduals, particularly their mothers, as a result. Proximity
patterns and vigilance rates (a measure of predation risk
through scanning behavior) have been found to be related
in A. pigra, with vigilance decreasing as the number of close
neighbors increases (Treves et al., 2001). Moreover, juve-
niles spend more time in social play than adults, increasing
the amount of time in close proximity.

Individual adult female proximity scores were higher than
those of adult males, as expected given the likely association
between adult females and their own juvenile offspring.
However, the analysis of the strength of different dyadic
combinations revealed a surprising affiliation between


adult females. In this study, adult females had equal op-
portunity to interact with another female or with the
adult male. Adult males, conversely, could only associate
with adult females. Thus, the finding that the male-female
and female-female dyads occurred equally was surprising,
with female-female dyads occurring more than would be
expected given availability of congeners and certainly
given the bisexual dispersal pattern and unimale groups,
which would predict weaker female-female associations
than male-female associations.

Further, evidence of seasonal mating appeared to be absent
as copulations were not observed. This result has been
found in other howler monkey studies, suggesting that the
dispersal patterns of female primates may not be a con-
sistent predictor of social bonds, at least as measured by
proximity patterns. Wang and Milton (2003) reported that
adult male howlers (A. palliata) at Barro Colorado Island
were most often in close association with adult females, as
would be expected for a female-dispersing species; these
findings were in contrast to those of Zucker and Clarke
(1998) and Kovacovsky (2002), who found A. palliata fe-
males spent more time in close proximity with one another
than expected. Zucker and Clarke (1998) reported that
adult dyads varied in frequency and intensity across years
and among individuals, and suggested that female bonds
were likely influenced by female reproductive status and
parity, and by changing memberships of adult males within
the groups.

When comparing A. pigra with red-tailed monkeys
(Cercopithecus ascanius schmidtii) and red colobus mon-
keys (Procolobus badius tephrosceles), Treves and Baguma
(2002) unexpectedly found that females in the two spe-
cies with female transfer black howler monkeys and
red colobus monkeys were significantly more cohesive
than the female red-tailed monkeys, who are female-resi-
dent. Though kinship was not known in our study, some
individuals could have been related, thereby affecting dif-
ferential proximity. Further, the data on the maintenance
of proximity presented here revealed that females were not
more responsible for maintaining proximity with adult
males than males were with them. Females may derive
more benefit from associating with males when in unimale
groups, as their groups can be more vulnerable to takeovers
by extragroup males (Crockett and Janson, 2000). Not sur-
prisingly, juveniles were more responsible for maintaining


Table 1. Number of approaches and leaves attributed to each age-sex class. AM = adult male; AF = adult female; JV= juvenile;
N App = number of approaches over study period; N Lea = number of leaves over study period; H Index = Hinde's index (%).
Age-sex class to Received AM Received AF Received JV
which action was N N H N N H N N
attributed App Lea Index App Lea Index App Lea H Index
AM 88 93 -5.5 35 36 2.6
AF 98 83 5.5 69 112 -15.3
JV 83 97 -2.6 196 159 15.3





Neotropical Primates 14(3), December 2007


proximity to adult females, as they may derive more benefit
from close associations with females for predator protec-
tion, and to gain social, survival, and maternal skills.

Though infants were not sampled, they were present
in each of the three groups at various times through the
study period and could conceivably have affected proxim-
ity results, particularly among lactating and non-lactating
females (see Corewyn, 2005). We caution against broad
generalizations given the small sample size in the number
of groups, particularly with regard to juvenile proximity,
since these data were only representative of one group. We
are unable to comment on male-male social relationships
in A. pigra, and look to future research to address these
limitations.

Acknowledgements

We would like to thank the people of Monkey River and
Placencia for their help and support. For his help with
statistical analyses, we gratefully acknowledge Dr. Tak
S. Fung of the Department of Mathematics and Statistics,
University of Calgary. We are grateful to Travis Steffens,
Keriann McGoogan, Alison Behie, Grainne McCabe, and
Allison Maclean for their help with data collection, and
to Tracy Wyman for technical assistance. Support for this
project was provided by the Calgary Zoo Conservation
Fund, Natural Sciences and Engineering Research Coun-
cil of Canada, Province of Alberta Graduate Scholarship,
National Geographic Society, Calgary Institute for the
Humanities, Department ofAn rl...p..1..;:, and the Facul-
ties of Social Sciences and Graduate Studies at the Univer-
sity of Calgary.

Lisa C. Corewyn, Department of i, rl-...p..1..;,, University
of Texas at San Antonio, One UTSA Circle, San Antonio,
TX 78249-0649, USA, e-mail:
and M.S.M. Pavelka, Department of Anrl-..i.p..1.. ,, Uni-
versity of Calgary, 2500 University Drive N.W., Calgary,
AB T2N 1N4, Canada.

References

Altmann, J. 1980. Baboon Mothers and Infants. Harvard
University Press, Cambridge, Massachusetts.
Bernstein, I. S. 1964. A field study of the activities of howler
monkeys. Anim. Behav. 12: 92-97.
Brockett, R. C., Horwich, R. H. and Jones, C. B. 2000a.
Female dispersal in the Belizean black howling monkey
(Alouatta pigra). Neotrop. Primates 8: 32-34.
Brockett, R.C., Horwich, R.H. and Jones, C.B. 2000b.
A model for the interpretation of grooming patterns ap-
plied to the Belizean black howling monkey (Alouatta
pigra). Primate Report 56: 23-32.
Brockett, R.C., Horwich, R.H. and Jones, C.B. 2005.
Hand-holding by Belizean black howler monkeys: In-
tentional communication in a Neotropical primate. Folia
Primatol. 76: 227-230.


Corewyn, L. C. 2005. Proximity patterns in the Central
American black howler (Alouattapigra) at Monkey River,
Belize. Master's thesis, University of Calgary, Alberta,
Canada.
Crockett, C.M. and Eisenberg, J.F. 1987. Howlers: Varia-
tions in group size and demography. In: Primate Societies,
B.B. Smuts, D. L. Cheney, R.M. Seyfarth, R.W. Wrang-
ham and T.T. Struhsaker (eds.), pp.54-68. University of
Chicago Press, Chicago and London.
Crockett, C. M. and Janson, C. H. 2000. Infanticide
in red howlers: Female group size, male member-
ship and a possible link to folivory. In: Infanticide
by Males and its Implications, C.P. van Schaik and
C.H.Janson (eds.), pp.75-98. CambridgeUniversityPress,
Cambridge.
IUCN. 2003. Alouatta pigra. 2003 IUCN Red List of
Threatened Species. Website: .
Accessed 26 May 2004.
Di Fiore, A. and Fleischer, R.C. 2005. Social behavior, re-
productive strategies, and population genetic structure of
Lagothrixpoeppigii. Int. J Primatol. 26: 1137-1173.
Di Fiore, A. and Campbell, C.J. 2007. The Atelines:
Variation in ecology, behavior, and social organization.
In: Primates in Perspective, C.J. Campbell, A. Fuentes,
K.C. MacKinnon, M. Panger and S.K. Bearder (eds.),
pp.155-185. Oxford University Press, New York.
Hinde, R.A. and Atkinson, S. 1970. Assessing the roles of
social partners in maintaining mutual proximity, as ex-
emplified by mother-infant relations in rhesus monkeys.
Anim. Behav. 18: 169-176.
Horwich, R.H., Brockett, R.C., James, R.A. and Jones,
C.B. 2001. Population structure and group productivity
of the Belizean black howling monkey (Alouatta pigra):
Implications for female socioecology. Primate Report 61:
47-65.
Kovacovsky, S. 2002. Proximity patterns of adult female
mantled howler monkeys (Alouatta palliata): Evidence
for female-bonding. Am. J Primatol. 57 (S1): 24-25.
Kummer, H. 1971. Spacing mechanisms in social behav-
ior. In: Man and Beast: Comparative Social Behavior,
J.F. Eisenberg and W.S. Dillon (eds.), pp.220-234.
Smithsonian Institution Press, Washington, DC.
Matsumura, S. and Okamoto, K. 1997. Factors affecting
proximity among members of a wild group of moor ma-
caques during feeding, moving and resting. Int. J Prima-
tol. 18: 929-940.
Ostro, L.E.T., Silver, S.C., Koontz, FW., Horwich, R.H.
and Brockett, R. 2001. Shifts in social structure of black
howler (Alouatta pigra) groups associated with natural
and experimental variation in population density. Int. J.
Primatol. 22: 733-748.
Pavelka, M. S. M. and Knopff, K. H. 2004. Diet and activ-
ity in black howler monkeys (Alouatta pigra) in southern
Belize: Does degree of frugivory influence activity level?
Primates 45: 105-111.
Printes, R. C., and Strier, K. B. 1999. Behavioral correlates
of dispersal in female muriquis (Brachyteles arachnoides).
Int. J Primatol. 20: 941-960.





Neotropical Primates 14(3), December 2007


Schneider, E.C., Hunter, L.F. and Horwich, R.H. 1999.
Adoption of a young juvenile in black howler monkeys
(Alouatta pigra). Neotrop. Primates 7: 47-51.
Siegel, S. and Castellan Jr., N.J. 1988. Nonparametric Sta-
tistics for the Behavioral Sciences. McGraw-Hill, Boston.
Silver, S.C., Ostro, L.E.T., Yeager, C.P. and Horwich,
R. 1998. Feeding ecology of the black howler monkey
(Alouatta pigra) in northern Belize. Am. J Primatol. 45:
263-279.
Stevenson, P.R., Quinones, M.J. and Ahumada, J.A.
1998. Effects of fruit patch availability on feeding sub-
group size and spacing patterns in four primate species
at Tinigua National Park, Colombia. Int. J. Primatol. 19:
313-324.
Strier, K.B. 1994. Brotherhoods among Atelins: Kinship,
affiliation, and competition. Behaviour 130: 151-167.
Strier, K.B. 1999. Why is female kin bonding so rare?
Comparative sociality of neotropical primates. In: Com-
parative Primate Socioecology, P. C. Lee (ed.), pp.300-319.
Cambridge University Press, Cambridge, UK.
Strier, K.B., Dib, L.T. and Figueira, J. E. C. 2002. Social
dynamics of male muriquis (Brachyteles arachnoides hy-
poxanthus). Behaviour 139: 315-342.
Treves, A. and Baguma, P. 2002. Interindividual proxim-
ity and surveillance of associates in comparative perspec-
tive. In: The Guenons: Diversity and Adaptation in African
Monkeys, M. E. Glenn and M. Cords (eds.), pp.161-172.
Kluwer Academic/Plenum Publishers, New York.
Treves, A., Drescher, A. and Ingrisano, N. 2001. Vigi-
lance and aggregation in black howler monkeys (Alouatta
pigra). Behav. Ecol. Sociobiol. 50: 90-95.
Wang, E. and Milton, K. 2003. Intragroup social relation-
ships of male Alouattapalliata on Barro Colorado Island,
Republic of Panama. Int. J Primatol. 24: 1227-1243.
White, F.J. and Chapman, C.A. 1994. Contrasting chim-
panzees and bonobos: Nearest neighbor distances and
choices. Folia Primatol. 63: 181-191.
Zucker, E.L. and Clarke, M.R. 1998. Agonistic and affili-
ative relationships of adult female howlers (Alouatta pal-
liata) in Costa Rica over a 4-year period. Int. J Primatol.
19: 433-449.


DENSITY OF SAGUINUS INUSTUS (SCHWARTZ,
1951) IN THE INTERFLUVIUM OF THE CAQUETA-
APAPORIS RIVERS, COLOMBIAN AMAZONIA

Claudia Idaly Castillo-Ayala
Erwin Palacios


Introduction


The Amazon bioregion is considered one of the highest bio-
diversity areas in the world. Primates are important com-
ponents of this biodiversity, and with 15 genera, 81 species
and 134 taxa, they are the most emblematic faunal group
of Amazonia (Mittermeier et al., 2002). Saguinus is per-
haps the most diverse of Neotropical primate genera, with


13-15 species and 33 recognized forms (Hershkovitz,
1977; Rylands et al., 2000). Defler (2003a) recognizes the
presence of six species of Saguinus in Colombia (40-46%
of the total species in the genus), three of them exclusively
distributed in the Colombian Amazon: S.fuscicollis (Spix,
1823), S. ..- (Spix, 1823), and S. inustus (Schwartz,
1951). Saguinus inustus, the mottled-face tamarin, is dis-
tributed in southeastern Colombia, west of the Andes,
between the Guayabero-Guaviare rivers and the Caqueti
River, and between the Mesay River and the border with
Brazil; however, accurate eastern and western boundar-
ies of its geographical range within the country are still
unknown (Defler, 2003a). The species is also present in
western Brazil, between the Rio Negro and the Colombian
border.

Saguinus inustus is one of the least-studied species of
Neotropical primates; preliminary information on its ecol-
ogy (ranging and diet) comes from only two short studies
carried out near La Pedrera, at Comeyafi Indigenous Re-
serve, an interfluvial area between the Caqueti and Apapo-
ris rivers (Palacios et al., 2004; Defler, unpublished data),
and from occasional observations of foraging groups in
the Amana Sustainable Development Reserve in Brazil (de
Souza et al., 2004). Here we present the first data on the
density of S. inustus. We collected this information during
a primate survey in the lower Caqueti River as part of a
larger effort started six years ago to document and monitor
the densities of primates and 15 other large vertebrate spe-
cies in eastern Colombian Amazonia (Palacios et al., 2003;
Palacios and Peres, 2005; Peres and Palacios, 2007).

Methods

Study area
Censuses were carried out in the interfluvial area between
the lower Caqueti and Apaporis Rivers, Amazonas, near
Loma Linda indigenous community (0116'S, 69044'W,
101 m a.s.1.; Fig. 1), C6rdoba Indigenous Reserve. Prima-
ry terra firme and virzea forests represented the majority
of the forested matrix in the study site. An area of second-
ary terra firme forest (locally called rastrojo) located around
the indigenous settlement comprised a small proportion
of such matrix. There were also patches of what is locally
known as savanna forest or varillal, which corresponds to
primary forest with a mean height of 17-18 m, and a very
sparse understory growing on rocky outcrops and white
sands; and another savanna type known as sabana capo-
tuda, with a mean canopy height of 8 m, deep soil litter
and a very dense understory with intermingled vines and
lianas.

Linear transects
We used the line transect method (Burnham et al., 1980)
to estimate S. inustus densities. From a zero point lo-
cated ca. 100 m away from the community secondary
forest area, two transects (4.6 and 4.9 km long, oriented
40 NW and 40 NE respectively) were cut; they were





Neotropical Primates 14(3), December 2007


Figure 1. The lower Caqueti region in Eastern Colombian Amazonia. Black square shows the area where censuses were carried out.


marked with flagging tape every 50 m to facilitate ac-
curate location of sightings. Transects were cut a month
before we started the censuses, so at the time of the study,
local fauna were already habituated to the transect paths.
The shortest transect crossed nearly 2 km of rastrojo,
1.1 km of varillal, and 1.5 km of primary terra firme ter-
race forest. The second transect crossed hilly primary
terra firme forest with sandy soils in the first half of its
length and clay soils in the second, as well as patches of
sabana capotuda.

Censuses were carried out during 10 days each month
between October 2005 and February 2006. Independent
observers walked the transects during days without rain at
a mean speed of 1.2 km/h, between 0630 and 1130 hrs.
Community members previously trained and able to accu-
rately detect and identify local primate species participated
in the surveys. Every time we encountered groups of S. in-
ustus, we recorded the date, time, number of individuals,
perpendicular distance from the transect, distance walked,
height and type of forest. After each encounter, a maxi-
mum of 15 minutes were spent to obtain accurate counts
of groups. Data were analyzed using DISTANCE 5.0 Beta
5 software (Thomas et al., 2005).


Results and Discussion

A total census effort of 380 km was achieved, during
which groups of S. inustus were sighted 33 times. Six ad-
ditional primate species are sympatric with S. inustus in
the lower Caqueti and Apaporis interfluvial area: Alouatta
seniculus, Aotus cf. vociferans, Callicebus torquatus, Cebus
,Ibj.fo1:s, Cebus apella, and Saimiri sciureus. Although the
study site is included in the distribution range of Lago-
thrix lagothricha, this species was not recorded during the
survey period. People from Loma Linda said they have
never seen woolly monkeys in that area, and this is likely
to be a consequence of a long history of human settlement
and subsistence hunting in the region. L. lagothricha has
not been recorded recently in the lower interfluvium of
the Caqueti and Apaporis Rivers, east of the mouth of the
Miriti River (Palacios, pers. obs.), and the species is likely
to be locally extinct.

We estimated a S. inustus density of 3.8 groups/km2
and 19.6 individuals/km2. Mean group size was 5.2 in-
dividuals (sd= 1.87). The mottled-face tamarin was one
of the primate species most frequently encountered after
C torquatus and S. sciureus (Castillo-Ayala, in prep.).





Neotropical Primates 14(3), December 2007


Mottled-faced tamarin density at Loma Linda is in the
range of that reported for other Saguinus species in nine
different localities in western Amazonia (Soini, 1981;
Freese etal., 1982; Pook and Pook, 1982; Terborgh, 1983;
Peres, 1997), but high compared with those reported for
S.fuscicollis at some sites in eastern Colombian Amazonia
(3.4-16.9 individuals/km2: Palacios et al., 2003; Palacios
y Peres, 2005; Palacios, unpublished data). In contrast,
S. fuscicollis densities in three other sites in eastern Co-
lombian Amazonia (Cano Arapa and Cano Esperanza,
Pure National Park, and Cano Curare) were much higher
(21.5, 26.5, and 30.3 individuals/km2 respectively; Pala-
cios, unpubl. data) than those found for S. inustus at Loma
Linda. Mean group size is in the range recorded for other
species of Amazonian Saguinus; for example, S. fuscicol-
lis showed a group size range of two to eight individuals
(Freese, 1975; Soini, 1981; Janson and Terborgh, 1985).

During the first month of censuses, 75% of the S. inustus
sightings were in secondary forest, while in the second and
third months the situation reversed, with 70% and 62.5%
of the sightings in primary terra firme forest. During the
last month of surveys the proportion of sightings of the
species was similar for both types of forest (53.8% pri-
mary vs. 46.2% secondary). The preference for secondary
forest during the first month of surveys may be a result
of higher fruit availability of various species of Inga in the
rastrojos. The sweet arils of Inga have been noted as one of
the most consumed resources by the mottled-face tamarin
(Palacios et al., 2004). S. inustus may show resource use
patterns similar to other species of Saguinus; for example,
S.fuscicollis usually forages on one or a few species of plants
during consecutive days until no more fruits are available
(Defler, 2003a). This may be the case with Inga fruits; other
primates such as red howlers also concentrate their forag-
ing efforts in particular Inga fruit patches until crops are
depleted (Palacios, unpublished data).

Based on occasional observations, Defler (2003a) suggest-
ed the possibility that S. inustus could be more abundant
in secondary forests near indigenous settlements than in
primary forests. Snowdon and Soini (1988) reported that
some species of Saguinus, among them S. .... attain
higher densities in secondary forests. Palacios et al. (2004)
observed the presence of S. inustus in both types of forests;
Defler (2003a) believes that S. ... .. may have the same
habitat preferences, and that S.fuscicollis seems to be the spe-
cies of Saguinus with the more diverse habitat use, as this
species uses primary forests as well as highly disturbed ones.
S. inustus at the Caqueti-Apaporis interfluvium used an
approximately equal proportion of primary and secondary
forest (51.16% and 48.8% respectively). Fourteen percent of
the sightings of S. inustus in primary forest corresponded to
sabana capotuda habitat with characteristics that this species
usually prefers; in a different study related to the ecology of
the species, S. inustus regularly used portions of forest with
dense understory (Castillo-Ayala, unpublished data). Fur-
thermore, 85.7% of the encounters with groups of S. inustus


in secondary forest corresponded to rastrojo alto with a very
dense understory. These preferences have been reported for
other species of Saguinus; for example, Emmons and Feer
(1999) mention that S. fuscicollis, S. .... and S. bicolor
often can be seen in habitats with high densities of lianas.

This first density estimate of S. inustus provides important
data, but supplemental information from other areas of
the Caqueti-Apaporis interfluvium will be necessary in
order to assess the conservation status of the species in this
region. The forests around the community of Loma Linda
still offer appropriate habitats for the conservation of the
species, including secondary forests at different succes-
sional stages, and a large proportion of primary forest. The
forest matrix in the lower Caqueti and Apaporis interflu-
vium corresponds mainly to indigenous reserves (Palacios
et al., 2004), which support a large indigenous population
that is increasing due to high birth and immigration rates.
As a consequence, the need for new housing and croplands
will continue to increase, transforming significant areas of
primary forest. New surveys and ongoing studies on the
ecology of the mottled-face tamarin will contribute to a
better knowledge of its density in the Caqueti-Apaporis
interfluvium, and will provide more data to help determine
their forest type preferences, how they cope with habitat
transformation, and the conservation strategies that need
to be implemented with local communities to preserve this
interesting primate.

Acknowledgements

Thanks to Conservation International-Colombia and the
Margot Marsh Biodiversity Foundation for funding the
field work. We also thank Angel Yucuna, chief of Loma
Linda indigenous community for facilitating logistical sup-
port. Nolberto Neira, Oscar Yucuna "Turf", Jos6 Angel
Rodriguez Macuna, Jarviz Rodriguez, Elisban Rodriguez,
Benedicto Neira and Enesilda Yucuna helped in conduct-
ing the censuses.

Claudia Idaly Castillo-Ayala, Conservation International
Colombia, Cra. 13 No. 71 41, Bogoti, Colombia, e-mail:
and Erwin Palacios, Conservation
International-Colombia and Estaci6n Biol6gica Capard,
e-mail: .

References

Barnett, A., Borges, S., Castilho, C., Neri, E and Shapley,
R. 2002. Primates of the Jad National Park, Amazonas,
Brazil. Neotrop. Primates 10(2): 65-70.
Cardoso da Silva, J.M. and Conway, D. 1996. Application
of parsimony analysis of endemicity in Amazonian bio-
geography: An example with primates. Biol. J. Linnaean
Soc. 59: 427-437.
CITES. 2001. Lista de species. Una referencia a los Ap6n-
dices de la Convenci6n sobre el Comercio Internacio-
nal de Especies Amenazadas de Fauna y Flora Silvestres.





Neotropical Primates 14(3), December 2007


Secretaria de la CITES/PNUMA Centro de Monitoreo
de la Conservaci6n Mundial. Unwin Brothers, Martins
Printing Group, Old Woking, Surrey. APENDICES I,
II y III adoptados en la 1 la Conferencia de las Partes y
vigentes a partir del 18 de septiembre de 1997 versionn
corregida: agosto de 2002).
De Souza, L., Queiroz, H.L. and Ayres, J.M. 2004. The
mottled-face tamarin, Saguinus inustus, in the Amand
Sustainable Development Reserve, Amazonas, Brazil.
Neotrop. Primates 12(3): 121-122.
Defler, T. R. 2003a. Primates de Colombia. Serie de Guias
Tropicales de Campo. Conservaci6n Internacional Co-
lombia, Bogoti.
Defler, T. R. 2003b. Densidad de species y organizaci6n es-
pacial de una comunidad de primates: Estaci6n Biol6gica
Capard, Departamento del Vaup5s, Colombia. In: Prima-
tologia delNuevo Mundo, V. Pereira, E Nassar and A. Savage
(eds.), pp.21-37. Fundaci6n Araguatos, Bogota D.C.
Freese, C. 1975. A census of non-human primates in Peru.
In: Primate Censusing Studies in Peru and Colombia.
Report to the National Academy of Sciences on Project
Amro-0719. Pan American Health Organization, Wash-
ington, DC.
Freese, C.H., Heltne, P. G., Castro, R.N. and Whitesides,
H. 1982. Patterns and determinants of monkey densities
in Peru and Bolivia, with notes on distributions. Int. J.
Primatol. 3: 53-90.
Hershkovitz, P. 1977. Living New World Monkeys (Platyr-
rhini) with an Introduction to Primates, Vol. 1. The Uni-
versity of Chicago Press, Chicago.
Heymann, E.W, Encarnaci6n, F and Canaquin, J.E.
2002. Primates of the Rio Curaray, northern Peruvian
Amazon. Int. J. Primatol. 23(1): 191-201.
Janson, C.H. andTerborgh, J.W 1985. Censando primates
en el bosque lluvioso con referencia a la Estaci6n Biol6gi-
ca de Cocha Cashu, Parque Nacional del Mand, Perd. In:
Report Mand, M.A. Rios (ed.). Centro de Datos para la
Conservaci6n, Universidad Nacional Agraria La Molina,
Lima.
Mittermeier, R.A., Goettsch, C., Robles, P., Pilgrim, J.,
Fonseca, G.A.B. da, Brooks, T. and Konstant, W.R.
2002. Areas Silvestres: Las Ultimas Regiones V . del
Mundo. Conservation International y Agrupaci6n Sierra
Madre, M6xico D. F.
NRC (National Research Council). 1981. Techniques for
the Study of Primate Population Ecology. National Acad-
emy Press, Washington, DC.
Palacios, E., Alarc6n, G. and Rodriguez, A. 2003. Densida-
des de Vertebrados y Patrones de Caceria en el Suroriente
de la Amazonia Colombiana. Informe final a la Funda-
ci6n para la Promoci6n de la Investigaci6n y la Tecnolo-
gia del Banco de la Repdblica, Bogoti D.C.
Palacios, E., Rodriguez, A. and Castillo, C. 2004. Prelimi-
nary observations on the mottled-face tamarin (Saguinus
inustus) on the lower Rio Caqueti, Colombian Amazo-
nia. Neotrop. Primates 12(3): 123-126.
Palacios, E. and Peres, C.A. 2005. Primate population
densities in three nutrient-poor Amazonian terra firme


forests of Southeastern Colombia. Folia Primatol. 76:
135-145.
Peres, C.A. 1997. Primate community structure at twenty
western Amazonian flooded and unflooded forests.
J. Trop. Ecol. 13: 381-405.
Peres, C.A. 1999. General guidelines for standardizing
line-transect surveys of tropical forest primates. Neotrop.
Primates 7(1): 11-16.
Pook, A.G. and Pook, G. 1982. Polyspecific association
between Saguinus fuscicollis, Saguinus labiatus, Callimico
goeldii and other primates in north-western Bolivia. Folia
Primatol. 38: 196-216.
Rylands, A.B., Schneider, H., Langguth, A., Mittermeier,
R.A., Groves, C. P. and Rodriguez-Luna, E. 2000. An as-
sessment of the diversity of New World primates. Neotrop.
Primates 8(2): 61-93.
Soini, P. 1981. Informe de Pacaya no. 4: Ecologia y dinami-
ca poblacional del pichico Saguinusfuscicollis (Primates,
Callitrichidae). Unpublished report.
Snowdon, C.T. and Soini, P. 1988. The tamarins, genus Sa-
guinus. In: Ecology and Behaviour of Neotropical Primates,
Vol. 2, R.A. Mittermeier, A.B. Rylands, A. Coimbra-
Filho and G.A. B. da Fonseca (eds.), pp.223-298. World
Wildlife Fund-US, Washington, DC.
Terborgh, J. 1983. Five New World Primates: A Study in
Comparative Ecology. Princeton University Press, Princ-
eton, New Jersey.
Thomas, L., Laake, J. L., Strindberg, S., Marques, E. E. C.,
Buckland, S.T., Borchers, D. L., Anderson, D. R., Burn-
ham, K.P., Hedley, S.L., Pollard, J.H., Bishop, J.R.B.
and Marques, T.A. 2005. Distance 5.0. Release "x"1. Re-
search Unit for Wildlife Population Assessment, Univer-
sity of St. Andrews, UK.


NEW OCCURRENCE RECORDS AND EASTERN
EXTENSION TO THE RANGE OF CALLICEBUS
CINERASCENS (PRIMATES, PITHECIIDAE)

Mauricio de Almeida Noronha
Wilson Roberto Spironello
Dayse Campista Ferreira

Introduction

Spix (1823) first described the ashy black titi monkey
(Callicebus cinerascens) from a male specimen assumed to
have been collected along the Rio Ia near the border with
Peru, in the state of Amazonas, Brazil. Van Roosmalen
and colleagues (2002) questioned the origin of this speci-
men, maintaining that as all subsequent records were for
the right bank of the Rio Madeira (Rylands, 1982; Her-
shkovitz, 1990; van Roosmalen et al., 2002), the type lo-
cality must be incorrect. During his taxonomic revision
of the genus Callicebus, Hershkovitz (1990) added three
valid localities for C. cinerascens, one on the right bank of
the Rio Aripuana, and two on the right bank of the Rio
Roosevelt. Rylands (1982) observed the species along the





Neotropical Primates 14(3), December 2007


right bank of the Rio Aripuana, and van Roosmalen et al.
(2002) included new records from the right banks of the
Rios Aripuana and Madeira and the left banks of the Rios
Arara and Canuma.

In their taxonomic revision of the genus Callicebus, van
Roosmalen et al. (2002) predicted that C. cinerascens would
only extend as far east as the left bank of the Rio Sucun-
duri. They indicated that possibly C. I/offats'.,, or anoth-
er yet-to-be-described species of titi monkey, would occupy
the Rio Canuma interfluve delineated by its tributaries, the
Rios Sucunduri and Abacaxis. Hershkovitz (1963, 1988,
1990; in Silva Jr. and Noronha, 2000) suggested that
C. Ioftfiait, extends south of the Rio Parand do Urarid
and along the right bank of the Rio Canuma. These range
predictions have yet to be tested, and the exact range of


this genus in the interfluve between the Rios Madeira and
Tapaj6s remains unknown (Silva Jr. and Noronha, 2000).
The objective of this study is to refine the range map for
the ashy black titi monkey, based on the literature and new
occurrence records from field surveys.

Materials and Methods

Occurrence data in the present study are based on a literature
review and two field excursions. During the first expedition,
between January and May of 2001, we surveyed the inter-
fluve between the Rios Madeira and Tapaj6s, specifically the
region of the Rios Mau5s, Abacaxis and Sucunduri. In the
second, in June and July of 2006, we surveyed the interfluve
between the Rios Aripuana and Juruena. This second excur-
sion formed part of the Juruena-Apui Expedition. During


Figure 1. Geographic range of (,:.. /.,, dnerascens, based on Hershkovitz (1990), Rylands (1982), van Roosmalen et al. (2002) and
this study: (1) Prainha, right bank of the Rio Aripuana, Amazonas; (2) Sao Joao and (3) Otoho, right bank of the Rio Roosevelt, Mato
Grosso; records for the species from the following locations on the right bank of the Rio Aripuana, Amazonas: (4) Cipotuba (05o48'23"S,
60l12'76"W), east bank of Lago Cipotuba; (5) Prainha (0545'S, 60l12'W), Igarap6 Prainha; (6) Sao Joao (05028'S, 6022'W), Igarap6
Terra Preta; and along the right bank of the Rio Madeira, Amazonas; (7) around the town of Novo Aripuana (0507'08"S, 6022'45"W);
(8) left bank of the Rio Arara (05l12'S, 60004'W), 40 km east ofNovo Aripuana; (9) around the town of Borba (04o22'S, 59035'W); (10)
left bank of the Rio Canuma; (11) Humboldt Pioneer Nucleus (1010'S, 59027'W), on the right bank of the Rio Aripuana, Mato Grosso;
right bank of the Rio Sucunduri, Amazonas; (12) BR230 (0646'S, 59000'W); (13) Vila de Sucunduri (0648'S, 59004'W); (14) 06o42'S,
59003'W; (15) 05o44'S 59022'W; (16) 05o30'S, 59028'W; (17) 05025'S, 59041'W; (18) source of Igarap6 Surubim (06053'S, 5903'W);
left bank of the Rio Sucunduri, Amazonas; (19) left bank of the Rio Tapaj6s (06034'S, 58024'W); (20) left bank of the Rio Tapaj6s
(06034'S, 58035'W); (21) Vicinal do Coruja (07038'S, 59049'W), Floresta Nacional do Jatuarana; (22) Serra do Sucunduri (08050'S,
59008'W), Floresta Estadual do Sucunduri; (23) right bank of the Rio Bararati (08021'S, 58037'W), Parque Estadual do Sucunduri; and
(24) right bank of the Rio Juma (06042'S, 59035'W).


Occurcucc records of
Callicebus cinerncews


* Odr studies





Neotropical Primates 14(3), December 2007


these surveys, we identified the ashy black titi monkey
using both the diagnostic characters defined by Hershkovitz
(1990) and material from the collection at the National In-
stitute of Amazonian Research (INPA 4085).

Results and Discussion

During both trips we observed C. cinerascens repeatedly
along the banks of the Rios Sucunduri and Abacaxis, close
to the left bank of the Rio Tapaj6s and the right bank of the
Rio Bararati (Fig. 1). All observations were in made in terra
firme, campinarana or secondary forests. Individuals were
frequently observed in relatively open areas of young sec-
ondary growth, which may indicate a degree of flexibility
in habitat use by this species. These new occurrence records
extend the eastern limit of C. cinerascens' range beyond that
proposed by van Roosmalen and colleagues (2002). We
now predict that this species' range should extend north to
the Rio Parand do Urarid, east to the left bank of the Rio
Abacaxis and the left bank of the upper Rio Tapaj6s, west
as far as the right bank of the Rio Madeira, and south to
the corridor formed between the Rios Aripuana-Roosevelt
and Tapaj6s-Juruena, in the states of Amazonas and Mato
Grosso. The most southerly record is Otoho on the right
bank of the Rio Roosevelt in Mato Grosso (Fig. 1).

During this study we found no overlap between the range
of C. cinerascens range and that of any other species of
Callicebus, suggesting that this species is parapatric with
its sister taxa, C. hIofft,/wa' C. baptista and C bernhardi.
While interviewing a resident of a community on the left
bank of the Rio Tapaj6s (0634'S, 5828'W), near the Rio
Palmares in the municipality of Mau5s, Amazonas State,
we discovered that a gray titi monkey with light spots
on its throat occurs in the area. It is possible that this is
C. ho'fft,/'asu. (van Roosmalen etal., 2002) and that the Rio
Palmares represents the eastern limit for C. cinerascens and
serves as a point of contact between the two species. In ad-
dition to improving the precision of C. cinerascens' range,
this study also enabled us to determine in which protected
areas it occurs. In the state of Amazonas, C cinerascens is
present in the Floresta Nacional do Jatuarana (837,100 ha),
the Parque Nacional do Juruena (2,002,565 ha), the Flo-
resta Estadual do Sucunduri (492,905 ha), and the Parque
Estadual do Sucunduri (808,312 ha). Its range also en-
compasses the Floresta Estadual de Apui (185,946 ha),
the Reserva de Desenvolvimento Sustentivel Bararati
(113,606 ha), the Parque Estadual do Guariba (72,296 ha),
the Reserva Extrativista do Guariba (150,465 ha), the Flo-
resta Estadual do Aripuand (336,040 ha), the Reserva de
Desenvolvimento Sustentivel do Juma (589,611 ha), the
Parque dos Campos Amaz6nicos (873,570 ha), the Flores-
ta Estadual de Manicor6 (83,381 ha) and the Reserva de
Desenvolvimento Sustentivel Aripuand (224,291 ha). In
Mato Grosso, it is expected to occur in the Reserva Extrati-
vista Guariba Roosevelt (57,630 ha), the Estagao Ecol6gica
do Rio Roosevelt (27,860 ha), and the Parque Estadual Iga-
rap5s do Juruena (227,800 ha).


Acknowledgements

We thank the Fundacao 0 Boticirio de Protegao a Natur-
eza for supporting the fieldwork undertaken in the lower
Madeira-Tapaj6s interfluve. The Juruena-Apui Expedition
sponsors (World Wildlife Fund Brazil, the Instituto Bra-
sileiro de Meio Ambiente e Recursos Naturais Renoviveis
and the Secretaria de Estado de Meio Ambiente e Desen-
volvimento Sustentivel do Amazonas) supported fieldwork
in the upper Aripuana-Juruena interfluve.

Mauricio de Almeida Noronha, Rua dos Jatobis, 142, Co-
roado III, Manaus, Amazonas 69085-380, Brasil, e-mail:
, Wilson Roberto Spironello,
Institute Nacional de Pesquisas da Amaz6nia (INPA), Co-
ordenacao de Pesquisas em Silvicultura Tropical, CP 478,
Manaus, Amazonas 69060-001, Brasil, e-mail: inpa.gov.br> and Dayse Campista Ferreira, Rua dos Ja-
tobis, 142, Coroado III, Manaus, Amazonas 69085-380,
Brasil, e-mail: .

References

Hershkovitz, P 1963. A systematic and zoogeographic account
of the monkeys of the genus Callicebus (Cebidae) of Amazo-
nas and Orinoco river basins. Mammalia 27(1): 1-79.
Hershkovitz, P. 1988. Origin, speciation and distribu-
tion of South American titi monkeys, genus Callicebus
(Family Cebidae, Platyrrhini). Proc. Acad. Natl. Sci.
Philad. 140(1): 240-272.
Hershkovitz, P. 1990. Titis, New World monkeys of the
genus Callicebus (Cebidae, Platyrrhini): A preliminary
taxonomic review. Fieldiana, Zoology, New Series (55):
1-109.
Noronha, M.A. 2004. Estado atual de conservacao e distribui-
cao geografica Mico saterei Silva Jr. e Noronha, M.A. 1998
(Primates: Callitrichidae), na Amaz6nia Central, Brasil. Dis-
sertanyo de Mestrado, Instituto de Florestas, Universidade
Federal Rural do Rio de Janeiro, Rio de Janeiro.
Rylands, A.B. 1982. The behaviour and ecology of three
species of marmosets and tamarins (Callitrichidae, Pri-
mates) in Brazil. Doctoral thesis, University of Cam-
bridge, Cambridge.
Silva Jdnior, J. de S. and Noronha, M.A. 2000. Resulta-
do de uma pequena expedigao primatol6gica a Amaz6-
nia Central (Primates: Platyrrhini). In: A Primatologia no
Brasil- 7, C. Alonso and A. Langguth (eds.). Sociedade
Brasileira de Primatologia, Jodo Pessoa.
Spix, J. 1823. Simiarum et Vespertilionum Brasiliensium
Species Novae ou Histoire Naturelle des Especes Nouvelles
Pendant le Voyage dans l'Interieur du Bresil. Typis Francisci
Seraphici Hubschmanni, Monachii.
Van Roosmalen, M. G. M, Van Roosmalen, T. and Mitter-
meier, R.A. 2002. A taxonomic review of the titi mon-
keys, genus Callicebus Thomas, 1903, with the description
of two new species, Callicebus bernhardi and Callicebus
stephennashi, from Brazilian Amazonia. Neotrop. Primates
10(Supp.): 1-53.





Neotropical Primates 14(3), December 2007


NEW OCCURRENCE RECORDS OF MICO
ACARIENSIS (PRIMATES, CALLITRICHIDAE)

Mauricio de Almeida Noronha
Jose de Sousa e Silva Jfnior
Wilson Roberto Sp.: ouello
Dayse Campista Ferreira

The Rio Acari marmoset (Mico acariensis) was described by
van Roosmalen et al. (2000). The holotype was originally
being kept as a pet by inhabitants of a small settlement near
the Rio Acari, in Central Amazonia, Brazil. A specimen was
collected and deposited in the vertebrate collection of the
National Institute of Amazonian Research (INPA 3931)
(van Roosmalen et al., 2000). The new species was clas-
sified in the C .-'. argentata group sensu Hershkovitz
(1977) and Vivo (1988, 1991), and was associated with
the bare-eared marmosets Mico saterei and M. melanurus.
Diagnostic characters include bright orange coloration of
the lower back, body underparts, legs and tail base (the
rest of the tail is black); upper parts are almost all white;
the white chest contrasts with a partly black muzzle; the
narrow triangular nose patch and ocular rings are black and


dark pigmented ears partially covered with white hairs (van
Roosmalen et al., 2000). According to van Roosmalen et al.
(2000), the type locality is a small settlement on the right
bank of the lower Rio Acari (05007'08"S, 60001'14"W),
close to the confluence of the Rios Canuma and Sucunduri
in the state ofAmazonas, Brazil. Based on distribution pat-
terns of marmosets in the Amazon region, these authors
predicted that the species would occupy the entire Acari-
Sucunduri interfluvium, probably extending to somewhere
between the Rios Aripuana and Juruena, forming a contact
zone with Mico melanurus.

During a recent field expedition (Noronha, 2004) to the
lower Madeira-Tapaj6s interfluvium, marmosets with the
same diagnostic characters were observed at three locations
along the left bank of the Rio Sucunduri. Four groups were
observed at the Vila de Sucunduri (0648'S, 59004'W),
and three specimens were obtained from local inhabitants
and deposited in the collection of Museu Paraense Emilio
Goeldi (MPEG 36085, 36086, 36087). Other troops
were also recorded close to the Igarapd Surubim (0654'S,
59003'W) and the Igarapd do Liso (0717'S, 5850'W).
These new records partially confirm the range proposed
by van Roosmalen and colleagues (Fig. 1). Information


Figure 1. The range of Mico acariensis based on van Roosmalen et al. (2000) and records from this study: 1. Type locality; 2. Vila de
Sucunduri; 3. Rio Sucunduri, at the mouth of the Igarap6 Surubim and 4. Igarap6 do Liso.


Occunence records of
Mi co acariensis
o This study
* Roosmalen et at. (2000)





Neotropical Primates 14(3), December 2007


obtained during interviews with the ex-inhabitants of an
abandoned village near the Igarapd do Urucd (a left affluent
of the Rio Sucunduri, along the Serra do Sucunduri) indi-
cates that M. acariensis and another species of marmoset
with blackish hairs occur in the area. As M. melanurus has
been confirmed as occurring in the Sucunduri Mountains
(Noronha, unpubl. data), it is possible that these species are
sympatric in this region.


Acknowledgements


SLEEP PARAMETERS IN CAPTIVE FEMALE OWL
MONKEY (AOTUS) HYBRIDS

Sachi Sri Kantha
Juri Suzuki
Yuriko Hirai
Hirohisa Hirai


Introduction


This study was supported by the Fundagao 0 Boticirio
de Protegao a Natureza, and the Juruena-Apui Expedition
(funded by the World Wildlife Fund- Brazil (WWF), the
Institute Brasileiro de Meio Ambiente e Recursos Natu-
rais Renoviveis (IBAMA) and the Secretaria de Estado
de Meio Ambiente e Desenvolvimento Sustentivel do
Amazonas).

Mauricio de Almeida Noronha, Rua dos Jatobis, 142,
69085-380, Coroado III, Manaus, Amazonas, Brazil,
e-mail: , Jos6 de Sousa e Silva
Junior, Museu Paraense Emilio Goeldi, Coordenacao de
Zoologia, CP 399, 66040-170, Belkm, PA, Brazil, e-mail:
, Wilson Roberto Spironello,
Institute Nacional de Pesquisas da Amaz6nia, Coorde-
nacao de Pesquisas em Silvicultura Tropical, CP 478,
69060-001, Manaus, AM, Brazil, e-mail: gov.br> and Dayse Campista Ferreira, Rua dos Jatobis,
142, 69085-380, Coroado III, Manaus, Amazonas, Brazil,
e-mail: .

References

Hershkovitz, P. 1977. Living New World Monkeys (Platyr-
rhini) with an Introduction to Primates, Vol. 1. The Uni-
versity of Chicago Press, Chicago.
Noronha, M.A. 2004. Estado atual de conservagno e dis-
tribuigao geografica Mico saterei Silva Jr. and Noronha,
M.A. 1998 (Primates: Callitrichidae), na Amaz6nia
Central, Brasil. Master's thesis, Instituto de Florestas,
Universidade Federal Rural do Rio de Janeiro, Rio de
Janeiro.
Van Roosmalen, M.G.M., Van Roosmalen, T., Mitter-
meier, R.A. and Rylands, A. B. 2000. Two new species of
marmoset, genus C .-' Erxleben, 1777 (Callithichi-
dae, Primates) from the Tapaj6s/Madeira interfluvium,
South Central Amazonia, Brazil. Neotrop. Primates 8(1):
2-18.
Vivo, M. de. 1988. Sistemitica de C .- Erxleben,
1777. Doctoral dissertation, Universidade de Sao Paulo,
Sao Paulo.
Vivo, M. de. 1991. Taxonomia de C .- Erxleben,
1777 (Callitrichidae, Primates). Fundagao Biodiversitas,
Belo Horizonte, Minas Gerais, Brasil.


In the 1970s and 1980s, captive breeding of owl monkeys
began in countries such as the United States of America
(Cicmanec and Campbell, 1977; Weller et al., 1991; Malaga
et al., 1997), Peru (Gozalo and Montoya, 1990) and Ger-
many (Rappold and Erkert, 1994). In 1977, a compara-
tively smaller owl monkey colony was established in Japan,
at the Primate Research Institute facility of Kyoto Uni-
versity, with founding members originating from Bolivia.
Unfortunately, at that time, the production of hybrids oc-
curred due to inadvertent pairing of different owl monkey
species before the existence of multiple Aotus species had
been determined (Hershkovitz, 1983; Ford, 1994; Groves,
2001). Extreme chromosomal diversity with diploid counts
ranging from 46 to 56 is one distinguishing feature of owl
monkeys, apart from their nocturnality (Ma et al., 1977;
Yunis et al., 1977; Reumer and de Boer, 1980; Simpson
and Jones, 1982). Previous studies on owl monkey hybrids
suggest that while the adult female hybrid monkeys may
sometimes conceive although at lower rates compared to
normal individuals adult male hybrid owl monkeys are
most probably sterile (Ma et al., 1977; Yunis et al., 1977;
Reumer and de Boer, 1980; Simpson and Jones, 1982).

Rigorous sleep quantification data exist for less than 10% of
extant primate species (Campbell and Tobler, 1984). Since
owl monkeys (1) are unique among platyrrhines for their
nocturnal behavior, (2) are notable for their strictly ar-
boreal habitat, and (3) use holes and platforms in lodge
trees as their sleep sites, sleep quantification in the wild
has remained a virtually impossible challenge. Under cap-
tive conditions owl monkey sleep has been recorded previ-
ously for A. trivirgatus (Perachio, 1971) and A. azarae (Sri
Kantha and Suzuki, 2006; Suzuki and Sri Kantha, 2006).
The objective of this study was to quantify the parameters
for sleeping behavior activity among captive-born owl
monkey hybrids.

Methods

Four female owl monkey hybrid siblings (age range
11-16 yrs; weight range 1.016-1.163 kg) and three
female owl monkey purebreds, including a mother and
two of her progeny (age range 6-16 years; weight range
1.050-1.079 kg) reared at Kyoto University's Primate
Research Institute (PRI), were the subjects of this study.
The founding members of the owl monkey colony, born
in the mid-1970s, originated from Bolivia. These seven





Neotropical Primates 14(3), December 2007


monkeys were housed in individual stainless steel cages
(100 x 70 x 60 cm). The Aotus colony room was maintained
on a shifted, alternating 12 hr light (2300-1100 hrs:
200 lux): 12 hr dark (1100-2300 hrs: 0.01-0.5 lux) cycle.
Lighting conditions of the room were routinely checked by
an illuminance meter (TopCon IM-5, Tokyo). Food and
water were available to the monkeys ad libitum, and the
commercial pellet diet for New World monkeys (25.1 g
protein and 10.6 g lipid/100 g diet) was supplemented daily
with fresh fruits and twice-weekly with mealworms. All
experiments were carried out with approval from the Re-
search Committee of the Institute, and according to the
Primate Research Institute's Guidelines for the Care and
Use of Laboratory Primates.

Quantification of the monkeys' sleep behavior activity was
carried out by actigraphy (Actiwatch AW-64, Mini Mitter
Co., Bend, Oregon, USA) for 12 consecutive days, as de-
scribed previously (Sri Kantha and Suzuki, 2006; Suzuki
and Sri Kantha, 2006). In brief, the following definitions
were applied as per the Actiwatch manufacturer's instruc-
tions: (1) Activity count: an instrument-specific arbitrary
unit (AU) quantifying primate activity, computed from
any omni-directional motion made by the caged monkey.
Though this count is not suitable for determining the abso-
lute activity of the monkey in concrete terms, it is helpful
in evaluating comparative activity patterns among the mon-
keys wearing the Actiwatches from the same commercial
supplier. (2) Total sleep time (TST): the cumulative count
of time, as measured in minutes in a continuous 24-hour
circadian cycle, that was recorded as sleep. As per the al-
gorithm used in the instrument, based on a one-minute
sampling epoch, activity counts of 0.40 were recorded as a
wake epoch, and activity counts below this threshold were
recorded as a sleep epoch. (3) Sleep episode length (SEL):
the mean length of blocks of continuous sleep, measured in
minutes, falling between two waking bouts, in a 12 h light
phase of the 24 h circadian cycle.

The weight of the Actiwatch was only 17 g (approximately
one-sixtieth of an owl monkey's body weight) and there
were few if any signs of discomfort due to its presence


around the monkey's neck. Karyotype analysis was per-
formed as previously reported by Hirai and colleagues
(1998). Data were analyzed by a two-tailed Student's t-test
for independent means for any significant differences. Sta-
tistical computations were performed using STATISTICA
software (StatSoft, Inc., Oklahoma, USA).

Results

The female parent of these sibling monkeys belonged to
A. azarae type (2n= 50), and the male parent was of un-
known lineage (2n= 53). The karyotype maps of the now-
deceased male parent A14 (2n = 53) have already been pub-
lished (Nagao et al., 2005). Based on the varying karyotype
profiles (with diploid numbers 51, 52 and 53) in four of
the monkeys in our study and the affiliated taxon data
available for owl monkeys (Ford, 1994), these first-genera-
tion captive-bred females were confirmed as Aotus hybrids.
Among these four hybrid females, A40 was an outlier, since
karyotype analysis demonstrated that this monkey car-
ried a trisomic condition for its X-chromosomes (data not
shown). Though this monkey remains healthy, certain be-
havioral and physiological differences from the other group
members were observed, such as excessive tear formation in
the eyes and agitated vocalizations.

Quantified sleep behavior activity data for each of the four
Aotus hybrids, for 12 consecutive days, are presented in
Table 1. Due to its trisomic condition for X-chromosomes,
the Aotus hybrid 40 monkey's activity-behavioral sleep pa-
rameters are of some interest. We recorded the lowest daily
activity amount in this trisomic monkey (103 + 34 AU)
and the shortest SEL/12 h light phase (13+ 5 min) com-
pared to the other three non-trisomic hybrid monkeys, in-
dicating that it may be partially suffering from lethargy and
discontinuous sleep phases. The mean SEL of the trisomic
hybrid monkey significantly differs from the mean SEL
(27+ 13 min) of non-trisomic hybrid monkeys (p < 0.01).
Table 2 provides a statistical comparison of group mean
variation in behavioral sleep parameters for non-trisomic
hybrid and purebred monkeys. Both the TST/24 h and
SEL/12 h light phase differed significantly (p<0.01)


Table 1. Measured behavioral sleep-activity parameters in the hybrid owl monkey subjects'.
Owl Monkey Behavioral Sleep Activity
ID number1 and sex TST/24 h2 SEL/12 h light phase3 Mean Activity Counts
(min) (min) (arbitrary units)
Non-trisomic
370 618+187 23+8 159+108
39$ 829+92 40+12 133+49
41 734+64 18+5 121+49
Trisomic
40 Y 730+196 13+5 103+34
1 Owl monkeys 37, 39, 40 and 41 are siblings, born to wild-born parents of the founder colony.
2Total Sleep Time; based on 12 consecutive days of data acquisition.
3 Sleep Episode Length, determined during the monkey's quiescent (light) phase.





Neotropical Primates 14(3), December 2007


Table 2. Comparison of group mean variation in behavioral sleep parameters for owl monkey non-trisomic hybrids and purebreds.
Owl Monkeysb
Parameter t-test (p)
Non-trisomic Hybrids Purebreds
n 3 3
age range (yr) 11-16 6-16
TST/24 h (min)a 727+150 591+82 <0.01, df 70
SEL/12 h light phase (min)a 27+13 51+36 <0.01, df 70
a Mean+SD.
bAll monkeys are females.


between the two groups, with the hybrid individuals regis-
tering a higher TST/24 h and a shorter SEL compared to
the pure breds.

Discussion

One of the females in our study (ID number 40) carries an
X chromosome trisomy, detected from karyotype analysis.
In the absence of published information on the sleep pro-
files of Aotus hybrids, or trisomic Aotus, the marked varia-
tion in SEL obtained for the trisomic Aotus hybrid monkey
is a novel finding. Studies on trisomy among nonhuman
primates have been understandably meager, partly due to
a very low survival rate of individuals with chromosomal
anomalies (Ruppenthal et al., 2004). Nevertheless, the
prevalence of significant sleep disturbances among humans
suffering from autosomal trisomic conditions (Ellingson
and Peters, 1980; Shaffer et al., 1996; Ruppenthal et al.,
2004; Segel et al., 2006) provide some clue to the unusual-
ly varied behavioral sleep profile recorded for this trisomic
Aotus hybrid monkey. To conclude, we report significant
differences in the TST and SEL parameters between the
purebred owl monkeys and the non-trisomic hybrid owl
monkeys. In addition, similar to trisomic humans who
suffer from sleep irregularities, the SEL and activity data
obtained in a trisomic hybrid owl monkey provide indi-
rect evidence to its behavioral irregularity in comparison to
non-trisomic hybrid owl monkeys.

Acknowledgements

We acknowledge the technical assistance provided by
Nobuko Matsubayashi and Norihiko Maeda of the Center
for Human Evolution Modeling Research, Primate Re-
search Institute, Kyoto University.

Sachi Sri Kantha, Section of Pharmaceutical English, Gifu
Pharmaceutical University, 5-6-1 Mitahora-higashi, Gifu
502-8585, Japan, e-mail: , Juri
Suzuki, Center for Human Evolution Modeling Research,
Kyoto University Primate Research Institute, Inuyama City
484-8506, Japan, and Yuriko Hirai and Hirohisa Hirai,
Molecular Biology Section, Dept of Cellular and Molecu-
lar Biology, Kyoto University Primate Research Institute,
Inuyama City 484-8506, Japan.


References

Campbell, S.S. and Tobler, I. 1984. Animal sleep: A review
of sleep duration across phylogeny. Neurosci. Biobehav.
Rev. 8: 269-300.
Cicmanec, J. C. and Campbell, A. K. 1977. Breeding the
owl monkey (Aotus trivirgatus) in a laboratory environ-
ment. Lab. Anim. Sci. 27: 512-517.
Ellingson, R.J. and Peters, J. E 1980. Development of EEG
and daytime sleep patterns in trisomy-21 infants during
the first year of life; longitudinal observations. Electroen-
ceph. Clin. Neurophysiol. 50: 457-466.
Ford, S.M. 1994. Taxonomy and distribution of the
owl monkey. In: Aotus: The Owl Monkey, J. E Baer,
R.E.Weller and I. Kakoma (eds.), pp.1-57. Academic
Press, San Diego.
Gozalo, A. and Montoya, E. 1990. Reproduction of the
owl monkey (Aotus nancymai) in captivity. Am. J. Prima-
tol. 21: 61-68.
Groves, C. 2001. Primate Taxonomy. Smithsonian Institu-
tion Press, Washington, DC.
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.
Hirai, H., Hasegawa, Y., Kawamoto, Y. and Tokita, E.
1998. Tandem duplication of nucleolus organizer region
(NOR) in the Japanese macaque, Macacafuscatafuscata.
Chromo. Res. 6: 191-197.
Ma, N. S. E, Jones, T. C., Bedard, M.T., Miller, A., Morgan,
L. and Adams, E. 1977. The chromosome complement of
an Aotus hybrid. J. Hered. 68: 409-412.
Nagao, K., Takenaka, N., Hirai, M. and Kawamura, S.
2005. Coupling and decoupling of evolutionary mode
between X- and Y-chromosomal red-green opsin genes in
owl monkeys. Gene 352: 82-91.
Perachio, A.A. 1971. Sleep in the nocturnal primate, Aotus
trivirgatus. In: Proceedings of the Third International Con-
gress ofP '. .-. '.: i. Vol. 2, J. Biegert and W. Leutenegger
(eds.), pp. 54-60. Karger, Basel.
Rappold, I. and Erkert, H. G. 1994. Re-entrainment,
phase-response and range of entrainment of circadian
rhythms in owl monkeys (Aotus lemurinus) of different
age. Biol. Rhythm. Res. 25: 133-152.
Reumer, J. W. E and de Boer, L. E. M. 1980. Standardization
of Aotus chromosome nomenclature, with descriptions





Neotropical Primates 14(3), December 2007


of the 2n = 49-50 karyotype and that of a new hybrid.
J Human Evol. 9: 461-482.
Ruppenthal, G. C., Moore, C.M., Best, R. G., Walker-Ge-
latt, C.G., Delio, P.J. and Sackett, G.P. 2004. Trisomy
16 in a pigtailed macaque (M. nemestrina) with multiple
anomalies and developmental delays. Am. J Ment. Retar-
dation 109: 9-20.
Segel, R., Peter, I., Demmer, L.A., Cowan, J.M., Hoff-
man, J. D. and Bianchi, D.W. 2006. The natural history
of trisomy 12p. Am. J Med. Genet. 140A: 695-703.
Shaffer, L. G., McCaskill, C., Hersh, J. H., Greenberg, E
and Lupski, J. 1996. A clinical and molecular study of
mosaicism for trisomy 17. Hum. Genet. 97: 69-72.
Simpson, J. S. and Jones, A. C. 1982. Hybrid production in
owl monkeys (Aotus trivirgatus). Lab. Anim. 16: 71-72.
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.
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.
Weller, R. E., Wierma, E. L., Malaga, C. E., Baer, J. E and
LeMieux, T.P. 1991. Battelle Primate Facility. J Med.
Primatol. 20: 133-137.
Yunis, E., Caballero, O.M. and Ramirez, C. 1977. Genus
Aotus Q- and G-band karyotypes and natural hybrids.
Folia Primatol. 27: 165-177.


FURTHER INFORMATION ON NEOTROPICAL
MONKEYS REPORTED IN THE XVWI CENTURY:
PART 2

Bernardo Urbani

This article presents new evidence on the manner in which
Neotropical primates were perceived in the 16th century
(after Urbani, 1999, 2004). It includes several aesthetic and
artistic views of New World primates from the early Con-
tact period. The Florentine Codex contains the first illus-
tration of human / non-human primate interactions from
the New World. Between 1540 and 1585, Friar Bernardino
de Sahagdn wrote a compendium of 12 books in Nahuatl,
Latin and Spanish and illustrated these volumes with the
cooperation of local assistants of Aztec descent. This work
was the result of interviews with people of Tlatecolco,
Tenochtitlan and Texcoco (today, the greater Mexico City
metropolitan area). This text is considered one of the major
illustrated treatises of the contact period in the New World.
A drawing in Book 11 depicts a scene entitled Captura de
monos ("capturing monkeys"; see Fig. 1). It is a represen-
tation of monkeys being lured and captured (Sahagdn,
1963). The physical appearance of the primates illustrated
suggests they might be spider monkeys (Ateles ..' ...i As
described in a previous report (Urbani, 1999), Sahagdn in-
dicated in 1555 that the Mexican Amerindians would use
monkeys' hands as omens for deciding when to sell their
merchandise.


The other representations include early European paintings
in which monkeys occupy a principal position posing with
nobles. These suggest that Neotropical primates played an
interesting role as preferred and "exotic" pets even during
the early Contact period. The earliest painting is of Prince
Edward of Wales with a marmoset, possibly C .-' jac-
chus (Fig. 2a; Zuckerman, 1998). It was painted by the
German Renaissance artist Hans Holbein (1497-1543),
living at that time in Basel, Switzerland. The monkey might
have been obtained by some of the English travelers that
visited the northeastern part of South America during the
16th century (see Ribeiro and Araujo Moreira Neto, 1992).
In Fig. 2b, the painting depicts the Infanta Isabela Clara
Eugenia (1566-1633), daughter of Felipe II and Isabel
de Valois, with a common marmoset (C .-' jacchus)
(Zuckerman, 1998). This painting by the Spanish Renais-
sance painter Alonso Sanchez Coello (1531-1588) is the
most realistic pictorial representation of any Neotropical
primate during the 16' century (see other figures in Urbani
1999, 2004, this study). These early European paintings
(Figs. 2a and 2b) suggest the existence of an early interna-
tional network of primate trade; the geographical distribu-
tion of these marmosets was a Portuguese territory in the
New World (today northeastern Brazil), out of the colonial
range of Spain and England.

Finally, Lucas Hombolte (1494-1544) painted a portrait of
Catarina de Arag6n y Castilla (1509-1533) of Spain with
a capuchin monkey (Fig. 2c; Zuckerman, 1998; Fragaszy
et al., 2004). It is neither a tufted capuchin nor a white-
faced capuchin, but may be either Cebus ,Idbfon.s or Cebus
olivaceus. Venezuela was the first Spanish territory to be


Figure 1. Obtaining monkeys by the Mexican Amerindians.


(c)


I (a)


Figure 2. (a) Prince Edward of Wales with a marmoset;
(b) The Infanta Isabela Clara Eugenia and a common marmoset;
(c) Catalina de Arag6n y Castilla with a capuchin monkey.





Neotropical Primates 14(3), December 2007


explored, between 1500 and 1535, and so this brown un-
tufted capuchin monkey species is most likely C. olivaceus.
Finally, it is interesting to note that Catalina de Arag6n y
Castilla was married to Prince Arthur of Wales; therefore it
is feasible to suggest that among the members of the Tudor
dynasty of England there was particular interest in primates
as pets.

Acknowledgements

Thanks to Paul Garber for his suggestions. The author is
supported by a UIUC Assistantship and I would appreciate
any comments and references for future updates.

Bernardo Urbani, Department of An rl.i.. p..1..;,, Univer-
sity of Illinois, 109 Davenport Hall, 607 S. Mathews Ave.,
Urbana, Illinois 61801, USA and Centro de Antropologia,
Institute Venezolano de Investigaciones Cientificas, Cara-
cas, Venezuela, e-mail: .

References

Fragaszy, D., Fedigan, L. and Visalberghi, E. 2004. The
Complete Capuchin: The Biology of the Genus Cebus.
Cambridge University Press, New York.
Ribeiro, D. and Araujo Moreira Neto, C. de. 1992. La
Fundacidn de Brasil: Testimonios, 1500-1700. Biblioteca
Ayacucho, Caracas.
Sahagdn, B. de. 1963. The Florentine Codex. A General His-
tory of the Things of New Spain, Book 11 (Translation by
A. Anderson and Ch. Dibble). University of Utah Press,
Santa Fe.
Urbani, B. 1999. Nuevo mundo, nuevos monos: Sobre
primates neotropicales en los siglos XV y XVI. Neotrop.
Primates 7(4): 121-125.
Urbani, B. 2004. Further information on Neotropical
monkeys reported in the XVI century. Neotrop. Primates
12(3): 146-147.
Zuckerman, S. 1998. The Ape in Myth and Art. Verdigris
Press, The Knowes, Scotland.







CONSERVATION EFFORTS FOR PERUVIAN
PRIMATES

Fanny M. Cornejo
Fanny Fernandez
Noga Shanee
Sam Shanee

Peru is amongst the countries with the highest biodiversity
of primates in the world (Cowlishaw and Dumbar, 2001).
While the exact number of species is still uncertain, at least
36 species are recognized now, with at least three endemic


species (V. Pacheco, pers. comm.). The number of primate
species is likely to increase further as new species are rec-
ognized and described or with changes in taxonomic ar-
rangements. However, the exact geographic distribution
and aspects of the biology of most Peruvian primates re-
mains poorly known or even unknown (Aquino and En-
carnaci6n, 1994). This lack of knowledge within scientific
circles is matched by a low degree of public awareness of
local primates, even when they inhabit forests surrounding
human settlements. Surveys conducted in towns within the
distribution of Peru's endemic primates showed that if local
people are aware of the presence of primates, they usually
know them as "chimpanzees," "gorillas" or just "monkeys"
(Shanee, unpubl. data).

There is an urgent need to save the endemic primates of
Peru and their habitats due to the great extinction risk they
face. Cities and communities within the habitat of many
of Peru's endemic and endangered species are also the areas
where poverty, deforestation, unsustainable land use and
immigration are highest (Elgegren, 2005) which is the
main reasons for the rapid decline of primate populations
in these areas (Leo Luna, 1984). At present, the main cause
of the present conservation problem is the lack of educa-
tion for creating conservation awareness (Pacheco, 2002).

As a response to this problem, the Peruvian-based NGO
Yunkawasi, together with the support of Neotropical Pri-
mate Conservation, the Peruvian National Institute of
Natural Resources (INRENA) and the Ministry of Educa-
tion of Peru, has started the program "Environmental Edu-
cation for the Conservation of Peruvian Primates," using
the Critically Endangered yellow-tailed woolly monkey
(Oreonaxflavicauda) as the flagship species. 0. flavicauda is
endemic to the northeastern Peruvian tropical Andes (Mit-
termeier et al., 1975; Macedo et al., 1979; Groves, 2001)
and is recognized as one of the World's 25 Most Endan-
gered Primates (Mittermeier et al., 2007). This program
aims to increase people's awareness of conservation issues,
to promote knowledge and understanding of the primates
of Peru, with emphasis on the endemic primate species and
the threats they face. It has already been launched in Lima,
Peru's capital, and in the next months it will be implement-
ed in cities within the ranges of many Peruvian primates.
Since education campaigns are fundamental in any conser-
vation effort (Defler et al., 2003), this environmental educa-
tion program is also complementary to the ongoing project
"La Esperanza-Community Conservation and Research
for the Yellow-Tailed Woolly Monkey Oreonaxflavicauda,"
carried out by Neotropical Primate Conservation and the
Museo de Historia Natural of the Universidad Nacional
Mayor de San Marcos. This program aims at establishing a
community-run reserve connecting two existing protected
areas to create a biological corridor for both 0. flavicauda
and another endemic, the night monkey Aotus miconax.
Even though both of these conservation efforts are neces-
sary and timely for helping to change the situation faced by
many Peruvian primates, they are not enough and many





Neotropical Primates 14(3), December 2007


more programs like this are needed. For more information
visit .

Acknowledgments

The project "Conservation of the Yellow-Tailed Woolly
Monkey" is generously funded by Apenheul Primate Con-
servation Trust, Born Free Foundation, IdeaWild, Inter-
national Primate Protection League (IPPL), La Vallee des
Singes, Primate Conservation Inc., Primate Society of Great
Britain, Restore UK and The Monkey Sanctuary Trust; and
the program "Environmental Education for the Conserva-
tion of Peruvian Primates" is funded by The Monkey Sanc-
tuary Trust. We wish to thank the important support from
the Environmental and Community Education Direction
of the Ministry of Education of Peru, Instituto Nacional de
Recursos Naturales (INRENA), Asociaci6n Peruana para
la Conservaci6n de la Naturaleza (APECO), Sociedad Pe-
ruana de Derecho Ambiental (SPDA), Instituto de Inves-
tigaci6n de la Amazonia Peruana (IIAP), the Campesino
Community ofYambrasbamba, Mariella Leo Luna, Victor
Pacheco, Eckhard W. Heymann, Stephen D. Nash, Carlos
Tello and Stella de la Torre.

Fanny M. Cornejo, Museo de Historia Natural, Univer-
sidad Nacional Mayor de San Marcos, Av. Arenales 1256,
Lima 11, Peru, e-mail: , Fanny
Fernandez, Yunkawasi, Lima, Peru, Noga Shanee, and
Sam Shanee, Neotropical Primate Conservation, London,
England.

References

Aquino, R. and Encarnaci6n, F 1994. Primates of Peru.
Primate Rep. 40: 1-127.
Cowlishaw, G. and Dunbar, R. 2000. Primate Conservation
Biology. The University of Chicago Press, Chicago.
Macedo-Ruiz, H. and Mittermeier, R.A. 1979. Redes-
cubrimiento del primate peruano Lagothrix flavicauda
(Humboldt 1812) y primeras observaciones sobre su
biologia. Rev. Cienc. Universidad Nacional Mayor San
Marcos 71: 79-92.
Defler, T. R., Rodriguez-M.J.V. and Hernandez-Camacho,
J.I. 2003. Conservation priorities for Colombian prima-
tes. Primate Conserv. (19): 10-18.
Elgegren, J.J. 2005. La Deforestacidn en el Peru. Avail-
able at: TallerAnilisis_Ambiental/La_Deforestacion en elPeru.
pdf>. Accessed 15 February 2008.
Groves, C.P. 2001. Primate Taxonomy. Smithsonian Insti-
tution Press, Washington, DC.
Leo Luna, M. 1984. The effects of hunting, selective log-
ging and clear-cutting on the conservation of the yellow-
tailed woolly monkey (Lagothrix flavicauda). Master's
thesis, University of Florida, Gainesville.
Mittermeier, R.A., Ratsimbazafy, J., Rylands, A.B., Wil-
liamson, L., Oates, J. F., Mbora, D., Ganzhorn, J. U., Ro-
driguez-Luna, E., Palacios, E., Heymann, E.W., Kierulff,


M. C. M., Yongcheng, L., Supriatna, J., Roos, R., Walker,
S. and Aguiar, J. M. 2007. Primates in Peril: The World's
25 Most Endangered Primates 2006-2008. Primate Con-
serv. (22): 1-40.
Pacheco, V. 2002. Mamiferos del Perd. In: Diversidady Con-
servacidn de los Mamiferos Neotropicales, G. Ceballos and
J. Simonetti (eds.), pp.503-550. CONABIO-UNAM,
M6xico, D.F.


NEOTROPICAL PRIMATE CONSERVATION

We are pleased to announce the creation of a new charita-
ble organisation dedicated to the conservation of primates
from the neotropics. Neotropical Primate Conservation
(NPC) aims to work through a combination of scientific
research, sustainable development, habitat protection and
restoration, creation of public awareness, environmental
education, and facilitation of the commercialization of
sustainable, ecological products on behalf of local people.
NPC's first project is an integrated conservation project for
the yellow tailed woolly monkey in Peru. We are also work-
ing to end the bush meat and illegal wildlife trade through
local and international ad campaigns. To find out more,
please visit us at .


WILDLIFE BIOLOGY IN PRACTICE

Jose Vitor Vingada, Editor in Chief
"Wildlife Biology in Practice" is an Open-Access Interna-
tional Journal edited by the Portuguese Wildlife Society,
and it is dedicated to wildlife research. The journal publish-
es research papers, review papers, discussion papers, meth-
odological papers, technical notes, clinical case reports and
short communications, with topics ranging from all aspects
of wildlife care to administration, fundraising, education
programs, case studies, environmental issues, legalities,
ethics and more. The journal seeks papers that are novel,
integrative and written in a way that is accessible to a wide
audience that includes an array of disciplines from the nat-
ural sciences, social sciences and the humanities concerned
with Wildlife Biology.


REGIONAL ENVIRONMENTAL
CONFERENCES: IPS 2008
WORKSHOP


ENRICHMENT
PRE-TRAINING


The topic of the workshop is improving captive primates
welfare through good husbandry. This workshop aims to
proactively promote the welfare of captive primates by
providing employees from habitat country zoos and/or
sanctuaries with the knowledge, skills, motivation and
management skills to implement BH in their home in-
stitutions. It wil be held from July 30th to August 3rd at
Edinburg Zoo. For more details go to: info/IPS2008.htm>.





Neotropical Primates 14(3), December 2007


PRIMATOLOGY FILM COMPETITION

A Primatology Film Competition is to be held to judge the
best films/videos made in the area of primatology produced
from 1997 up to present. The winning productions will be
screened at the Congress of the International Primatological
Society in Edinburgh, Scotland, August 3-8, 2008. There
will be two categories: (1) professionally made, with budget
above $30,000, and (2) independent productions that cost
less than $30,000. There will be preliminary screenings and
judging and the five best entries in each category will be
screened in Edinburgh. Monetary prizes will be awarded
to the top entries in the non-professional category, and
appropriate certificates from the IPS will be awarded the
winners in the professional category. The deadline for re-
ceiving entries is January 31, 2008. For further informa-
tion see the Congress website: FilmCompetition.html> or contact Charles Weisbard at:
.


HORWICH EARNS FIRST WNPRC JACOBSEN
CONSERVATION AWARD

Jordana Lenon
Robert Horwich, Director of Community Conservation,
a nonprofit primate conservation organization, is the first
recipient of the Lawrence Jacobsen Conservation Research
Award. This award from the Wisconsin National Primate
Research Center supports studies in applied conservation
biology that protect non-human primate species and their
habitats. The award will benefit Dr. Horwich's ongoing work
to conserve the golden langur (T ..' : .-.'..... geei) in India.
The Golden Langur Conservation Project is a holistic proj-
ect that blends conservation, research, education, economic
development and community development. Horwich will
use the award to step up conservation and evaluation ef-
forts at one focal area, the Kakoijana Reserve Forest. He
and project participants, including national forest members
and villagers from adjacent communities, plan to measure
changes in reforestation, the increase in golden langurs, and
changes in economic development within 10 communities
surrounding Kakoijana. "Thus, through this project, we will
use Kakoijana as a model to determine the effectiveness of
the conservation effort," Horwich said.


THE WORLD'S 25 MOST ENDANGERED PRIMATES

Humankind's closest living relatives-the world's apes,
monkeys, lemurs and other primates-are under unprec-
edented threat, with 29 percent of all species in danger of
going extinct, according to a new report by the Primate
Specialist Group of IUCN and the International Primato-
logical Society (IPS), in collaboration with Conservation
International. The World's 25 Most Endangered Primates
list, compiled at the 21st Congress of the International


Primatological Society in Entebbe, Uganda, shows that
eight of the primates on the latest list, including the Suma-
tran orangutan of Indonesia and the Cross River gorilla of
Cameroon and Nigeria, also appeared on the previous three
lists (2000, 2002, 2004). Six other species are on the list for
the first time, including a recently discovered Indonesian
tarsier that has yet to be formally named.By region, the
list includes 11 species from Asia, seven from Africa, four
from Madagascar, and three from South America, show-
ing that non-human primates are threatened wherever they
live. The full report is published in Primate Conservation
22, available at .


NEW CACAJAO SPECIES

A uakari monkey living in north-western Amazonia, it be-
longs to a species unknown to science until recently but is
now named Cacajao ayresii in honour of Brazilian biologist
Marcio Ayres, who pioneered field studies on uakaris. Ua-
karis are traditionally associated with flooded forests on the
margins of lowland rivers, but Cacajao ayresii turned up in
a mountainous area of the Pico de Neblina region on the
border between Brazil and Venezuela, a long way from its
relatives of the Cacajao genre. The new species has a very re-
stricted distribution, and since it lives outside any protected
area and is hunted by local people, it should immediately
be considered endangered. The complete article has been
published in the National Geographic News at news.nationalgeographic.com/news/2008/02/080204-
new-monkey.html>.


CONSERVATION ENDOWMENT FUND -REQUEST
FOR PROPOSALS

The Conservation Endowment Fund (CEF) supports the
cooperative conservation-related scientific and education-
al initiatives of AZA and its member institutions. Every
major type of conservation and animal care initiative is rep-
resented research, field conservation, education, animal
welfare, animal health and captive breeding. The 2008 ap-
plication is now available on the AZA website at www.aza.org/ConScience/WhatIsCEF/>. Proposals are due
on 4 April 2008.








BOOKS

The Evolution of Mind: Fundamental Questions and Contro-
versies, by Steven W. Gangestad. 2007. The Guilford Press.
448 pp. ISBN: 978-1593854089. In the past two decades,
an explosion of research has generated many compelling





Neotropical Primates 14(3), December 2007


insights, as well as hotly debated controversies, about the
evolutionary bases of human nature. This volume brings
together leading proponents of different theoretical and
methodological perspectives to provide a balanced look at
12 key questions at the core of the field today. In 43 concise,
accessible chapters, followed by an integrative conclusion,
the contributors present viewpoints informed by human be-
havioral ecology, evolutionary psychology, and gene-culture
coevolutionary approaches. Topics include the strengths
and limitations of different methodologies; metatheoretical
issues; and debates concerning the evolution of the human
brain, intellectual abilities, culture, and sexual behavior.
Content sample: 9. What nonhuman primates can and
can't teach us about the evolution of mind-C. B. Stand-
ford; 10. Who lived in the environment of evolutionary
adaptedness? -J. B. Silk; 11. Chimpanzee and human in-
telligence: life history, diet and the mind -J. B. Lancaster
and H.S. Kaplan; 12. Optimality approaches and evolu-
tionary psychology: a call for synthesis-H.S. Kaplan and
S.W. Gangestad; 13. The games people play-P. DeScioli
and R. Kurzban; 17. The developmental dynamics of ad-
aptation-H. Honeycutt and R. Lickliter; 18. An alterna-
tive evolutionary Psychology? -K. Sterelny; 22. The role of
group selection in human psychological evolution-D.S.
Wilson; 24. On detecting the footprints of multilevel se-
lection in humans-R. Kurzban and C.A. Aktipis; 25. The
hominid entry into the cognitive niche-H.C. Barrett,
L. Cosmides and J. Tooby; 41. The evolutions of human
mating strategies: consequences for conflict and coopera-
tion-D.M. Buss; 42. Social structural origins of sex dif-
ferences in human mating-W. Wood and A.H. Eagly;
43. The evolutions of women's estrus, extended sexuality,
and concealed ovulation, and their implications for human
sexuality research-R. Thornhill.

The Future of the Wild: Radical Conservation for a Crowded
World, by Jonathan S. Adams. 2007. Beacon Press. 267 pp.
ISBN: 978-0807085370. With appropriate urgency and a
thorough understanding of history and the issues, Jonathan
Adams offers a sound conservation strategy in The Future
of the Wild, using the latest in conservation science as well
as the desires of local communities to protect the places
where people live and work. With modern examples, Adams
shows how each small success moves conservationists closer
to creating protected landscapes large enough to support
animals like bison and wolves. Only with freedom to roam
through and between these huge lands, using wilderness
corridors, can such large animals flourish. Content: Part I.
Thinking Big: 1. A Parliament of owls; 2. Do big things
run the world?; 3. Save some of everything; Part II. Science
and Community: 4. Conservation in exurbia: Florida and
California; 5. Appointment in Sonora; 6. The native home
of hope; 7. Save enough to last: Florida and everglades; Part
III. Yellowstone and the best hope of Earth: 8. Blind men
and elephants; 9. Guarding the golden goose.

Why Conservation is Failing and How It Can Regain Ground,
by Eric T.Freyfogle. 2006. Yale University Press. 320 pp.


ISBN: 978-0300110401.Critics of environmental laws
complain that such rules often burden people unequally,
restrict individual liberty, and undercut private property
rights. In formulating responses to these criticisms, the
conservation effort has stumbled badly. Freyfogle explores
why the conservation movement has responded ineffectu-
ally to the many cultural and economic criticisms leveled
against it. He addresses the meaning of good land use,
describes the many shortcomings of "sustainability," and
outlines six key tasks that the cause must address. Among
these is the crafting of an overall goal and a vision of re-
sponsible private ownership. The book concludes with a
stirring message that situates conservation within America's
story of itself and with an extensive annotated bibliography
of conservation's most valuable voices and texts-impor-
tant information for readers prepared to take conservation
more seriously. Content: 1. The Four Faces of Resistance;
2. Five Paths and Their Values; 3. The Lure of the Garden;
4. Back to Sustainability; 5. What is Good Land Use?;
6. Conservation's Core Tasks, A conservation message to
the American people, Conservation's central Readings:
A bibliographic essay.

Protected Areas and International Environmental Law,
by Alexander Gillespie. 2007. Brill. 318 pp. ISBN:
978-9004161580. This volume seeks to provide the reader
with a clear understanding to the way that protected areas
are created, listed and managed in international law. In
doing so, it provides a complete overview of the primary
international and regional conventions in this area, and
the decisions and resolutions that have come from them.
In doing so, it provides a comprehensive examination of,
inter alia, the World Heritage Convention, the Man and
the Biosphere regime, the Ramsar (Wetlands) Treaty, and
the Convention on Migratory Species. It also deals exten-
sively with the important regional conventions in this area,
covering Europe, Africa and the Americas. The regimes
governing international maritime protected areas, and Ant-
arctica, are also dealt with. In each area, the values, selec-
tion considerations, management, and compliance consid-
erations are examined in detail and linked into recognizable
examples from well known protected sites of international
significance. Content: 1. The History and Scope of Pro-
tected Areas; 2. Definitions; 3. Values; 4. Obligations and
Gaps; 5. Management; 6. Local Populations; 7. Threats;
8. Compliance; 9. Financial Assistance, Communication,
Constituents and Final Issues; 10. Conclusion.


ARTICLES

Arroyo-Rodriguez, V., Mandujano, S., Benitez-Malvido,
J. and Cuende-Fanton, C. 2007. The influence of large
tree density on howler (Alouatta palliata mexicana) pres-
ence in very small rain forest fragments. Biotropica 39(6):
760-766.
Baumgarten, A. and Williamson, G. B. 2007. The distribu-
tions of howling monkeys (Alouatta pigra and A. palliata)





Neotropical Primates 14(3), December 2007


in southeastern Mexico and Central America. Primates.
48(4): 310-315.
Bloch, J.I. and Boyer, D.M. 2007. New skeletons of Pa-
leocene-Eocene Plesiadapiformes: a diversity of arboreal
positional behaviors in early primates. Primate Origins:
Adaptations and Evolution. Ravosa, M.J. and Dagosto,
M., Editors. New York: Springer. 2007. pp. 535-581.
Camargo, C.C. and Ferrari, S. E 2007. Observations of
daytime births in two groups of red-handed howlers
(Alouatta belzebul) on an island in the Tucurui Reser-
voir in eastern Brazilian Amazonia. Am. J. Prim. 69 (10):
1075-1079.
Check, E. and Hayden, T. 2007. Strike threat over jailed
primatologist. Nature. 448(7154): 634.
Conroy, G. C. 2007. Creating, displaying, and querying
interactive paleoanthropological maps using GIS: an ex-
ample from the Uinta Basin, Utah. Am. J. Phys. Anthro-
pol. (Suppl 44): 89.
Corte, A.C., Svoboda, W.K., Navarro, I.T., Freire, R.L.,
Malanski, L.S., Shiozawa, M.M., Ludwig, G., Aguiar,
L.M., Passos, E C., Maron, A., Camargo, Z.P., Itano,
E.N. and Ono, M.A. 2007. Paracoccidioidomycosis in
wild monkeys from Parana State, Brazil. 1 i...' .,'.'
164(5): 225-228.
Cristobal-Azkarate, J. and Arroyo-Rodriguez, V. 2007. Diet
and activity pattern of howler monkeys (Alouattapalliata)
in Los Tuxtlas, Mexico: effects of habitat fragmentation
and implications for conservation. Am. J. Prim. 69(9):
1013-1029.
Crofoot, M. C. 2007. Mating and feeding competition in
white-faced capuchins (Cebus capucinus): the importance
of short- and long-term strategies. Behaviour. 144(12):
1473-1495.
da Cunha, R. G.T. and Jalles-Filho, E. 2007. The roaring of
southern brown howler monkeys (Alouatta guariba clami-
tans) as a mechanism of active defence of borders. Folia
Prim. 78(4): 259-271.
Defler, T. R. and Bueno, M. L. 2007. Aotus diversity and the
species problem. Primate Cons. 22: (online 1-16).
DeLuycker, A.M. 2007. Notes on yellow-tailed woolly
monkey (Oreonax flavicauda) and its status in the pro-
tected forest of Alto Mayo, Northern Peru. Primate Cons.
22: (online 1-7).
de Lyra-Neves, R.M., Oliveira, M.A.B., Telino-Junior,
W. R. and dos Santos, E. M. 2007. Interspecific behaviour
between C .-' jacchus (Linnaeus) (Callitrichidae, Pri-
mates) and some birds of the Atlantic Forest, Pernam-
buco State, Brazil. Rev. Brase Zool. 24(3): 709-716.
Diaz, L.A., del Pilar Diaz, M., Almiron., W.R. and Con-
tigiani, M. S. 2007. Infection by UNA virus (Alphavi-
rus; Togaviridae) and risk factor analysis in black howler
monkeys (Alouatta caraya) from Paraguay and Argentina.
Transactions Of The Royal Society Of Tropical Medicine
And Hygiene. 101(10): 1039-1041.
Di Fiore, A., Fernandez-Duque, E. and Hurst, D. 2007.
Adult male replacement in socially monogamous equa-
torial saki monkeys (Pithecia aequatorialis). Folia Prim
78(2): 88-98.


Di Fiore, A. and Suarez, S.A. 2007. Route-based travel and
shared routes in sympatric spider and woolly monkeys:
cognitive and evolutionary implications. Anim. Cogni-
tion. 10(3): 317-329.
Engels, C.A. and Jacobson, S.K. 2007. Evaluating long-
term effects of the golden lion tamarin environmental ed-
ucation program in Brazil.J. Environ. Educ. 38(3): 3-14.
Field, M.Y. 2007. If you give a monkey an onion: an in-
troduction to fur rubbing in human-commensal white-
fronted capuchin monkeys (Cebus ,lb.f one). Am. J. Phys
Anthropol. (Suppl 44): 108.
Ford, S.M. and Boinski, S. 2007. Primate predation by
Harpy eagles in the Central Suriname Nature Reserve.
Am. J. Phys Anthropol. (Suppl 44): 109.
Grassi, N. E., Berman, C. M., Lessnau, R. G., Gould, L.
and Blumfeld-Jones, K. 2007. Variations in ring-tailed
lemur (Lemur catta) male inter-group transfer patterns in
three populations. Am. J. Prim. 69(Suppl 1): 106-107.
Hankerson, S.J., Franklin, S.P. and Dietz, J. M. 2007. Tree
and forest characteristics influence sleeping site choice by
golden lion tamarins. Am. J. Prim. 69(9): 976-988.
Haugaasen, T. and Peres, C.A. 2007. Vertebrate responses
to fruit production in Amazonian flooded and unflooded
forests. Biodiver. Cons. 16(14): 4165-4190.
Heard, S. B. and Cox, G. H. 2007. The shapes of phyloge-
netic trees of clades, faunas, and local assemblages: ex-
ploring spatial pattern in differential diversification. Am.
Nat. 169(5): E107-E118.
Holroyd, P.A. and Strait, S. G. 2007. New data on Loveina
(Primates: Omomyidae) from the early Eocene Wasatch
Formation and implications for Washakiin relationships.
Elwyn Simons: A Search for Origins. Fleagle, J. G., Gilbert
C.C., Editors. New York: Springer. pp. 243-257.
Hopkins, M. E. and Nunn, C. L. 2007. A global gap analy-
sis of infectious agents in wild primates. Diversity. Distri-
butions 13 (5): 561-572.
Horvath, J., Croswell, M., O'Malley, R.C. and McGrew,
W. 2007. Plant species with potential as food, nesting
material, or tools at a chimpanzee refuge site in Caddo
Parish, Louisiana. Int. J. Prim. 28(1): 135-158.
Jones, C.B. and Jost, C.A. 2007. Update on studies of Be-
lizean primates, emphasizing patterns of species distribu-
tion. Lab. Prim. News. 46(3): 1-5.
Kay, R.E, Fleagle, J.G., Mitchell, T.R.T., Colbert, M.,
Bown, T. and Powers, D.W. 2007. The anatomy of
Dolichocebus gaimanensis, a stem platyrrhine monkey
from Argentina. J. Human Evol. (Advance online publi-
cation): online (1-60).
Klopchin, J. L., Stewart., J. R., Webster, L. F. and Sandifer,
PA. 2007. Assessment of environmental impacts of a
colony of free-ranging rhesus monkeys (Macaca mulatta)
on Morgan Island, South Carolina. Environ. Monitoring
Assess. (Advance online publication): online (1-13).
Lapenta, M.J., Procopio de Oliveira, P. and Nogueira-Neto,
P. 2007. Daily activity period, home range and sleep-
ing sites of golden lion tamarins (Leontopithecus rosalia)
translocated to the Uniao Biological Reserve, RJ-Brazil.
Mammalia. 71(3): 131-137.





Neotropical Primates 14(3), December 2007


Lisboa, C.V., Pinho, A. P., Monteiro, R.V. and Jansen,
A. M. 2007. Trypanosoma cruzi (Kinetoplastida Trypano-
somatidae): Biological heterogeneity in the isolates de-
rived from wild hosts. Exp. Parasitol. 116(2): 150-155.
Loettker, P., Huck, M., Zinner, D.P. and Heymann, E.W.
2007. Grooming relationships between breeding females
and adult group members in cooperatively breeding
moustached tamarins (Saguinus mystax). Am. J. Prim.
69(10): 1159-1172.
Mallapur, A., Sinha, A. and Waran, N. 2007. A world survey
of husbandry practices for lion-tailed macaques Macaca
silenus in captivity. Int. Zoo Yearbook. 41: 166-175.
Martinez-Mota, R., Valdespino, C., Sanchez-Ramos, M.A.
and Serio-Silva, J. C. 2007. Effects of forest fragmenta-
tion on the physiological stress response of black howler
monkeys. Anim. Cons. 10(3): 374-379.
Martins, W. P., de Oliveira Guimaraes, V. and Strier, K. B.
2007. A case of infant swapping by wild northern muriqu-
is (Brachyteles .' .-'.. Primates. 48(4): 324-326.
Martin, R.D., Soligo, C. and Tavare, S. 2007. Primate
origins: implications of a cretaceous ancestry. Folia Prim.
78(5-6): 277-296.
McCabe, G.M. and Fedigan, L.M. 2007. Effects of re-
productive status on energy intake, ingestion rates, and
dietary composition of female Cebus capucinus at Santa
Rosa, Costa Rica. Int. J Prim. 28(4): 837-851.
Mena, J. L., Dosantos, A., Gil, J. G., Escobedo, M., Aquino,
R. and Peres, J. 2007. First record of Saguinus fuscicollis
melanoleucus (Miranda Ribeiro, 1912) in the Peruvian
Amazon. Rev. Peruana Biol. 14(1): 39-42.
Mendes Pontes, A.R., Chivers, D.J. and Lee, P.C. 2007.
Effect of biomass on assemblages of large mammals in a
seasonally dry forest in the Brazilian Amazonia. J Zool.
271(3): 278-287.
Monteiro, R.V., Dietz, J.M., Raboy, B. Beck. B., Vlee-
schower, K. D., Baker, A., Martins, A. and Jansen, A.M.
2007. Parasite community interactions: Trypanosoma
cruzi and intestinal helminths infecting wild golden lion
tamarins Leontopithecus rosalia and golden-headed lion
tamarins L. chrysomelas (Callitrichidae, L., 1766). Para-
sitol. Research. 101(6): 1689-1699.
Moura, A.C.A. 2007. Primate group size and abundance
in the Caatinga dry forest, northeastern Brazil. Int. J.
Prim. 68(6): 1279-1297.
Nascimento, E E, Bonvicino, C.R. and Seuanez, H.N.
2007. Population genetic studies of Alouatta caraya (Al-
ouattinae, Primates): inferences on geographic distribu-
tion and ecology. Am. J. Prim. 69(10): 1093-1104.
Notarnicola, J., Jimenez., EA. and Gardner, S. L. 2007.
A new species of Dipetalonema (Filarioidea: onchocerci-
dae) from Ateles chamek from the Beni of Bolivia. J Para-
sitol. 93(3): 661-667.
Ohl-Schacherer, J., Shepard, G.H. Jr., Kaplan, H., Peres.
C.A., Levi, T. and Yu, D.W. 2007. The sustainability of
subsistence hunting by Matsigenka native communities in
Manu National Park, Peru. Cons. Biol. 21(5): 1174-1185.
Ortiz-Martinez, T. and Rico-Gray, V. 2007. Spider mon-
keys (Ateles ._ .,r ..' vellerosus) in a tropical deciduous


forest in Tehuantepec, Oaxaca, Mexico. Southwest. Natu-
ralist. 52(3): 393-399.
Parga, J.A. and Lessnau, R.G. 2007. Male dispersal as a
mating strategy in the ringtailed lemur (Lemur catta).
Am. J Phys. Anthropol. (Suppl 44).
Pavelka, M. S. M., McGoogan, K. C. and Steffens, T. S. 2007.
Population size and characteristics ofAlouattapigra before
and after a major hurricane. Int. J Prim. 28(4): 919-929.
Peres, C.A. and Palacios, E. 2007. Basin-wide effects of
game harvest on vertebrate population densities in Ama-
zonian forests: Implications for animal-mediated seed
dispersal. Biotropica. 39(3): 304-315.
Porter, L.M., Sterr, S.M. and Garber, PA. 2007. Habitat
use and ranging behavior of Callimico goeldii. Int. J Prim.
28(5): 1035-1058.
Rasmussen, D.T. 2007. Fossil record of the Primates from
the Paleocene to the Oligocene. Handbook of Paleoan-
-'. ..:i.. '.., Volume 2. Primate Evolution and Human Or-
igins. Henke, W. and Tattersall, I., Editors. New York:
Springer-Verlag: 889-920.
Schmidt, D.A., Kowalewski, M.M., Ellersieck, M.R.,
Zunino, G.E., Stacewicz-Sapuntzakis, M., Chen, T.C.
and Holick, M.F. 2007. Serum nutritional profiles of
free-ranging Alouatta caraya in northern Argentina: Lipo-
proteins; amino acids; vitamins A, D, and E; carotenoids;
and minerals. Int. J Prim. 28(5): 1093-1107.
Seiffert, E. R. 2007. Evolution and extinction of Afro-
Arabian primates near the Eocene-Oligocene boundary.
Folia Prim. 78(5-6): 314-327.
Silcox, M.T. 2007. The biogeographic origins of Primates
and Euprimates: east, west, north, or south of Eden? Am.
J Phys. Anthropol. (Suppl 44): 218.
Slater, K.Y., Schaffner, C.M. and Aureli, E 2007. Embrac-
es for infant handling in spider monkeys: evidence for a
biological market? Anim. Behaviour. 74(3): 455-461.
Smith, A.C., Knogge, C., Huck, M., Lottker, P., Buchan-
an-Smith, H.M. and Heymann E.W 2007. Long-term
patterns of sleeping site use in wild saddleback (Saguinus
fuscicollis) and mustached tamarins (S. mystax): effects of
foraging, thermoregulation, predation, and resource defense
constraints. Am. J Phys. Anthropol. 134(3): 340-353.
Soligo, C. 2007. Invading Europe: did climate or geogra-
phy trigger early Eocene primate dispersals? Folia Prim.
78(5-6): 297-313.
Souto, A., Bezerra, B.M., Schiel, N. and Huber, L. 2007.
Saltatory search in free-living C .-' jacchus: environ-
mental and age influences. Int. J. Prim. 28(4): 881-893.
Spathelf, M. and Waite, T.A. 2007. Will hotspots conserve
extra primate and carnivore evolutionary history? Diver-
sity Distributions. 13(6): 746-751.
Stone, A. I. 2007. Ecological risk aversion and foraging be-
haviors of juvenile squirrel monkeys (Saimiri sciureus).
Ethology. 113(8): 782-792.
Trejo-Macias, G., Estrada, A. and Mosqueda Cabrera,
M.A. 2007. Survey of helminth parasites in populations
of Alouatta palliata mexicana and A. pigra in continuous
and in fragmented habitat in southern Mexico. Int. J.
Prim. 28(4): 931-945.





Neotropical Primates 14(3), December 2007


Veiga, L. M. and Ferrari, S. F. 2007. Geophagy at termitaria
by bearded sakis (Chiropotes satanas) in southeastern Bra-
zilian Amazonia. Am. J Prim. 69(7): 816-820.
Vilela, S.L. 2007. Sympatry and diet of C .-- penicil-
lata (Hershkovitz) (Callitrichidae) and Cebus libidinosus
(Spix) (Cebidae) in gallery forests from Distrito Federal,
Brasil. Rev. Brasil. Zool. 24(3): 601-607.
Vitazkova, S.K. and Wade, S.E. 2007. Effects of ecology
on the gastrointestinal parasites of Alouatta pigra. Int. J.
Prim. 28(6): 1327-1343.
Vogel, E.R., Munch, S.B. and Janson, C.H. 2007. Under-
standing escalated aggression over food resources in white-
faced capuchin monkeys. Anim. Behav. 74(1): 71-80.
Wang, Y. H., Tu, X. M., Humphrey, C., McClure, H., Jiang
X., Qin, C., Glass, R. I. and Jiang, B.M. 2007. Detection
of viral agents in fecal specimens of monkeys with diar-
rhea.J. Med. Prim. 36(2): 101-107.
Wehncke, E.V. and Dominguez, C.A. 2007. Seed disper-
sal ecology of non-restricted frugivores, capuchin mon-
keys in three neotropical forests. J Tropical Ecol. 23(5):
519-528.
Westgate, J.W, Cope, D.A. and Beard, K.C. 2007.
A new Uintan genus of omomyine primate from the Casa
Blanca community, Laredo, Texas. Am. J Phys. Anthropol.
(Suppl 44): 247.
Williams, S.H., Vinyard, C.J., Glander, K.E., Teaford,
M.E, Deffenbaugh, M. and Thompson, CL. 2007.
A telemetry system for studying jaw-muscle activity in
free-ranging primates: pilot data from howling monkeys
(Alouattapalliata) at La Pacifica, Costa Rica. Am. J Phys.
Anthropol. (Suppl 44): 250.
Wrangham, R., Crofoot. M., Lundy, R. and Gilby, I. 2007.
Use of overlap zones among group-living primates: a test
of the risk hypothesis. Behaviour. 144(12): 1599-1619.
Young, H., Fedigan, L. M. and Addicott, J. F. 2007. Look
before leaping: foraging selectivity of capuchin monkeys
on acacia trees in Costa Rica. Oecologia. (Advance online
publication): online(i-8).
Zunino, G.E., Kowalewski, M. M., Oklander, L. I. and
Gonzalez, V. 2007. Habitat fragmentation and popula-
tion size of the black and gold howler monkey (Alouatta
caraya) in a semideciduous forest in northern Argentina.
Am. J Primatol. 69(9): 966-975.


ABSTRACTS

Alguns Resumenes do XII Congresso Brasileiro de Prima-
tologia. Belo Horizonte PUC-Minas, 22 a 27 de Julho de
2007. .
Abreu, C.T., Tavares, M. C. H., Gomes, U.R, Waga, I. C. and
Tomaz, C.A.B. Aumento no comportamento sexual du-
rante o tratamento com estradiol em femeas de Cebus spp.
Afonso, C.G., Santos, R.V., Young, R.J. and Ciisar, C.
Dados preliminares sobre a variacao didria da dieta de
Callicebus nigrifrons spix, 1823 na natureza.
Aguiar, L.M., Mellek, D.M., Abreu, K.C., Boscarato,
T.G., Bernardi, I.P., Miranda, J.M.D. and Passos, F.C.


Simpatria entire Alouatta caraya e Alouatta clamitans e a
re-descoberta de hibridos potenciais em vida livre no sul
do brasil.
Aradjo, A. C., Gomes, U. R., Didonet, J.J., Soares, M.V. R.,
Aradjo, C. S., Saletti, P. and Pessoa, V. E Aprendizagem em
discriminacao de cores no bugio preto (Alouatta caraya).
Assungao, M.L., Young, R.J. and Cisar, C. Estudo pre-
liminar da freqiiencia e duracao do comportamento vocal
e social em Callicebus nigrifrons spix, 1823 na rppn san-
tuirio do caraga/mg.
Azevedo, R. B., Gordo, M. and Bicca-Marques, J. C. Cogni-
tive ecology and social foraging in Saguinus bicolor (Spix,
1823).
Barbosa, E.F., Dias, L.G., Moreira, L.S. and Melo, E R.
Influencia do muriqui-do-norte, Brachyteles ..
(Primates, Atelidae) no comportamento de outros animals
no Parque Estadual da Serra do Brigadeiro.
Beltrao-Mendes, R., Coles, R. and Talebi, M. Censo popula-
cional de muriqui-do-sul (Brachyteles arachnoides, e. Geof-
froy 1806-primates, Atelidae) no parque estadual Carlos
Botelho, Sao Miguel Arcanjo sp: dados preliminares.
Bezerra, B.M., Souto, A.S., Oliveira, M.A.B. and Halsey,
L. G. Social and ontogenetic influences on the vocalisa-
tions of wild common marmosets.
Bortolini, T.S., and Bicca-Marques, J.C. Captive enrich-
ment elicits tool use in capuchin monkeys.
Boubli, J.P., Souza, L.G.D., Mourth6, I.M.C. and Strier,
K.B. Padres de utilizagao do espago por um grupo de
Muriquis-Do-Norte (Brach.-. '... .. ATELIDAE)
na estagao biol6gica de Caratinga, mg, Brasil.
Bueno, R. S. and Galetti, M. Diagn6stico da comunidade de
primatas no parque estadual Carlos Botelho, Sp, Brasil.
Burity, C. H. F., Da Silva, M. R., De Souza, A. M., Lancetta,
C. E E, Medeiros, M. E and Pissinatti, A. 0 estudo da ul-
traestrutura (mev) do dorso da lingua de Leontopithecus
chrysomelas cativos (Callithrichidae, primates).
Buti, T.E.M., Kugelmeier, T., Viau, P., Neves, D.V.D.A.,
Van Tol, E.M. and Oliveira, C.A. M6todos n o-inva-
sivos de avaliacao dos niveis de estresse em primatas
nao-humanos: uma ferramenta para a conservagao.
Cabral, J.N.H., Rossato, R.S., Gomes, M.J.T.M. and
Aradjo, F.A.P. Program Macacos Urbanos: relagao entire
fragmentagao e parasitismo em populagoes silvestres de
bugios-ruivos (Alouatta clamitans; Cabrera 1940) em
Porto Alegre.
Camargo, C.C., Lima, E.M., Kierulff, M.C.M. and Silva
Junior, J. S. Dados preliminares sobre diversidade de pri-
matas diurnos em area de exploracao madeireira, Parago-
minas, Pard.
Cardoso, N.A., Le Pendu, Y., Lapenta, M.J. and Raboy,
B. E. Frugivoria De Mico-Leao-Da-Cara-Dourada
(Leontopithecus chrysomelas) Na Reserva Biol6gica De
Una, Bahia.
Carminatti, M. 0. E and Izar, P. Intera6oes iniciais de filho-
tes de macacos-prego (Cebus apella).
Castelo-Branco, R.; Lopes, F.A. Anilise da motivagao
na resolugao de tarefas pelo sagiii-comum (C
jacchus).





Neotropical Primates 14(3), December 2007


Castro, C. S. S., Silva, D. M. R., Costa Jdnior, E A., Angei-
ras, P.H.G., Souza, M.E, Torres, R.A.M., Alves, W.E
and Souza, P. G. Censo populacional do sagiii (C
jacchus) em remanescente de Mata Atlntica.
Coelho, A. S., Ruiz-Miranda, C. R., Martins, A. and Beck,
B. B. Efeito de corredores florestais nos padres sociais de
micos-le6es-dourados (Leontopithecus rosalia).
Condessa, S.S., Barbosa, L.P., Souza, M.P., Morais, D.B.,
Neves, M.M., Coelho, C.D.P. and Ribeiro, A.L. Estra-
tegia social de enriquecimento ambiental no comporta-
mento de macaco-prego (Cebus apella) em cativeiro.
Cordeiro, A.M., Tavares, G.S., Medeiros, M.C. and Dias,
L.G. Dispersao de sementes de CIy'oplyll:iuw imperi-
ale pelo muriqui-do-norte (Brachyteles .':.i... .-.'... no
Parque Estadual do Rio Doce, MG.
Correa, C. M. and Neves, D.V. D.A. Tratamento de canal
conventional em Alouatta guariba clamitans (primates,
Atelidae).
Correa, I. C., Hirano, Z. M. B., Oliveira, D. A. G. and Quin-
tani, I.J. Vocalizagoes de long alcance, estrutura social e
uso de irea em um grupo de Alouatta guariba clamitans.
Costa, C.G., CSmara, E.M.V. C, Santiago, E L. and Paula,
T.P. Registro de tres esp6cies de primatas na airea de in-
fluencia da usina hidreltrica de irapd (uhe irapd), mddio
Jequitinhonha, Minas Gerais.
Costa-Aradjo, R., Schiler da Silva, A., Astarita, L.V. and
Bicca-Marques, J. C. Variagoes temporais na germinadao
de sementes de Ficus organensis (Miq.) Miq. ingeridas por
um bando de bugios-ruivos (Alouatta guariba clamintans
Cabrera, 1940).
Couto-Santos, ER., Boubli, J.P. and Strier, K.B. Pheno-
logical patterns and resource availability to northern
Muriqui in the rppn fma-estagao biol6gica de Caratinga,
mg, Brazil.
Cutrim, F.H.R., Ribeiro, M.D. P and Arruda, M. E Trans-
fer&ncia de alimento em um grupo de C .-('. jacchus
como parte do cuidado a prole na floresta national de assu-
rn.
Cysne, L.B., Cabello, P.H., Gongalves, M.A.B., Cunha,
D. H.S., Marinho, A.M., Zanini, G.M. and Andrade,
M. C. R. Avaliacao clinic e morfom6trica de macacos cy-
nomolgus (Macacafascicularis) cativos.
D'aradjo, J.A., Moura, A.C. de A. and Langguth Bonino,
A. R. Comportamento de catacao social em grupos cativos
de Leontopithecus chrysomelas (Callitrichidae).
da Cunha, R.G. T and Byrne, R.W. The screech complex
of calls of immature black howler monkeys (Alouatta
caraya).
da Silva, L.R., Spironello, W.R. and D'Affonseca Neto,
J.A. Estudo comportamental de um grupo de parauacd
(Pitheciapithecia, Platyrrhini, Cebidae) em um fragmento
florestal urbano, Manaus, Amazonas.
Dias, P.A. D., Coyohua, A. and Canales-Espinosa, D. Effects
of habitat disturbance on the diet and activity patterns
of black howler monkeys (Alouatta pigra) in Campeche,
Mexico.
Emile, N., Nunes, D.M., Gongalves, I. and Barros, M.
Introdugao de goma aribica na dieta de micos-estrela


cativos (C .-('. penicillata): analise em curto prazo da
palatabilidade, preferencia de horirio e fator novidade/
habituacao.
Erbesdobler, E.D., Ajuz, R.C.A., Gelinski, C.S. and
Mello, R.S.R. Relato de caso: associacao entire tres es-
p&cies de primatas (Callimico goeldii, Callicebus cupreus e
C .-'. jacchus) em cativeiro.
Esperanga, E.M., Bezerra, B.M., Souto, A.S., Chichero,
C. and Schiel, N. Efeito da predagao no comportamento
do sagiii comum, C .-.'. jacchus, em fragmento de
mata atlhntica.
Espinosa-G6mez, F.C., Hernindez-Salazar, L.T., Morales-
Mivil, J. and Serio-Silva, J. C. Tiempo de retenci6n de
la digesta en dos grupos de monos aulladores negros
(Alouatta pigra).
Estrela, A. R., Nogueira, E. M. S. and Porfirio, S. Callicebus
barbarabrownae (Hershkovitz, 1990) (primates: pithecii-
dae) de lamarao / ba: resultados preliminares.
Evaristo, G.H., Sangiao, G.M. and Dornelles, S.S.
Censo e analise da situacao dos primatas encontrados
na drea de protegao ambiental Serra Dona Francisca,
Joinville/SC.
Fal6tico, T. and Ottoni, E. B. Transporte de ferramentas de
pedra por macacos-prego (Cebus apella).
Fasano, D.M., Kugelmeier, T., Lopes, C.A.A., Cysne,
L.B., Cunha, D. H. S. and Andrade, M. C.R. Cuidados
neonatais com primatas nao-humanos cativos
Fernandes, R., Silva, F.R. and Verona, C.E. Comporta-
mento alimentar de macaco-prego (Cebus sp.) noParque
Nacional da Tijuca, RJ.
Ferraz, D.S., Nogueira, D. E and Melo, E R. Parimetros
populacionais das esp6cies de primatas no entorno do
Parque Estadual do Ibitipoca, Minas Gerais.
Ferreira, F.B., Burity, C. H.F. and Pissinatti, A. Histologia
do tegumento em Cebus robusuts Silvaa jr., 2001) e Cebus
xanthosternos (wied-neuwied, 1826) cativos (Cebidae,
primates).
Franco, E.S., Soares, G.C.N., Young, R.J.and Cisar, C.
Variagoes na composigao da dieta nas diferentes faixas
etirias de Callicebus nigrifrons Spix, 1823 na natureza.
Fr6es, A. P., Torquetti, C.G., Lino, D., Young, R.J. and
Talamoni, S.A. Fatores que influenciam a distribuigao de
C .-'. penicillata (mico-estrela) em Parques Urbanos
de Belo Horizonte -MG.
Galvao-Coelho, N. L. and Sousa, M. B. C. Influencia da
dominancia social na resposta ao estresse psicossocial em
femeas de sagui.
Gomes, D. F. and Bicca-Marques, J.C. Cognitive ecology
and social foraging in black-horned capuchin monkeys,
Cebus nigritus (Goldfuss, 1809).
Guedes, D., Young, R.J. and Strier, K. B. Ecologia da re-
produgao em femeas muriquis.
Guidorizzi, C.E., Canale, G.R., Kierulff, M.C.M. and
Gatto, C.A.F.R. Uso de pedras como ferramentas por
populagoes selvagens de Cebus xanthosternos e Cebus li-
bidinosus nos estados da Bahia, Alagoas e Minas Gerais.
Hernindez-Salazar, L.T., Espinosa-G6mez, E C., Morales-
Mivil, J. E. and Serio-Silva, J. C. Estrategias digestivas del





Neotropical Primates 14(3), December 2007


mono aullador de manto Alouattapaliatta hacia una dieta
silvestre baja en energia.
lurck, M.F.and Costa, L.C.M. Estudo comportamen-
tal em muriquis-do-sul (Brachyteles arachnoides e. Geof-
froy, 1806), no cativeiro do passeio pdblico de curitiba,
parand, brasil.
Jardim, M.M.A. and Setz, E.Z.F. Analise temporal dos
nascimentos de bugio-ruivos (Alouatta clamitans) em
fragments florestais no sul do Brasil.
Jerusalinsky, L. Analise de viabilidade populacional como fer-
ramenta para a conservagao do guig6 Callicebus coimbrai.
Koch, F. and Bicca-Marques, J.C. Comportamento
social de um grupo de bugios-ruivos (Alouatta guariba
clamitans).
Lacerda, E N. and Resende, B. D. Microgen&tica da quebra
de cocos por macacos-prego (Cebus ssp.): comparadao
entire adults em diferentes estigios de proficiencia por
meio de seqiencias comportamentais.
Lapenta, M.J. and Proc6pio de Oliveira, P. Importhn-
cia da dispersao de sementes por micos-le6es-dourados
(Leontopithecus rosalia) na reserve biol6gica Uniao-RJ,
para a conservagao.
Ledo, D.T., Brum, M., Lamim-Guedes, V. and Antonini,
Y. Ecologia e comportamento de um grupo de Callice-
bus nigrifrons spix, 1823 residents no parque estadual do
lacolomi, Ouro Preto, mg -Dados preliminares.
Leopoldo, B. F., Viana, L. R., Viana, T. L. H. and Fernandes,
G.W. Monitoramento de primatas na floresta national
Saraci-Taqiiera, Pard, Brasil.
Lima, A. K.M. and Arruda, M.F. Desenvolvimento em
C .-'. jacchus no ambiente natural.
Lisboa, O.A., Porto, M., Pissinatti, A. and Fedullo, L.P.L.
Anatomia do sistema reprodutor feminino de C -
jacchus (1. 1758) eC .-C aurita (Humboldt 1812)
(Callitrichidae-primates).
Lokschin, L.X., Teixeira, E Z., Buss, G,., Cabral, J.N.H.,
Printes, R. C., Rossato, R. S., Setubal, R. B., Lopes, M. S.,
Nascimento, L.S. and Romanowski, H.P. Program
Macacos Urbanos: Ocorrencia e distribuigao do bugio-
ruivo (Alouatta clamitans; Cabrera, 1940) em Porto
Alegre: Etapa 2 zona centro-sul.
Lousa, T. C., Portilho, K.A., Grande, T. 0O., Cardoso, R.M.
and Mendes, E D. C. Comportamento alimentar de um
grupo semi livre de Cebus libidinosus em um experimen-
tagao em context natural.
Ludwig, G., Aguiar, L. M. and Passos, F. C. Area de vida de
Alouatta caraya (Primates, Atelidae) (Humboldt, 1812)
em ilha e continent do Alto Rio Parand.
Maia, R.T., Fivaro, L.B., Moreira, L.S. and Dias, L.G.
Area de vida de um grupo de muriqui-do-norte (Brachyte-
les .'i ...' .-'.. 1 em um fragmento florestal do Parque Es-
tadual da Serra do Brigadeiro, MG.
Makyama, S.T., Marques, K.L.S. and Galvao, O.F. Dis-
crimina6oes de cores em Cebus apella.
Mannu. M.; Ottoni, E.B. Plasticidade e diversidade no
uso de ferramentas em dois grupos selvagens de maca-
cos-prego (Cebus libidinosus) na caatinga: uso sequencial,
mdltiplo e produgao de ferramentas.


Matias, C.A.R. and Bruno, S. E Novas observagces sobre
a presenga de Leontopithecus chrysomelas (Callitrichidae,
primates) fora de sua irea biogeogrnfica.
Melo, D.S.V., Dell'porto, A. and Teixeira, D.S. Ocorren-
cia de ovos do genero Conspicuum (Trematoda, Dicrocoe-
liidae) em fezes de mico-estrela (C .- penicillata).
Mendes, C. L. S., Dias, L. G. and Melo, F. R. Area de uso e
preferencia de habitat do muriqui-do-norte (Brachyteles
.',..... .-.'... i na Mata do Sossego, Simonesia-mg.
Messias, M. R, Oliveira, M.A. and Ferronato, M. L. Supe-
rexploragao de frutos de cacau por primatas na estagao
experimental da ceplac de ouro preto do oeste/ro: uma
tentative de resolugao de conflitos atraves do manejo de
fauna.
Miranda, J.M.D., Silva-Pereira, J.E., Mellek, D.M. and
Passos, E C. Nota sobre o hibito de beber igua e o con-
sumo de macr6fitas aquiticas em Alouatta caraya (hum-
boldt, 1812) na ilha mutum, alto rio Parand, Brasil.
Morales-Maivil, J. E., Dominguez-Dominguez, L., Hernhn-
dez-Salazar, L.T. and Serio-Silva, J.C. El mono arafina
(Ateles ... ..,'i y la iguana verde (Iguana iguana) como
facilitadores de la germinaci6n de semillas de ficus.
Nagy, M.B.R., Nascimento, A.M. and Resende, B.D.
Estudo preliminary da biomecanica da quebra de cocos
por macacos-prego (Cebus ssp).
Nakai, E. S. and Izar, P. Orgamento de atividades e dieta de
Cebus nigritus na mata atlintica.
Nascimento, A.T.A., Schmidlin, L.A.J. and Valladares-
Pidua, C.B. Relagao entire habitat e uso do espago pelo
mico-leao-da-cara-preta (Leontopithecus caissara lorini e
person, 1990, Callitrichidae, primates).
Nery, M.S., Ferraz, D.S., Souza, S.L.E, Rodes, E.R. and
Melo, E R. Inventirio de primatas do medio rio pardo,
Bahia.
Neves, L.G., Kierulff, M.C.M., Santos, G.R.J., Alvarez,
M., Marques, A. and Raboy, B. E. Resultados prelimin-
ares sobre a irea de ocorrencia de C .-' kuhlii (pri-
mates, Callitrichidae).
Nogueira, D. F., Ferraz, D. S., Oliveira, A. F., Tabacow, F. P.;
Souza, S.M. and Melo, E R. Parmnetros populacionais
de um grupo de muriqui-do-norte (Brachyteles hypoxan-
thus) no entorno do parque estadual do Ibitipoca, Ginas
gerais.
Nunes, A.M., Santos, C.V. and Bicca-Marques, J. C. Eco-
logia cognitiva e forrageio social em hibridos de C
penicillata x C .-' jacchus (primates: Cebidae: Cal-
litrichinae) introduzidos na ilha de Santa Catarina.
Oklander, L.I., Jerusalinsky, L. and Bonatto, S.L.
Aplicabilidade de microssatelites heter6logos em Alouatta
guariba e outros primatas brasileiros.
Oliveira, A. F., Ferraz, D. S., Barros, J. B. G, Vilela, D.A. R.
and Melo, F. R. A translocacao de uma femea isolada de
muriqui-do-norte (Brachyteles .'...' .-'.. como ferra-
menta de manejo para a conservagao da esp6cie.
Ortiz, M.C., Vilela, D.A.R. and Melo, A.L. Ocorrencia
de parasites gastrointestinais em cinco especies de pri-
matas neotropicais de um criadouro conservacionista de
minas gerais.





Neotropical Primates 14(3), December 2007


Orue, M. E. and Oklander, L. Potential functions of long
distance calls in population of Alouatta caraya, Chaco,
Argentina.
Paulo, L.G., Chagas, W.A., Pissinatti, L., Nascimento,
M. D. and Pissinatti, A. Estudo bioquimico s&rico e his-
topatol6gico em Cebus xanthosternos (wied, 1820) (Cebi-
dae -primates) com diabetes mellitus espontdnea.
Peker, S., Kowalewski, M.M., Pave, R., Oklander, L. I. and
Zunino, G. E. Notes on births in wild black and gold
howler monkeys in northern Argentina.
Pereira, P.M. and Melo, E R. Densidade populacional e
ocorrencia native de primatas em um fragmento de mata
atlbntica no municipio de Itajubi, mg.
Pessoa, D.M.A., Perini, E.S. and Pessoa, V.E Deteciao
de alvos naturais pelo sagii-do-cerrado (C
penicillata): avaliacao do papel da visao de cores.
Pessutti, C., Rassy, B. F. and Teixeira, C. R. Implica6oes
decorrentes da caga de primatas: relato de caso.
Peter, E P., Decker, E.B. and Jardim, M.M.A. Interagoes
lidicas extra-grupo entire individuos de Alouattta clami-
tans no sul do Brasil.
Pinha, P.S., Coelho, L.A., Santos, L.L.S., Cho, D.F.,
Almeida, M.R. and Macedo, R.H.F. Transferencia de
comida entire macacos-prego (Cebus libidinosus) de difer-
entes classes etirias.
Pontual, F.B. A paradigm shift for the Atlantic forest,
Brazil: Participatory conservation using agroecological
principles to foster rural development and recuperation
of degraded areas in Caratinga, MG.
Prates, H. M. and Bicca-Marques, J. C. Vivendo no limited?
dieta de um grupo de bugios-pretos (Alouatta caraya
humboldt, 1812) habitante de um pomar.
Presotto, A. and Izar, P. Padres de movimento de Cebus
nigritus no parque estadual Carlos Botelho.
Printes, R. C., Lokshin, L., Teixeira, E Z., Godoy, J. C. F.,
Cabral, J.H., Suertegaray, R., Lopes, M. and Buss, G.
Program Macacos Urbanos: Pontes de corda para traves-
sia de bugios-ruivos (Alouatta clamitans; Cabrera, 1940)
em Porto Alegre, RS.
Queiroz, H. L. and Valsecchi, J. Avaliacao preliminary dos
impacts das mudangas climiticas e da redugao de ndme-
ros sobre populagoes de Cacajao melanocephalus e Cacajao
calvus calvus na amaz6nia ocidental brasileira.
Quintana-Morales, P. C., Morales-Maivil, J. E. and Escobar-
Aliaga, M. Estimaci6n del imbito hogarefio de Alouatta
palliata: una propuesta metodol6gica.
Rangel-Negrin, A., Dias, P.A.D., Canales-Espinosa, D.
and Vea, J.J. A description of the social behavior of black
howler monkeys (Alouattapigra) in Campeche, Mexico.
Rossato, R. S., Vogel, G. H., Eskelsen, P., Rossi, M.J., Oli-
veira, D.A.G., Souza Jr., J. C. and Hirano, Z.M. B. An-
lise da eficicia de enriquecimento alimentar como pro-
motor de bem-estar de bugios-ruivos (Alouatta clamitans,
cabrera 1940) mantidos no centro de pesquisas biol6gicas
de indaial.
Rossi, M.J., Dada, A.N., Hirano, Z.M.B., Souza Junior,
J.C., Oliveira, D.A.G. and Kalk, J.M. Manejo de in-
fantes de Alouatta guariba clamitans (Cabrera, 1940)


(Primates:Atelidae) no centro de pesquisas biol6gicas de
indaial.
Sampaio, D.T. and Ferrari, S.F. Padrao de atividades
de um grupo de macacos-prego (Cebus apella apella,
Linnaeus, 1758) em um fragmento florestal da amaz6nia
oriental.
Santos, R.V., Afonso, C.G., Young, R.J. and Cisar, C.
Anilise preliminary das "batalhas vocais" de Callicebus ni-
grifrons na natureza.
Sena, M.L.C., Silva, P.H.N., Young, R.J. and Casar, C.
Observagao de caga oportunista de uma ave por um
macho de Callicebus nigrifrons na natureza.
Sevciuc, S.M., Laroque, P.O. and Valenga-Montenegro,
M.M. Consolidagao do repovoamento da reserve bi-
ol6gica guaribas, mamanguape pb, por Alouatta belzebul
belzebul, atrav5s dos m6todos de translocacao e soltura
progressive de individuos.
Sgai, M.G.F.G., Stasieniuk, E.V.Z., Rocha, C.G., Por-
tella, T.P., Cottini, A. P., Pizzutto, C.S., Viau, P., Nichi,
M., Oliveira, C.A. and Guimaraes, M.A.B.V. Estudo
end6crino e comportamental do cuidado parental de
individuos da esp6cie sagii-de-tufo-preto (C
penicillta), em cativeiro.
Silva, P.H.N., Young, R.J. and Casar, C. Incentive a mi-
gracao de macho sub-adulto de Callicebus nigrifrons no
sitio de dormida.
Shares, G.C.N., Franco, E.S. and Casar, C. Desenvol-
vimento do filhote de parauacu Pithecia irrorata (gray,
1842) e suas intera6oes sociais em cativeiro.
Souza, M. B. and Ruiz-Miranda, C. R. Anilises acdsticas
das vocalizagoes de longa distdncia de sagiiis (C
spp.) introduzidos em um fragmento de mata atlhntica
no Rio de Janeiro.
Summa, M.E.L., Neves, D.V.D.A., Rossi, EW., Bauab,
A.R., Joppert, A.M., Florio, A.M.S., Peres, N. E, Si,
L. R. M., Almeida, M. F., Gifalli-Iughetti, C. and Correa,
C.M. Manejo e conservagao de bugios Alouatta guariba
clamitans (cabrera, 1940), (primates, Atelidae) progra-
ma de reintrodugao: protocolo sanitario*.
Suscke, P. G., Kierulff, M. C. M., Canale, G. R. and Santos,
G.R. Area de uso de um grupo de macacos-prego-do-
peito-amarelo (Cebus xanthosternos), na reserve biol6gica
de una, bahia.
Tabacow, E P., Mendes, S. L. and Strier, K.B. Observagces
sobre comportamento de infante 6rfao de muriqui-do-
norte (Brachyteles .'\: .'
Teixeira, D.S., Proenga, L. and Pratesi, R. Caso fatal de
distocia de parto em C .- penicillata afetada por os-
teomalicia no centro de primatologia da universidade de
Brasilia.
Veracini, C. and Masseti, M. Early appearance of south-
american monkeys in catholic italy: the second rediscov-
ery of the marcgraves's capuchin monkey, Cebus flavius
(schreber, 1774).
Verona, C.E., Brandao, M., Chame, M., Sianto, L., Ruiz-
Miranda, C., Dietz, J.M. and Beck, B. Exame copro-
16gico de mico-ledo-dourado (Leontopithecus rosalia) e
sagii-de-tufo-branco (C .- jacchus) como m6todo





Neotropical Primates 14(3), December 2007


auxiliar de avaliacao de populagoes selvagens e fragmen-
tos de floresta atlntica do rio de janeiro.
Vieira, P. R., Tavares, M. C. H. andTomaz, C.A. B. Mem6ria
espacial em macacos-prego (Cebus spp.) e humans.
Vilela, A.A.; Del Claro, K. Caracterizagao das populagoes
e uso de habitat por C .-' penicillata em uma reserve
de Cerrado no Triangulo Mineiro.
Villar, D.N.A., Costa, T.C. and Mendes, E D.C. Censo
populacional de Cebus libidinosus no parque estadual
Altamiro de Moura Pacheco, no dominio do bioma cer-
rado, goinia go.
Waga, I.C., Pinha, P.S., Sabbatini, G., Stammati, M. and
Tavares, M. C. H. Predagao e ingestao de vertebrados por
macacos-prego (Cebus libidinosus) no parque national de
Brasilia.
Wruck, E.C., Hirano, Z.M.B. and Ferreira Dos Santos,
W. Caracteristicas bioquimicas da coloracao do pelo por
secregao epid&rmica de Alouatta guariba clamitans.
Xavier, M.S., Pissinatti, L., Nascimento, M.D., Santos,
K. B. and Pissinatti, A. Alguns valores bioquimicos sdri-
cos em Saguinus bicolor (spix, 1823) e Saguinus niger (e.
.. i 1883) Callitrichidae primates.
Zago, L., Regolin, A.L., Juk, L. and Santos, C.V. Resul-
tados preliminares de estimativa populacional e ecologia
de C .- penicillata no parque ecol6gico do C6rrego
Grande (florian6polis, sc).







AMAZONIA THROUGH THE EYES, HARAL
SIOLI-A PIONEER OF TROPICAL ECOLOGY
RESEARCH

Review of: Gelebtes, geliebtes Amazonien Forschungsreis-
en im brasilianischen Regenwald zwischen 1940 und 1962,
by Harald Sioli (edited by Gerd Kohlhepp), 2007. Miinchen,
Verlag Dr. Friedrich Pfeil. ISBN: 978-3-89937-071-3.
228 pages, 2 colour figures, 61 b/w-figures, 1 expedition
map. Price: 38.00 EURO html>.

Eckhard W Heymann

Ecological research in Amazonia is inseparably linked to the
name of Harald Sioli. He is one of the pioneers, if not the
pioneer of the systematic study of Amazonian ecosystems
in the 20th century. Trained as a zoologist, botanist and
limnologist at the University of Kiel in Germany, he first
participated in an expedition to Brazil in 1934-35. When
he returned to Brazil in 1938, he became stuck there by the
outbreak of World War II and could not return to Germa-
ny. Starting in 1940, he spent the next 16 years with eco-
logical research in Amazonia. Sioli returned to Germany in
1957 to become a director of the Hydrobiologische Anstalt
in Plan, which was later renamed as Max-Planck Institute


for Limnological Research, one of the mayor nuclei for
tropical ecology research in Germany. Sioli continued to
do research in Amazonia as a director of this institute, and
much of today's research in Brazilian Amazonia is based
on his pioneering work. Apart from numerous scientific
publications, Sioli also has written lifetime memories in a
total of eight volumes. This book summarizes the essentials
of Sioli's years in Amazonia. Its main title does note easily
translate into English; the literal translation is "Lived, be-
loved Amazonia", with "lived" having the sense of "having
intensively experienced".

This is a wonderful and fascinating book. Each page tran-
spires the commitment of the author to scientific research
in Amazonia, and his strong affection for this part of the
world and to the people living there. A sentence in the
second chapter of the book nicely illustrates this: "I have
not only performed scientific research in Amazonia, I also
have lived this country as it was by that time" (p. 20). The
book describes both the research and personal experiences
Sioli made during his expeditions into the Brazilian rain-
forest between 1940 and 1962. He was fortunate to live
and work in Amazonia by a time when rainforest destruc-
tion was not yet a major issue, but it must also have been a
terrible experience for him to see destruction gaining pace
and changing Amazonia in a way that makes it barely rec-
ognizable to those who knew it in earlier times. As Sioli
writes: "My Amazonia that I have lived with does no longer
exist. Another Amazonia has replaced it..." (p. 104).

Sioli took an integral approach to Amazonian ecology. He
clearly recognized the intimate link between water, soils,
vegetation, and the animals living there. Nowadays, with
an ever increasing specialization, scientists with such broad
perspective have become as rare as many of the organisms
of tropical rainforests. Although there is little reference to
primates in this book, Neotropical primatologists with an
interested in the ecology of the forests where their study
subjects are living will find it a highly informative, exciting,
entertaining, but also emotional reading. At many places,
I felt strongly reminded to my personal feelings and ex-
periences when first coming to Peruvian Amazonia in the
early 80s. I also learned many things about the fascinating
Amazonian ecosystem which I had not known before. For
primatologists, there is an interesting statement concerning
the hunting of primates: according to Sioli, Parintintin In-
dians occasionally hunt woolly monkeys, but never spider
monkeys, because consumption of the latter may transmit
diseases (p. 90). Is it possible that there are diseases around
in Amazonia that have not yet been recognized or diag-
nosed by scientists, but that some day might have simi-
lar impacts as diseases spread from hunted and butchered
monkeys and apes to humans in Africa?

I recommend this book to everybody interested in Ama-
zonian ecology and in the history of research in Amazonia
who is capable of reading and understanding at least a bit





Neotropical Primates 14(3), December 2007


of German. Hopefully, this book will be translated into
English (or into Brazilian Portuguese), to make it accessible
for a wider audience.

Eckhard W. Heymann, Abt. Verhaltensakologie & Sozi-
obiologie, Deutsches Primatenzentrum, Kellnerweg 4,
D-37077 Gbttingen, e-mail: .







2007

Animal Training & Behavior Through Positive Reinforce-
ment-Further Challenging and Advanced Issues. De-
cember 7-9, 2007, Munich, Germany. This seminar will
be imparted by Ken Ramirez, vice president for animal col-
lections and animal training; he develops and supervises
animal-care programs, staff training and development as
well as public presentation programs for the animal col-
lection at Shedd Aquarium. The Seminar will include
themes related to operant conditioning, training situa-
tions and problem solving with positive reinforcement.
For more information visit: KenRamirezl .htm>.

6. Gbttinger Freilandtage. Primate Behavior and Human
Universals. December 11-14, Gbttingen, Germany. This
conference aims to bring together primatologists, evolu-
tionary anthropologists and psychologists to summarise
our current state of knowledge concerning behavioral
variation and its determinants within the order Primates,
including humans. Specifically, it will focus on three as-
pects: (1) comparative studies of behavioral adaptations
across (human and non-human) primates that examine
evolutionary principles, (2) the ability and failures of evo-
lutionary theory to explain human behavioral traits that
affect survival and reproduction, and (3) to identify and ex-
plain human behavioral universals. For additional details
contact Prof. Dr. Peter Kappeler, e-mail: or
visit the weg page: de/welcome.html>.


2008

III Confer&ncia Nacional do Meio Ambiente. Em maio
de 2008 seri realizada a "III Confer&ncia Nacional do
Meio Ambiente", cujo objetivo seri construir um espago de
convergencia social para a formulacao de uma agenda na-
cional do meio ambiente, por intermedio da mobilizacao,
educacao e ampliacao da participacao popular, com vistas
ao estabelecimento de uma political de desenvolvimen-
to sustentivel para o Pais. Afinal, a definicao de political
piblicas para um Brasil sustentivel depend de mudancas
na forma de atuacao das esferas governamentais, do setor


produtivo, das organizagoes da sociedade, chegando ao
cotidiano de cada cidadao. Em suas edicges, a conferencia
coloca para a sociedade temas estrategicos para o Pais, que
visam a conservagao da biodiversidade, da agua, do clima
e dos recursos energ6ticos, com vistas ao desenvolvimento
sustentivel, levando em consideracao que 6 possivel sim
crescer sem degradar a natureza. Quem quiser enviar textos
para compor a Comissao Nacional, pode envii-los at6 dia
15 de dezembro para . In-
forma6oes sobre a Conferencia Nacional em gov.br/conferencianacional> ou pelo e-mail gov.br>.

5th Annual Assesment and Treatment of the Pain and
Distress in Animals (ATOP V). February 8, 2008. Will
be held at the Massachussetts Medical Society Conference
Center at Waltham Woods Corporate Center. What are the
consequences for your science if human endpoints are not
taken into consideration in the experimental design? The
conference will examine this question in detail. For more
information go to info.html>.

Behaviour and Individuality in Primates and other Mam-
mals. March 17-18, 2008, Lisbon, Portugal. The confer-
ence Behaviour and Individuality in Primates and other
Mammals is held as part of the celebrations of the 6th an-
niversary of BioCEL, and will take place at the Auditorium
Agostinho da Silva at Lus6fona University. The conference
aims to launch a creative debate and brainstorm for future
research on a rather new topic of research: the study of
inter-individual variation in animal behaviour. As we get
to know more about each animal species the evidence of in-
dividuality also grows. For more information visit the web
site: .

9th Student Conference on Conservation Science. March
25-27, 2008. Department of Zoology, University of Cam-
bridge, United Kingdom. The SCCS is aimed at young re-
searchers working in universities departments, conservation
organizations, or resource management agencies. Approxi-
mately 170 postgraduate students attend the conference
each year, from a broad range of disciplines in conserva-
tion, including ecology, geography, sociology and econom-
ics. The most important part of the three-day programme
will be poster sessions and 33 fifteen minute talks by stu-
dents on any aspect of conservation science. There will also
be workshops, presentations by conservation NGOs and
agencies and social events designed to give participants the
opportunity to make new contacts in their own and related
disciplines. Prizes are awarded to posters and talks of out-
standing quality and relevance to conservation. For more
information and applications go to: .

American Association of Physical Anthropologists Annual
Meeting. April 7-13, 2008, Columbus, Ohio. For more
information visit the web site: annmeet/>.





Neotropical Primates 14(3), December 2007


3rd International Conference on Primate Genomics: Pri-
mate Genomics and Human Disease. April 13-16, 2008,
University of Washington, Seattle. The conference includes
a focus on genomic and proteomic resource development,
advances in computational biology and bioinformatics,
and new developments in comparative genomics and evo-
lutionary biology. The 2008 conference also highlights re-
search activities in which genomics and nonhuman primate
models are being used to better understand human disease.
Recent advances in the field, including the sequencing of
the rhesus macaque genome, the development of macaque-
specific DNA microarrays, and new opportunities for non-
human primate proteomics make this conference particu-
larly timely, significant, and exciting. For more information
go to: .

IV Simp6sio de Areas Protegidas. 19-23 de maio, 2008.
0 SAP 6 uma oportunidade de colocar juntas as pessoas
que viabilizam a conservagao no campo, com aqueles
pensam seus conceitos, com aqueles que lutam nas frentes
de batalha juridica e political, com aqueles que estao dando
os primeiros passos na protegao de areas dentro das uni-
versidades. Nesta ocasiao, o SAP seri realizado na atraente
cidade de Canela, localizada na Serra Gadcha. Para mais
informacoes contatar , ou
visit o site .

31st Meeting of The American Society of Primatologists.
June 18-21, 2008, West Palm Beach, Florida. For more in-
formation visit the web site: http://www.asp.org/asp2008/
index.htm or contact Matthew Novak, e-mail: mail.nih.gov>.

II Congress Colombiano de Primatologia. Junio
26-28 de 2008, Bogoti, D.C. Organizado por la Aso-
ciaci6n Colombiana de Primatologia (ACP). Se reali-
zarin presentaciones a manera de conferencias magis-
trales, ponencias, presentaci6n de carteles, mesas de
discusi6n, talleres y cursos, en torno a dos grandes temi-
ticas: conservaci6n in situ y ex situ. Para mayor informa-
ci6n contactar org>/, o visit el
sitio .

22nd Annual Meeting of The Society of Conservation Bi-
ology. July 13-17, 2008, Chattanooga, Tennessee, USA.
The chair of the meeting will be Dr. David A. Aborn, from
the Department of Biological and Environmental Sciences,
University of Tennessee at Chattanooga. As evidenced by
several previous meeting themes, there are connections
among many aspects of the environment and its conser-
vation, and recognizing those connections is critical for
achieving the goals of conservation biology. To that end,
the theme for the 2008 SCB annual meeting T'ow the
mountains to the sea"will examine several major ecosystems,
both as separate components and as a connected entity. For
more information and submission dates, go to: conbio.og _'i" >.


XXIInd IPS Congress. August 3-8, 2008, Edinburg In-
ternational Conference Center, Edinburg, Scotland. Spon-
sored by the Primate Society of Great Britain. Abstracts
for oral and poster presentations must be submitted by
30th November 2007. For information consult the web
page: .

XXth International Congress of Zoology. August 26-29,
Jussieu Grand campus, Paris, France. Held every four years,
the International Congress of Zoology gives zoologists and
professionals from all fields related to zoology the chance
to come together to discuss the current status of zoology
and to share ideas about future development of all its dis-
ciplines. The International Society of Zoological Sciences
(ISZS) and the Societe Zoologique de France invite you
to the XX International Congress of Zoology. It will be
co-hosted by the Universities Pierre et Marie Curie (PVI),
Paris-Sud (PXI) and the Museum National d'Histoire
Naturelle. Registration will open on 1st December 2007.
For information about the Congress, please visit: icz2008.snv.jussieu.fr> or index-new/20icz.htm>.

6th International Conference on Methods and Techniques
In Behavioral Research. August 26-29, 2008, Maastricht,
The Netherlands. The theme of the 6th international con-
ference on methods and techniques in behavioral research
will be Measuring Behavior. This conference is the premier
interdisciplinary event for scientists and practitioners con-
cerned with the study of human or animal behavior. This
unique conference focuses on methods, techniques and
tools in behavioral research in the widest sense, from be-
havioral ecology to neuroscience and from physiology to
ergonomics. In doing so, Measuring Behavior responds to
a growing need to cross disciplines and create bridges be-
tween them. For more details go to net/mb2008/>.


2009

Neotropical Primate Husbandry, Research, and Conser-
vation Conference. October 13-15, 2009. Brookfield Zoo
is pleased to announce that it will host a Neotropical Pri-
mate Husbandry, Research, and Conservation Conference.
This conference will focus on a variety of topics pertaining
to neotropical primates like husbandry, conservation, and
emergent issues pertaining to captive and wild populations.
The workshop will include three days of presentations, a
poster session, as well an icebreaker, silent auction, and
banquet. Additional information regarding registration
fees, travel information, and submission of abstracts will be
made available in late 2008. For questions please contact
.















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 Bogoti
D.C., Colombia, Tel: (571) 345-2852/54, Fax: (571) 345-2852/54,
e-mail: , and all Portuguese contribu-
tions to: Julio Casar Bicca-Marques, Departamento de Biodiversidade
e Ecologia, Pontificia Universidade Cat61lica do Rio Grande do Sul,
Av. Ipiranga, 6681 Pr6dio 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 et al, 2001)..."
In the list of references, the title of the article, name of the journal,
and editorial should be written in the same language as they were
published. All conjunctions and prepositions (i.e., "and", "In") should
be written in the same language as rest of the manuscript (i.e., "y"
or "e", "En" or "Em"). 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 "Dissertacyo de Mestrado" and "Tesis de
Maestria" for articles in Portuguese and Spanish respectively.
"Unpublished report" changes to "Relat6rio Tkcnico" and "Reporte
no publicado" for articles in Portuguese and Spanish respectively.








Neotropical Primates
A Journal and Newsletter of the IUCN/SSC Primate Specialist Group
Vol. 14(3), December 2007


Contents

Articles

Flora Bacteriana de la Cavidad Oral del Mono Titf (Saimiri oerstedii) y Su Perfil de Sensibilidad a Antibi6ticos
Carlos E. Rodriguez-Rodriguez, Evelyn Rodriguez-Cavallini, Maria del Mar Gamboa-Coronado,
Silvia fiminez-Cuadra, Ronald Sdnchez-Porras y Gustavo A. Gutidrrez-Espeleta............................................ ......................... 103

Short Articles

Behavioral Flexibility and Tool Selection in a Tufted Capuchin Monkey (Cebus apella)
Euphly Jalles-Filho, Rogrio Grassetto Teixeira da Cunha and Rodolfo Aureliano Salm .......................................................................112
Distribution and Conservation Status of the Yellow-Tailed Woolly Monkey (Oreonaxflavicauda, Humboldt 1812) in
Amazonas and San Martin, Peru
Sam Shanee, Noga Shanee and Angela M M aldonado ................................................................................ ............................. 115
Grandmaternal Infant Carrying in Wild Northern Muriquis (Brachyteles hypoxanthus)
Maira de Lourenfo Assunfao, Sergio L. Mendes and Karen B. Strier................................................................... ....................... 120
Caracterizaci6n de la Poblaci6n del Mono Aullador (Alouatta palliata palliata) en el Refugio Nacional de Vida Silvestre
Isla San Lucas, Costa Rica
Marta Marleny Rosales-Meda......................... ..... .........................................................122
Aspectos Ecol6gicos de Alouatta guariba clamitans Cabrera, 1940 na Area de Relevante Interesse Ecol6gico Floresta da
Cicuta, Rio de Janeiro, Brasil
Sandro Leonardo Alves e Andrd Scarambone Zaus.................................................................................. ................................. 127
A Preliminary Study of Proximity Patterns Among Age-Sex Classes in a Population of Central American Black
Howlers (Alouatta pigra)
Lisa C. Corewyn and M S. M Pavelka.................................................................................................. .............. ...........................130
Density of Saguinus inustus (Schwartz, 1951) in the Interfluvium of the Caqueti-Apaporis Rivers, Colombian Amazonia
Claudia Idaly Castillo-Ayala and Erwin Palacios ................................................................... ........................................... 134
New Occurrence Records and Eastern Extension to the Range of Callicebus cinerascens (Primates, Pitheciidae)
Mauricio de Almeida Noronha, Wilson Roberto Spironello and Dayse Campista Ferreira.................... .. ..........................137
New Occurrence Records ofMico acariensis (Primates, Callitrichidae)
Mauricio de Almeida Noronha, Jose de Sousa e Silva Jinior, Wibon Roberto Spironello and Dayse Campista Ferreira .......................140
Sleep Parameters in Captive Female Owl Monkey (Aotus) Hybrids
Sachi Sri Kantha, Juri Suzuki, Yuriko Hirai and Hirohisa Hirai ..................................... ................................................ 141
Further Information on Neotropical Monkeys Reported in the XVIt" Century. Part 2
Bernardo Urbani.................................................................. ................................ .............................144

N ew s .......................................................................................................................................................................................... 14 5

R ecen t P publications ......................................................................................... ........ ..................................................147

M eetin g s ................................................................................................................................................................................... ...56




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