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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 Supplement 2005
Frequency: quarterly
regular
 Subjects
Subject: Primates -- Periodicals -- Latin America   ( lcsh )
Primates -- Periodicals   ( lcsh )
Wildlife conservation -- Periodicals   ( lcsh )
Genre: review   ( marcgt )
periodical   ( marcgt )
Spatial Coverage: Brazil
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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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Bibliographic ID: UF00098814
Volume ID: VID00051
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
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    Copyright
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    Back Matter
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    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 13
Supplement
December 2005

The Ecology and Conservation
of the Muriqui (Brachyteles)
Reports from 2002-2005


Guest Editors
Karen B. Strier, Luiz Paulo de S. Pinto,
Adriano Paglia, Jean P. Boubli,
Sergio L. Mendes and Onildo]. Marini-Filho



Editors
Anthony B. Rylands
Ernesto Rodriguez-Luna
Assistant Editors
John M. Aguiar
Liliana Cort6s-Ortiz
PSG Chairman ,CENTER
Russell A. Mittermeier FOR APPLIED
BIODIVERSITY
PSG Deputy Chairman CONSERVATION SPECIESSURVIAL SCIENCE
Anthony B. Rylands INTERNATIONAL COMMISSION INTERNATIONAL









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
DOI: 10.1896/ci.cabs.2005.np.13.suppl.

Editors
Anthony B. Rylands, Center for Applied Biodiversity Science, Conservation International, Arlington, VA, USA
Ernesto Rodriguez-Luna, Universidad Veracruzana, Xalapa, Mexico

Assistant Editors
John M. Aguiar, Center for Applied Biodiversity Science, Conservation International, Arlington, VA, USA
Liliana Cortes-Ortiz, Universidad Veracruzana, Xalapa, Mexico

Editorial Board
Hannah M. Buchanan-Smith, University of Stirling, Stirling, Scotland, UK
Adelmar F. Coimbra-Filho, Academia Brasileira de Ci&ncias, Rio de Janeiro, Brazil
Liliana Cortes-Ortiz, Universidad Veracruzana, Xalapa, Mexico
Carolyn M. Crockett, Regional Primate Research Center, University of Washington, Seattle, WA, USA
Stephen E Ferrari, Universidade Federal do Para, Belem, Brazil
Eckhard W. Heymann, Deutsches Primatenzentrum, Gittingen, Germany
Russell A. Mittermeier, Conservation International, Arlington, VA, USA
Marta D. Mudry, Universidad de Buenos Aires, Argentina
HorAcio Schneider, Universidade Federal do Para, Belem, Brazil
Karen B. Strier, University of Wisconsin, Madison, WI, USA
Maria Emilia Yamamoto, Universidade Federal do Rio Grande do Norte, Natal, Brazil

Primate Specialist Group
Chairman Russell A. Mittermeier
Deputy Chair Anthony B. Rylands
Co-Vice Chairs for the Neotropical Region Anthony B. Rylands & Ernesto Rodriguez-Luna
Vice Chair for Asia Ardith A. Eudey
Vice Chair for Africa Thomas M. Butynski
Vice Chair for Madagascar Jirg U. Ganzhorn

Layout: Kim Meek, Center for Applied Biodiversity Science, Conservation International, Arlington, VA, USA

Editorial Assistance:
Mariella Superina, University of New Orleans, Department of Biological Sciences, New Orleans, LA

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

Front cover: Adult female northern muriqui (Brachyteles hypoxanthus) at the RPPN-Feliciano Miguel Abdala. Photo by Carla B. Possamai.

In collaboration with Conservacao Internacional do Brasil, Avenida Getulio Vargas 1300, 7 andar, Savassi, Belo Horizonte 30112-021, Minas Gerais,
Brazil. Website: .

This publication is funded in part by the Gordon and Betty Moore Foundation, Presidio of San Francisco, P.O. Box 29910, San Francisco, California
94129-0910; 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.




MARGOT MARSH

GORDON AND BETTY
ooow o MOORE
CONSERVAQAD M O
INTERNATIONAL F O U N D A T I N
BRASIL





Neotropical Primates 13(Suppl.), December 2005


IN MEMORY OF EDUARDO MARCELINO VENTURA VEADO, 1960-2006

The muriquis at the RPPN-Feliciano Miguel Abdala (previously, the Estacao Biol6g-
ica de Caratinga, or EBC), lost one of their greatest champions when Eduardo and his
wife, Simone, were killed by a hit-and-run driver while they were taking an evening
walk on the outskirts of Ipanema, Minas Gerais on 5 October 2006.

Eduardo's long history with the EBC began when he was a student of Cdlio Valle,
Professor of Vertebrate Zoology at the Federal University of Minas Gerais (UFMG).
Cdlio was sponsoring Karen's doctoral research at Caratinga, and knew that she needed
a field assistant. He encouraged Eduardo, who showed up at the EBC in August 1983,
and ended up working with Karen through July 1984. He then returned to Belo Horizonte to complete his university stud-
ies, and soon afterward, he married Simone.

Eduardo was hired by the Fundagao Biodiversitas to be the Director of the EBC in 1986, and he and Simone moved to
Santo Ant6nio de Manhuacu, a small town nearby, to facilitate his work. He hosted many visitors, developed conservation
education programs, and dedicated his life's work to helping maintain the field station of the EBC in the Fazenda Montes
Claros of Sr. Feliciano Miguel Abdala and his family, with its forest and its muriquis. Eduardo's son, Lucas, was born in
1989, and a few years later, Eduardo and his family moved to Caratinga, where his daughter, Bruna, was born. Eduardo
led campaigns in Caratinga to involve the city in preserving the muriquis. Despite his successful activities there, Eduardo
felt that Caratinga was too far from the forest, so he and his family moved to Ipanema, where he visited with Sr. Feliciano,
checked on the researchers, and administered the field station and its personnel almost daily.

Over the years, Eduardo built an impressive team of dedicated assistants to help him, many of whom are still working
with us today. In 1993, Eduardo received a prestigious recognition award from the American Society of Primatologists,
and an ongoing subscription to the American Journal of '. .-. '., i. which the researchers at the EBC still value greatly.
In 1994, after his position with the Fundagao Biodiversitas ended, Eduardo obtained support from the Liz Claiborne and
Art Ortenberg Foundation to initiate conservation efforts among the farmers in the region surrounding the EBC. By then,
our long-term research had shown that the muriqui population was growing, and would eventually need more forest.
Eduardo developed a strong relationship with Sr. Feliciano, who agreed to let some of the coffee fields and pastures sur-
rounding the forest regenerate. Eduardo also built a nursery, where the seeds from fruits in the diet of the muriquis could
be cultivated to supply seedlings for reforestation. Throughout all of this, he continued to manage the EBC, providing the
infrastructure necessary for maintaining the long-term muriqui research there, and the logistical support for visitors and the
researchers themselves.

By 1998, Eduardo's conservation efforts had expanded and were generating important results. He created the Associaiao
Pr6-Estagao Biol6gica de Caratinga, an environmental organization with the aim of establishing strategies for the conserva-
tion of the muriqui and the forests in the entire region. He served as the Executive Director of this organization. The Asso-
ciacao Pr6-Estagao Biol6gica de Caratinga became a partner of Conservation International-Brazil, which funded Eduardo's
ongoing activities at the EBC.

With his extensive experience and accumulated knowledge of muriqui management, Eduardo was invited to serve as a
member of the Committee for Management and Conservation of Muriqui when it was established in 2002. The Commit-
tee's purpose is to develop strategies for the conservation of this species and to provide technical advice to IBAMA about
decisions concerning muriquis. Eduardo's participation was highly valued.

Following the death of Sr. Feliciano in 2000, Eduardo was diligent in accompanying the discussions among the Abdala
family about the future of their forest. It was through Eduardo that many of us learned that the Abdala family had made the
historic decision to convert their family's forest to a Private Reserve (RPPN) in 2001.

By April 2005, the Preserve Muriqui, which administers the RPPN-Feliciano Miguel Abdala, was well-established, and
Eduardo's long-term service as Director of the EBC came to an end. During his tenure as Director, he oversaw the electricity
that was brought to the EBC, the expansion of the research house, the construction of the Visitors Center "Cdlio Valle",
and the inauguration of the Field Laboratory "Dra. Karen B. Strier", in celebration of 20 years of muriqui research at EBC.
Eduardo encouraged and coordinated the visits of hundreds of bus loads of students from schools in the region, as well as
numerous groups of Brazilian and foreign eco-tourists, and visiting researchers, photographers, and film crews from around
the world.





2 Neotropical Primates 13(Suppl.), December 2005

Eduardo was employed by the Mayor of Ipanema until his death, and was full of new ideas to expand conservation efforts
in the region. Among the most important of these was his plan to fulfill his long-time dream of establishing a forest corridor
to link the RPPN forest with the forest in Ipanema, and ultimately, with the Mata do Sossego Private Reserve, inhabited by
another isolated population of muriquis.

All of us who have worked with Eduardo know the depth of his commitment to the forest and its muriquis. Eduardo was a
colleague to everyone involved with muriqui conservation, and a close friend to many of us. Most of all, he was a friend of
the muriquis.

We will always remember Eduardo, and his many contributions, with great appreciation.

Karen B. Strier and Luiz Paulo de Souza Pinto
June 2007





Neotropical Primates 13(Suppl.), December 2005 3

THE ECOLOGY AND CONSERVATION OF THE MURIQUI (BRACHYTELES):
REPORTS FROM 2002-2005. INTRODUCTION

Karen B. Strier1, Luiz Paulo S. Pinto2, Adriano Paglia3, Jean P. Boubli4, Sergio L. Mendes5,
Onildo J. Marini-Filho6 and Anthony B. Rylands 7

1Department of Andr. ..p..1..; ,, 1180 Observatory Drive, University of Wisconsin-Madison, Madison, WI 53706, USA,
e-mail:
2Conservagao Internacional (CI-Brasil, Av. Getdlio Vargas 1300, Belo Horizonte 30112-021, Minas Gerais, Brazil, e-mail:

3Conservagao Internacional (CI-Brasil), Av. Getdlio Vargas 1300, Belo Horizonte 30112-021, Minas Gerais, Brazil, e-mail:

'Department of Anrli. .p. .1..;,, The University of Auckland, Auckland, New Zealand, e-mail:
5Departamento de Ciencias Biol6gicas CCHN, Universidade Federal do Espirito Santo, Vit6ria 29040-090, Espirito
Santo, Brazil, e-mail:
6IBAMA- Coordenacao de Conservagao da Fauna Ameagada de Extingao e Migrat6ria (COFAU), SCEN Avenida L4
Norte, Ed. Sede IBAMA, Bloco B subsolo, Brasilia 70.800-200, DF, Brasil, e-mail:
'Center for Applied Biodiversity Science, Conservation International, 2011 Crystal Drive, Suite 500, Arlington, VA 22202,
USA, e-mail:


This special issue of Neotropical Primates is dedicated to the muriqui (genus Brachyteles), the largest of the New World pri-
mates and one of the flagships for conservation efforts worldwide. Two species are now recognized, the southern muriqui
(B. arachnoides) and the northern muriqui (B. :.. -'.. Southern muriquis are classified as Endangered, while northern
muriquis rank among the 25 most Critically Endangered primates on the planet (Strier et al., 2006). They are endemic to
the Atlantic Forest of southeastern Brazil, one of the "hottest" of the biodiversity hotspots; very highly threatened regions
with exceptionally large numbers of endemic species (Myers et al., 2000).

The Atlantic Forest hotspot is distributed over more than 23 degrees of latitude and encompasses parts of three
countries-Brazil, Argentina, and Paraguay. The forest once covered nearly 1, 360,000 km2 in Brazil alone; nearly 15 percent
of the nation's territory and spanning all or part of 15 states (Galindo and CSmara, 2003). The Brazilian Atlantic Forest
shows impressive biodiversity gradients, with extraordinary levels of biological diversity in a varied set of landscapes and
socioeconomic contexts. Eighty (80 percent) of the 24 primate species and subspecies in the Brazilian Atlantic Forest are en-
demic, including two endangered endemic genera-the lion tamarins (Leontopithecus) and the muriquis. It is unquestion-
ably one of the most threatened regions, not only in Brazil but worldwide. Less than 8 percent of the original forest persists,
much of which is fragmented, degraded and polluted, and still hunted. More than 60 percent of the animals and the vast
majority of plants threatened with extinction in Brazil are found in this biome alone (Paglia, 2005).

Muriquis were first described by naturalists in the 19th century (1806), but it was Aguirre's (1971) pioneering monograph
that brought their plight to the attention of Brazilian scientists and conservationists, such as Adelmar E Coimbra-Filho
(1972) and Cdlio Valle (Valle et al., 1984). Since the late 1970s, research on primates and protected areas in the Atlantic
forest carried out by these scientists, together with Russell Mittermeier, Gustavo Fonseca and others, showed that this
region ranks among the most diverse and most endangered on Earth. The initial focus on primates has now blossomed
into a number of internationally and nationally supported conservation projects. Work on the lion tamarins (Kleiman and
Rylands, 2002) and the muriquis, and the importance of the Atlantic forest to the survival of these endemic genera, provide
some of the best examples of the use of flagship species to achieve broader conservation objectives.

The results of these efforts are evident in the new discoveries about muriquis and conservation initiatives described in this
volume. Contributors include researchers and conservationists from academic and both governmental and nongovernmen-
tal organizations. Some have devoted the greater part of their professional careers to muriquis; others are more recent part-
ners who bring comparative perspectives from their work in other ecosystems and on other primates and nonprimate fauna
to ongoing muriqui research and conservation efforts.

Among the many advances in research have been the insights from captive management of muriquis at the Centro de Pri-
matologia do Rio de Janeiro (Pissinatti), and from field studies that describe newly contacted populations in the states of
Minas Gerais (Melo and Dias), Rio de Janeiro (Garcia), Espirito Santo (Mendes, Santos and Carmo.; Vieira and Mendes)
and Paranai (Koehler et al) and new research on previously studied populations in Sao Paulo (Martins; Talebi and Soares).
Long-term data on the northern muriquis at the Estagao Biol6gica de Caratinga/ Feliciano Miguel Abdala Private Reserve





Neotropical Primates 13(Suppl.), December 2005


(hereafter, RPPN-FMA) in Minas Gerais have provided insights into reproductive ecology and demography (Strier) and the
populations of sympatric primates in this forest (Almeida-Silva et al.). Other studies also contribute with new insights into
the genetics of wild populations (Fagundes), and directives for the conservation and management of this species (Mendes et
al.; Pontual and Boubli; Oliveira, Marini-Filho and Campos).

Conservation efforts have increasingly involved local human communities in primate conservation programs, as exempli-
fied in a recent initiative in Caratinga (Pontual and Boubli). The government has also become more involved in support-
ing conservation, as is clear with the efforts of the Coordination for the Conservation of Threatened Fauna and Migratory
Species (Coordenafdo de Conservaado da Fauna Ameacada de Extincdo e ,Il',gro,:; COFAU) of Brazil's Institute for the
Environment (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renovdveis-IBAMA), and the associated Center
for the Protection of Brazilian Primates (Centro de Proteado de Primatas Brasileiros- CPB), also part of IBAMA, created in
2001 (Oliveira, Marini-Filho, and Campos). IBAMA created an international advisory committee for the conservation of
the muriqui in 2003, involving many of the authors in this special issue. Consideration of the Atlantic forest brown howler
monkey was later deemed essential too, and in 2005 the committee became the "International Committee for the Conserva-
tion and Management of the Atlantic Forest Atelids." All issues concerning research, monitoring and conservation of these
species are now discussed, and given direction and resolution, through this government committee.

Nearly all of the advances described in this volume build on what has been a long-standing and ongoing commitment to the
dual priorities and synergistic dynamics between research and conservation programs. Thus, knowledge obtained from basic
research is as necessary for the development of informed conservation and management plans as effective conservation and
management plans are for the continuity of research.

In an historical act, in 2003 the Brazilian Ministry for the Environment (MMA), through its Project for the Conservation
and Sustainable Use of Brazilian Biological Diversity (Projeto de Conservaado e Utilizafdo Sustentdvel de Diversidade Bioldgica
Brasileira- PROBIO) (in partnership with The World Bank and the Global Environment Facility) approved, simultaneously,
three large conservation projects to work on different northern muriqui populations (one in Espirito Santo and two in Minas
Gerais). The total amount approved for the three projects was the record-breaking sum of 1 million reais (roughly equivalent
to U$500,000); never in Brazil had a species attracted such large funds from the government. This was strong evidence of
the growing awareness of, and concern for, the critical state of Brachyteles .'\ .-.'... and its Atlantic Forest habitat.

The three projects were complementary, and formed a coordinated a strategy to increase our understanding of the species,
and contribute to its conservation. The first of the projects assumed responsibility for the development both of a conserva-
tion program in Espirito Santo State and of comparative analyses of the conservation genetics of all northern muriquis.
The second was responsible for developing a long-term field study of a wild population of muriquis inhabiting possibly the
only large non-fragmented forest for the species-the Rio Doce State Park, Minas Gerais-in addition to locating other
remnant populations of northern muriquis. The third project involved a synthesis of the ecology of the genus Brachyteles,
and conservation measures for the northern muriqui population at the RPPN-FMA, Caratinga, now estimated to support
approximately 25% of the remaining animals of the species. Muriquis at this site have been intensively studied since the
early 1980s, and the analyses of Strier (1993/1994) have shown that the only factor now hampering the continued growth
and expansion of the RPPN-FMA muriqui population, and thus its long-term survival, is the availability of habitat. The
RPPN-FMA is an island surrounded by open pastures, and a major goal now is to regenerate forest within and around the
Reserve and to establish faunal corridors to connect it to neighboring forests.

The RPPN-FMA is one of the five protected forests encompassed by the "Muriqui Nucleus," an area of nearly 1 million ha
that contains the largest remaining northern muriqui populations in the species' entire range. The four other protected areas
are a national park that extends across the state borders of Minas Gerais and Espirito Santo (Capara6), two state parks (Rio
Doce and Serra do Brigadeiro), and a second private reserve in Minas Gerais (Mata do Sossego). The Muriqui Nucleus was
conceived by researchers Luiz Paulo Pinto and Adriano Paglia at Conservation International- Brazil, which, with the partici-
pation of government officials, NGOs and private landowners, are now actively engaged in the challenge of expanding and
linking these protected areas. The product of these efforts will be the establishment of conservation connectivity across the
Muriqui Nucleus, providing critical habitat for the healthy expansion of populations of muriquis and other species.

This initiative and several others were discussed during a workshop held in Belo Horizonte in May of 2005, with the support
of Conservation International-Brazil and PROBIO. Jean Philippe Boubli organized the workshop with the goal of develop-
ing a global perspective for future discussions on the conservation and management of the two muriqui species. Some of the
presentations given at this workshop are included in this volume.





Neotropical Primates 13(Suppl.), December 2005


Another recent product is the completion of a management plan for northern muriquis, coordinated by S&rgio L. Mendes
and discussed and revised at the May 2005 meeting of the Committee for the Atlantic Forest Atelids. The plan suggests a
number of measures, including biomonitoring studies of demography, genetics, parasites, and hormones, as well as practi-
cal activities such as management in captivity, environmental education, and habitat restoration. This Management Plan
constitutes the basis for the preparation of an Action Plan, which will be the next step in organizing an integrated system for
monitoring and conserving the northern muriqui.

The articles in this special issue of Neotropical Primates are a sample of the diversity of approaches being taken for the con-
servation of muriquis. Clearly, tremendous advances in our knowledge of this species and its conservation needs have been
made. Yet, this collection also emphasizes the simultaneous need for ongoing efforts on behalf of northern muriquis, and
greater investment in comparative studies on southern muriquis. Our ability to develop an informed conservation manage-
ment strategy for both species of muriqui will depend upon the continuity of integrated research and conservation efforts
that involve partnerships among universities, government, and nongovernmental organizations. There is also an urgent need
to incorporate more extensive assessments of local population genetics into management plans, and to establish priorities
among protected populations to ensure they have the habitat they need to expand to sizes which can provide some guarantee
for their long-term health and survival.

The future of muriquis looks more promising today than it did a quarter century ago, but it is still, by no means, secure.
Our task for the next 25 years is clear.

References

Aguirre, A. C. 1971. 0 mono Brachyteles arachnoides (E. C.. .. ). Situaado Atual da Especie no Brasil. Academia Brasileira
de Ciencias, Rio de Janeiro.
Coimbra-Filho, A. F. 1972. Mamiferos ameagados de extingao no Brasil. In: Espicies da Fauna Brasileira Ameacadas de Extin-
tao, Academia Brasileira de Ciencias (ed.), pp.13-98. Academia Brasileira de Ciencias, Rio de Janeiro.
Galindo-Leal, C. and CSmara, I. G. (eds.). 2003. State of the Hotspots: The Atlantic Forest of South America. Island Press,
Washington, DC.
Myers, N., Mittermeier, R. A., Mittermeier, C. G., Fonseca, G. A. B. and Kent, J. 2000. Biodiversity hotspots for conserva-
tion priorities. Nature, Lond. 403: 853-858.
Paglia, A. P. 2005. Panorama geral da fauna ameagada de extingao no Brasil. In: Lista da Fauna Brasileira Ameacada de
Extinfao-Incluindo a Lista das Quase Ameacadas e Deficientes em Dados, A. B. M. Machado, C. Shares Martins and
G. M. Drumond (eds.), pp.17-22. Fundagao Biodiversitas, Belo Horizonte.
Kleiman, D. G. and Rylands, A. B. (eds.). 2002. Lion Tamarins: Biology and Conservation. Smithsonian Institution Press,
Washington, DC.
Strier, K. B. 1993/1994. Viability analyses of an isolated population of muriqui monkeys (Brachyteles arachnoides): implica-
tions for primate conservation and demography. Primate Conserv. (14/15): 43-52.
Strier, K. B., Mendes, S. L., Boubli, J. P. and Dias, L. G. 2006. The northern murqiui, Brachyteles '.' .-'.. (Kuhl, 1820).
In: Primates in Peril: The World's 25 Most Endangered Primates, 2004-2006, R. A Mittermeier, C. Valladares-Pidua,
A. B. Rylands, A. A. Eudey, T. M. Butynski, J. U. Ganzhorn, R. Kormos, J. M. Aguiar, and S. Walker (eds.), pp.10, 23.
Primate Conserv. (20): 1-28.
Valle, C. M. C., Santos, I. B., Alves, M. C., Pinto, C. A. and Mittermeier, R. A. 1984. Algumas observagoes sobre o com-
portamento do mono (Brachyteles arachnoides) em ambiente natural (Fazenda Montes Claros, Municipio de Caratinga,
Minas Gerais, Brasil). In: Primatologia no Brasil, M. T. de Mello (ed.), pp.271-283. Sociedade Brasileira de Primatologia,
Brasilia.








Neotropical Primates 13(Suppl.), December 2005 7

DIRECTIVES FOR THE CONSERVATION OF THE NORTHERN MURIQUI, BRACHYTELES
HYPOXANTHUS (PRIMATES, ATELIDAE)

Sergio L. Mendes', Fabiano R. de Melo2, Jean P. Boubli3, Luiz G. Dias Karen B. Strier5,
Luiz Paulo S. Pinto6, Valeria Fagundes1, Braz Cosenza2 and Paulo De Marco Jr7

1Departamento de Ciencias Biol6gicas, CCHN, Universidade Federal do Espirito Santo, Vit6ria, Espirito Santo, Brazil, and
Institute de Pesquisas da Mata Atlhntica (IPEMA), Vit6ria, Espirito Santo, Minas Gerais, Brazil, e-mail: gmail.com>
2Universidade do Estado de Minas Gerais- Carangola, Minas Gerais, Brazil
3Department of Anrl-i ..p..1. .;-,, The University of Auckland, New Zealand
"Fundagao Biodiversitas, Belo Horizonte, Minas Gerais, and The Tropical Ecological Assessment and Monitoring (TEAM)
project (CI / UFMG), Belo Horizonte, Minas Gerais, Brazil
5Department ofAnrl-..i p..1. .;,-, University of Wisconsin-Madison, Madison, Wisconsin, USA
6Conservagao Internacional (CI-Brasil), Belo Horizonte, Minas Gerais, Brazil
Universidade Federal de Goias, Goiania, Goias, Brazil


Abstract

There are two species of muriqui, Brachyteles-the northern muriqui (B. .'i .... .-.'... i and the southern muriqui (B. arach-
noides). The northern muriqui is the most endangered of the two. The species originally occurred through most of the Atlan-
tic forest in the south of the state of Bahia, eastern Minas Gerais, and south central Espirito Santo. Hunting and widespread
loss of its native forest means that today just a few small and isolated populations remain, with poor chances of survival
in the long term. Currently the northern muriqui can be found in 12 places, six on private land, three in state protected,
and three in federal protected areas. Combined, these areas total about 160,000 ha and a minimum known number of
855 individuals. The known population has increased significantly in the last five years, but the total is still very small and
fragmented for long-term viability-no single population exceeds 500. In this article we report on the areas where they are
known to occur, the main threats to them, and the conservation measures that have been proposed to avoid the premature
extinction of the species.


Key Words- primates, Brachyteles, conservation, Atlantic forest, Brazil


Introduction

Muriquis are endemic to the Brazilian Atlantic forest, oc-
curring in a number of forest types, from the humid coastal
formations of the Serra do Mar to the semideciduous for-
ests inland in the states of Sao Paulo and Minas Gerais,
extending from the south of the state of Bahia to northern
Parand (Aguirre, 1971). Two species are recognized-the
southern muriqui (Brachyteles arachnoides) and the north-
ern muriqui (B. hypoxanthus)-differentiated by the pres-
ence of a vestigial pollex and spotty pigmentation on the
face and perineum in B. .'A .... .-.'*.. (Aguirre, 1971; Ry-
lands etal., 2000; Groves, 2001).

The range of the northern muriqui (B. .'\ .... .-.'... i covers
the Atlantic forest of the states of Minas Gerais, Espirito
Santo and Bahia, excluding the lowland forests in the ex-
treme south of Bahia and northern Espirito Santo. Accord-
ing to Aguirre (1971), the northern limit to its range was
probably the Rio Jequirigi basin, which flows into the Bafa
de Todos os Santos, and including the forests of the right
bank of the Rio Paraguacu. The southern limit is more


poorly defined, but it probably extended to the Serra da
Mantiqueira, in southern Minas Gerais, near to the state
boundaries with Rio de Janeiro and Sao Paulo.

Almost all of the information we have on the ecology,
behavior, reproduction and demography of the northern
muriqui comes from a single population at the Caratinga
Biological Station (Reserva Particular do Patrimonio Natural
Feliciano Miguel Abdala), Minas Gerais. There, muriquis
have been systematically monitored and researched since
1982 (Fonseca, 1985; Strier, 1987a, 1987b, 1993/1994,
1999, 2000; Strier et al., 2002, 2006).

The extinction of the muriqui throughout a large part of its
range is a result of the destruction of its forests and, with its
large size, hunting (Aguirre, 1971; Mittermeier et al., 1987;
Lane, 1990). The Atlantic forest, originally extending for
more than 1,300,000 km2 along the Brazilian coast, has
been reduced to fragments that today total a mere 7.5%
of its original cover (Myers et al., 2000). The population
growth rate of the muriqui is at best slow (Strier, 1996)
contributing to its vulnerability to extinction. Its capacity







to use secondary forests, even those in relatively early suc-
cessional stages, however, has allowed for the survival, and
even recovery, of small, isolated populations. Eliminating
the causes of decline such as hunting and epidemic dis-
eases, muriqui populations can grow and thrive in regener-
ating, remnant forests.

Protected Areas for the Northern Muriqui

The northern muriqui is today known to survive in 12 lo-
calities, six on private land, three in state protected areas,
and three in federal protected areas (Table 1, Fig. 1.). The
12 areas total approximately 160,000 ha, providing forest
for at least 855 individuals. Although, the numbers of wild
muriquis known to be surviving have increased consider-
ably in the last five years, the total population is still small,
and no single population is considered to be viable in the
long-term, none even close to 500 or more in size. Here we
describe each of 12 known populations and discuss their
conservation status.

1. Alto Cariri
This forest, of about 18,000 ha, is in the extreme north-
east of Minas Gerais, extending across the border with the
state of Bahia (1624'S, 40003'W). It has been identified
as of high priority for biodiversity conservation, and both
the State Forestry Institute of Minas Gerais (Instituto Es-
tadual de Florestas- MG) and the Brazilian Institute for
the Environment (Instituto Brasileiro do Meio Ambiente e
dos Recursos Naturais Renovdveis-IBAMA) are consider-
ing the creation of a protected area there. The vegetation
is predominantly dense evergreen forest; much of it well
preserved, even though some areas have suffered selective
logging. Alto Cariri takes in parts of the municipalities of
Santa Maria do Salto, in Minas Gerais, and Guaratinga, in


Neotropical Primates 13(Suppl.), December 2005

Bahia. At least seven muriquis were seen there, but due to
the large size of the forest (in relative terms) it is probable
there are many more, and a census is needed to determine
the exact size of the population (Mendes et al., 2004). The
creation of protected areas is the major priority for this
region.

2. Mata Escura Biological Reserve
The Mata Escura Biological Reserve covers some
50,890 ha in the municipalities of Jequitinhonha and
Almenara, in the Rio Jequitinhonha valley, Minas Gerais
(1620'S, 4100'W). Two muriquis were seen there in
April 1999 at the headwaters of a stream called C6rrego
Duas Barras (Melo et al., 2002). Three were seen there on a
subsequent occasion, but in 2000 a second group of about
15 muriquis was located along the banks of the C6rrego
Mata Escura (Melo, 2004). This group was later found to
have 25 members. It is possible that further groups will be
found in other valleys in the reserve. The C6rrego Duas
Barras has about 1,500 ha of forest in the municipality
of Jequitinhonha, and the Mata Escura valley has about
1,000 ha. The principal threats are fire, hunting, selective
logging, and unregulated and destructive tourism. The
priority measures for the implementation of the biologi-
cal reserve include building some physical infrastructure,
increasing the policing of the area, resolving landownership
and indemnities, and counting, mapping and studying the
muriqui groups.

3. Fazenda Cdrrego deAreia
There is about 450 ha of seasonal semideciduous forest
at the Fazenda C6rrego de Areia. It is near the transition
zone of the Cerrado and Atlantic forest (1826'S, 4225'W,
altitude 388-805 m above sea level), in the municipality of
Peganha, Minas Gerais. The farm is privately owned, and


Table 1. Confirmed populations of the northern muriqui*.
# Locality State Owner Area (ha) Minimum population
1 Alto Cariri MG/BA Private 18,000 7
2 Mata Escura Biological Reserve MG IBAMA 50,890 28
3 Fazenda C6rrego de Areia MG Private 494 13
4 Rio Doce State Park MG IEF-MG 35,976 124
5 Caratinga Biological Station (RPPN Feliciano Miguel Abdala) MG Private 957 226
6 Augusto Ruschi Biological Reserve and vicinity ES IBAMA 3,573 14
7 Santa Maria de Jetiba ES Private +2,0001 84
8 Fazenda Esmeralda MG Private 44 3
9 RPPN Mata do Sossego MG Fundacao Biodiversitas 180 41
10 Capara6 National Park ES IBAMA 31,853 82
11 Serra do Brigadeiro State Park MG IEF-MG 13,210 226
12 Ibitipoca State Park MG IEF-MG 1,4882 7
Total 158,665 855
*Data from October 2005.
BA = Bahia, MG = Minas Gerais, ES = Espirito Santo, IBAMA = Brazilian Institute for the Environment, IEF-MG = Minas Gerais State Forestry
Institute.
lIn Santa Maria de Jetiba the area (+2,000 ha) encompasses a group of 13 partially isolated forest fragments.
2 The muriqui population of Ibitipoca is largely in forest fragments outside the state park.





Neotropical Primates 13(Suppl.), December 2005 9

about 230 km from the state capital, Belo Horizonte. The and agroforestry, for example), and the creation of a private
forest is surrounded by coffee plantations and cattle pas- natural heritage reserve (Reserva Particular do Patrimonio
ture. The main threats are fire and selective logging. Hirsch Natural- RPPN) to protect the remaining forest patch.
et al. (2002) registered 13 muriquis there in 2001. Priority
measures for this area include a monitoring program for the 4. Rio Doce State Park
few muriquis remaining on the farm, the provision of in- The Rio Doce Park covers parts of the municipalities ofMar-
centives for less harmful uses of the soil (organic cultivation likria, Tim6teo and Dionisio, in Minas Gerais (4238'W


Gw maw


Figure 1. Historical and current records of the northern muriqui. Muriquis occur in Itatiaia National Park (#13), but the species has yet
to be confirmed there.







and 4828'W, 19045'S and 19030'S). It is one of the most
important remnants of Atlantic forest in the entire state,
with 35,976.43 ha, limited to the north by the Rio Piraci-
caba, to the east by the Rio Doce, and to the south and west
by extensive eucalyptus plantations and cattle pasture. Past
surveys have indicated a very low population density for the
muriquis (Hirsch, 1995). However, studies in recent years
have shown that there are at least 12 groups there, totaling
a minimum of 124 individuals (Dias et al., 2005). Despite
the considerable infrastructure in the park for fire detec-
tion, big forest fires continue to be the greatest threat to
the wildlife there. Hunting is also still significant, especially
in the north of the park, close to large urban centers, and
along the 22-km road which bisects the park, connecting
Pingo D'igua to Tim6teo. Long-term measures for action
in the park include research on the ecology and behavior of
the muriqui groups there, resolution of landownership and
indemnities, improved policing, and the upgrading of the
municipal fire brigade to combat the forest fires, besides a
broad environmental awareness and education program for
the communities, farms and towns around the park.

5. Caratinga Biological Station Reserva Particular do
Patrim6nio Natural Feliciano Miguel Abdala (EBC/RPPN-
FMA )
The privately-owned, semideciduous, 957-ha forest of the
EBC/RPPN-FMA is in the municipality of Caratinga in
Minas Gerais (1950'S, 4150'W). It is mostly secondary,
in different states of succession, surrounded by pasture and
coffee plantations. In 2001, the forest was turned into the
Private Natural Heritage Reserve "Feliciano Miguel Abdala"
(RPPN-FMA). The ecology, behavior, reproduction, and
demography of the largest of the groups there (Grupo do
Matao) have been studied consistently since 1982 (Strier et
al., 2002). It has more than tripled in size in 20 years, from
22 to more than 70 individuals, due to low mortality and
high fecundity, and the increase in births and survival of
offspring. The same growth evidently occurred in a second
group (Grupo do Ja6) that had about 18 individuals in
the early 1980s, but numbered 73 in 1999 (Strier et al.,
2002). In January of 2005, the muriqui population at the
EBC/RPPN-FMA reached 226 individuals, in four mixed
groups of 37 to 77 and a group of eight males that associ-
ates with two of the mixed groups (Strier et al., 2006). Be-
sides the long-term studies coordinated by Karen B. Strier,
Jean. P. Boubli has been leading a project supported by
the nationwide Project for the Conservation and Sustain-
able Use of Brazilian Biological Diversity (Projeto de Con-
servafdo e Utilizafdo Sustentdvel de Diversidade Bioldgica
Brasileira PROBIO) of the Ministry of the Environment
(MMA), coordinated through the Instituto Driades. The
aims of the PROBIO/MMA project are (1) to synthesize
our understanding of the ecology of Brachyteles, mainly of
those at the EBC/RPPN-FMA, so as to develop a global
perspective that can support decisions and plans for the
conservation of muriquis throughout their geographic
range, (2) to set up a pilot project for the recuperation of
degraded areas, promoting their return to forest habitat for


Neotropical Primates 13(Suppl.), December 2005

the muriquis at the EBC/RPPN-FMA, and (3) to formu-
late a proposal to expand forest recuperation and natural
habitat conservation to areas neighboring the EBC/RPPN-
FMA, that will allow for conditions to create wildlife cor-
ridors to support a metapopulation of muriqui groups ex-
tending across the region. Future measures that we suggest
include a more intensive biomonitoring of the population,
habitat restoration with a view also to provide connectivity
with forest fragments on neighboring farms, and the syn-
thesis of a formal action plan for the RPPN.

6. Augusto Ruschi Biological Reserve
In the municipality of Santa Teresa, Espirito Santo, the
then Nova Lombardia Biological Reserve was created by
Decree number 87.589 of 20 September 1982 (19045'S
and 2000'S, 4027'W and 4038'W). The reserve is
3,573 ha of dense montane evergreen gorest (Floresta
Ombrofila Densa Montana), on very high relief with steep
slopes, valleys and rocky outcrops, at altitudes that range
from 780 m to 1,050 m above sea level (Brasil, 2007).
Aguirre (1971) recorded the presence of muriquis there,
estimating about 150-180 individuals. Visiting the reserve,
Mittermeier et al. (1987) only heard vocalizations, but were
able to confirm a minimum of 10 individuals through re-
ports of sightings by the park guards. Pinto et al. (1993)
found two groups there, each of four to seven individuals.
The only information we have had since then that indi-
cates the continued presence of muriquis comes from the
park guards. With the lack of more precise information, we
can only indicate a population of about 10. In April 2005,
Vieira and Mendes (2005) reported another group of four
muriquis in a privately-owned forest near to the biologi-
cal reserve, suggesting that the reserve and the neighboring
forests have more muriquis than we have suspected to date.
Suggested actions: a detailed census of the population,
intensified policing of the reserve, and the development of
an environmental awareness and education program for the
buffer zone.

7. Santa Maria deJetibd
Santa Maria de Jetibd is a municipality in the central, mon-
tane region of the state of Espirito Santo. The municipal
capital is 2002'S and 4041'W. It lies in a geomorphologi-
cal formation known as the Crystalline Complex, with alti-
tudes ranging from 600 to 1,200 m, in the phytogeograph-
ic domain of montane and submontane Atlantic forest. The
region was colonized in the 19th century by European im-
migrants, many from what was then Pomerania, establish-
ing a system of small farms and family agriculture. Despite
the intense fragmentation of the forests in the region, about
30 to 40% still has native forest in middle to advanced
stages of succession. The situation in the municipality of
Santa Maria de Jetibi is unusual in that the muriquis are
surviving in small forest fragments of 60 to 350 ha, because,
it would seem, the human population of the region has no
tradition of hunting, and frowns upon anybody who does.
The muriquis have been found in at least 13 forest frag-
ments throughout the entire municipality of Santa Maria





Neotropical Primates 13(Suppl.), December 2005

de Jetiba, with a minimum population estimated at 84 in-
dividuals (Mendes et al., 2005). The number of muriquis
seen in these fragments varies from one to 16. The solitary
individuals seen are females, and solitary females have been
seen even in fragments with groups of muriquis. Reports
of muriquis occurring in another 11 fragments have yet to
be confirmed but suggest a total population of more than
100 individuals. Suggested actions: Further surveys and
censuses in the region, development of an environmental
education program, promotion of ecotourism, develop-
ment of a program to carry out studies necessary for popu-
lation management, studies of dispersal using field data and
spatially-explicit models, work towards the creation of pro-
tected areas, and help promote socio-economic activities
compatible with biodiversity conservation.

8. Fazenda Esmeralda, Rio Casca, Minas Gerais
The only forest fragment of the Fazenda Esmeralda that
still has muriquis is 44 ha. The forest, about 30 km north
of the town of Rio Casca, is seasonal and semideciduous
and surrounded by monocultures and pasture. On the top
of a small hill, the maximum altitude is 480 m above sea
level. The forest has suffered a long history of depreda-
tion and disturbance during the economic cycles driven
by coffee and maize and, most recently, by sugar-cane, be-
sides selective logging for timber and charcoal during the
1960s and 70s. A few sparse forest fragments remain on the
farm, isolated by crops and open fields. The fragment con-
taining the muriquis is a mosaic of different successional
stages, and dense in lianas. The first record of their occur-
rence there was provided by Aguirre (1971), who indicated
7-8 individuals. Subsequent studies on the single group
from 1983 to 2003 witnessed a decline in the population
from 18 to just three: two adult males and an adult female,
all old (Melo et al., 2005). The population was considered
no longer viable, and in 2003 the Committee for the Con-
servation and Management of the Muriqui recommended
that they be removed and taken into captivity. The main
threats to the muriquis have been hunting, forest fires,
selective logging, predation and harassment by farm dogs
and, besides, the very small size of the forest. Suggested
action: capture and remove the remaining muriquis and
incorporate them into a captive breeding program.

9. RPPNMata do Sossego
The Mata do Sossego Private Natural Heritage Reserve
(RPPN) is in the municipality of Simon6sia (4205'W,
2004'S). Although the registered area for the RPPN is
180 ha, there are forests around it which form a single
block of forest of about 800 ha. Use of the soil around the
reserve is mainly dedicated to coffee plantations, and the
major threat to the muriquis comes from fires set in the dry
season by hunters. In 1984, the population was estimated
to be about 21 individuals (Mittermeier et al., 1987). Pet-
roni and Steinmetz (2000) indicated a minimum number
of 20, and the most recent census counted a group of 41
(Dias et al., 2005). Suggested actions: a long-term study
on their ecology and behavior; demographic monitoring of


the muriquis in the reserve; negotiation with the landown-
ers to consider the creation of further private reserves or
the acquisition of the forested areas; establishment of forest
corridors; population management.

10. Caparad NationalPark
The park extends across the state border of Espirito Santo
and Minas Gerais in a montane region, part of the Serra da
Mantiqueira (20019' and 2037'S, 41043' and 4153'W).
The park is 31,853 ha, 60% (18,200 ha) of which is in
southwestern Espirito Santo, and the rest is in Minas Gerais.
Predominantly montane, vegetation types include dense
evergreen forest, montane forest, semideciduous seasonal
forest and high altitude grassland (campos de altitude). The
occurrence of muriquis there was reported by Mittermeier
et al. (1987) based on information from the park guards of
a group of at least 12. Further research is underway that is
indicating the presence of muriquis in nine locations on
the Espirito Santo side of the park. They have been con-
firmed for four of the valleys: Vale do Ribeirao Calgado,
Vale do C6rrego Jacutinga, Vale do C6rrego Santa Marta,
and Pedra do Facao. In the first of these, there are at least
two groups, with a minimum population of 40 individu-
als, seen at altitudes of 1,000 to 1,800 m above sea level.
Muriquis have been seen 18 times in the Vale do Jacutinga,
indicating the presence of one group with a minimum size
of 42. We don't know the number of muriquis in other
valleys. The data from the Capara6 National Park are still
preliminary, and suggest the population may be very much
larger. Worrying, however, are the signs of hunters inside
the park. The hunting of muriquis was reported in the park
a few years ago. Suggested actions: carry out a systematic
census of the entire park; set up an environmental educa-
tion program; and invest in improving the policing of the
park in the part on the Espirito Santo side.

11. Serra do Brigadeiro State Park
The Serra do Brigadeiro State Park in southern Minas
Gerais is 13,210 ha. It has a perimeter of 156.9 km, and
altitudes range from 1,000 to 2,000 m above sea level
(20033' to 2100'S; 42040' to 4020'W). The forest there is
fragmented. The majority is seasonal semideciduous forest,
but there are some areas above 1,400 m altitude that show
characteristics of dense montane evergreen forest. Records
from the last two years show that there are at least seven
groups of muriquis, and a minimum population of 226
(Dias etal., 2005). The principle threats include forest fires,
hunting, selective logging, squatters, unregulated tourism,
and subsistence cattle-farming. Suggested actions: more
regular and systematic monitoring of the muriqui popula-
tion; resolution of landownership issues; strengthening of
the policing of the park; improvement in capacity to pre-
vent and combat forest fires; and the development of an
environmental education program.

12. Ibitipoca State Park
This park, of 1,488 ha, lies between the plateaus of Itatiaia
and Andrelhndia (21040' to 2143'S, 43052' to 4354'W,







altitudes 1,050-1,784 m above sea level). The predomi-
nant vegetation is high altitude grassland, with gallery
forest along the rivers and streams. In 1995, Fontes et al.
(1996) saw a female muriqui three times in a forest of 80
ha in the center of the park. In 2002, Mendes et al. (2003)
saw a group of nine in a small forest called the Mata dos
Luna on the property of Carlos Repetto near to the north-
ern boundary of the park. They were also told of a group
in another area, aptly called the Mata dos Monos. Oliveira
(2003) also mentioned a group of 10 muriquis in a forest
neighboring the park, believed to be the same as was seen
by Mendes et al. (2003). Ferraz et al. (2005), however, in-
dicated that the group consisted of only seven individuals.
The vegetation found in most of the park is not ideal for
muriquis, and it is evident the preservation of the muriqui
in this region will depend on protecting the forest fragments
on the properties around the park. The priority, therefore,
for this area is to carry out a more precise and systematic
census of the muriquis, and to adopt measures for the pro-
tection of the forest fragments and to increase the connec-
tions among them. The presence of solitary females in a
small fragment of forest in the park indicates that there is
a lack of opportunities for dispersal and reproduction else-
where. Suggested actions: a census of muriquis around the
park; expansion of the park to include neighboring forest
fragments; the creation of private natural heritage reserves
(RPPNs); and the promotion of conservation measures by
the local landowners and farmers.

13. Itatiaia National Park
The Itatiaia National Park (28,155 ha) is in southern Minas
Gerais, in the municipalities of Alagoa, Bocaina de Minas,
and Itamonte, extending across state border into southeast
Rio de Janeiro in the municipalities of Resende and Itatiaia
(22016' to 2228'S, 44034' to 4442'W). It is the oldest
national park in Brazil (1937), located in the Serra da Man-
tiqueira, with altitudes ranging from 650 to 2,780 m above
sea level. Five vegetation types have been described in the
park: dense montane, high montane, and mixed evergreen
forest, seasonal, semideciduous forest, and high altitude
grasslands at elevations above 1,600 m. The main threats
to the fauna and flora of the park are fires, destructive tour-
ism, illegal clearings and construction, and palm heart col-
lectors. It has not been possible to clearly define whether
the muriquis there are northern or southern. The very few
sightings have not even allowed for a minimum population
estimate. This makes a thorough census of the park and its
muriquis a very high priority. Suggested actions: a census
to determine the species occurring there; to map the groups
and count their numbers; set up a long-term monitoring
program for the groups; and resolve issues still pending
concerning landownership and domain.

Priority Actions

A Population and Habitat Viability Assessment (PHVA)
workshop for the muriqui was held in Belo Horizonte
in May 1998 (Rylands et al., 1998), and in 2002, the


Neotropical Primates 13(Suppl.), December 2005

Brazilian Institute for the Environment (IBAMA) set up
the Committee for the Conservation and Management of
the Muriqui (Oliveira et al. 2005). From 2001 to 2003 the
Project for the Conservation and Sustainable Use of Brazil-
ian Biological Diversity (Projeto de Conservafdo e Utilizaado
Sustentdvel da Diversidade Bioldgica Brasileira- PROBIO),
of the Ministry of the Environment (MMA), approved fi-
nancing for three projects for the conservation and man-
agement of the northern muriqui. Two important meetings
resulted from this, the first in January 2003 in Santa Maria
de Jetibi, Espirito Santo, and the second in March 2004 in
Belo Horizonte. They provided the information and direc-
tives for the elaboration of a management plan for the spe-
cies. As such, the following discussion of the priority meas-
ures for the conservation of muriquis is the result of the
thoughtfulness, dedication and expertise of the numerous
institutions and people who took part in these meetings.

Monitoring. Surveys and censuses
Recent studies have resulted in the discovery of new popu-
lations of muriquis. In the last 10 years, our estimate of the
total population of the species has increased from about
300 to at least 855, and from seven to 12 localities. We owe
this to more systematic surveys and to new technologies
such as the use of playback-playing recordings of their
vocalizations in the forest so as to increase the chances of
locating them. New found areas in eastern Minas Gerais,
and the montane regions of Espirito Santo and Bahia re-
quire further surveys, and we recommend GIS modeling
tools to orient and prioritize the areas to be surveyed.

Monitoring and conservation status assessment
Currently there are research programs on, and conservation
initiatives for, muriquis being carried out in six locations,
four in Minas Gerais (RPPN Feliciano Miguel Abdala,
RPPN Mata do Sossego, and Serra do Brigadeiro and Rio
Doce state parks) and two in Espirito Santo (Capara6 Na-
tional Park and Santa Maria de Jetibi). These studies and
initiatives cover about 90% of the entire population of
B. '... .-'..Continuity for these projects is vital. The
definition of a basic protocol for the collection of ecologi-
cal and behavioral data is important to allow us to compare
the results of the programs in the different areas; essential
if we are to evaluate their contributions and efficacy in im-
proving the status of the species. Initially we need to have
estimates of the total population and some definition of the
population structure in the localities where long-term stud-
ies have been set up. The first is possible with the knowl-
edge that we already have, provided that some additional
information can be obtained as outlined below. An under-
standing of population structure and demography will be
possible based on the few groups which have been subject
to long-term studies. It is vital that some guarantees be put
into place for the continuity of these long-term studies.
We suggest that the six localities mentioned above be tar-
geted for funding to this end. One or two groups should be
closely monitored for their social structure in each of the
six areas-either continuously or at least through detailed





Neotropical Primates 13(Suppl.), December 2005

counts every five years. The total population, of course,
should also be closely monitored over the long-term, with
censuses every five years. Monitoring the total population
will allow us to track population changes, and monitor-
ing population structure and demography will allow us to
understand the nature of the changes. The causes can only
be tracked by understanding the availability of resources
in terms of food and habitat, and the threats to them both
indirect (forest degradation and loss) and direct (hunting).
Changes in habitat availability can be assessed every five
years using satellite imagery, and monitoring the quantity
and quality of the remaining forests in the areas where the
muriquis still occur.

Genetic studies
The analysis of intra- and inter-population genetic diversity
is the first step to identifying what we may consider "evolu-
tionarily significant units"; genetically distinct populations
which need to be protected. Currently there are genetic
samples available from only three of the twelve known
northern muriqui populations; all in the DNA Bank of the
Department of Biological Sciences of the Federal Univer-
sity of Espirito Santo. Of the three, two have been subject-
ed to genetic studies using a mitochondrial DNA marker,
demonstrating genetic differences between the muriquis
of Santa Maria de Jetibi and the EBC/RPPN-FMA (Paes,
2005). The identification of variable genetic loci will
provide a useful means to measure genetic variation and
population differentiation, and allow for an understand-
ing of the evolutionary relationships which need to be
conserved. As such, we consider that a knowledge of the
genetic profiles of all of the known muriqui populations,
using at least two genetic markers (one mitochondrial, the
other nuclear), is vital for the conservation and manage-
ment of the species. This is also vital when using the genetic
profiles of individual muriquis to guide translocations and
reintroductions whenever they are deemed expedient. The
Laboratory of Animal Genetics of the Federal University of
Espirito Santo has developed a protocol for the extraction
of fecal DNA in Brachyteles that is already being applied in
genetic studies of the muriquis at Santa Maria de Jetibi and
the Caratinga Biological Station (Chaves et al., 2006). We
propose the establishment of a single protocol for genetic
studies using fecal material for all of the muriqui popula-
tions (Fagundes, 2005).

Parasitological studies
Parasitological studies can provide a good understanding of
the state of health of the muriquis, and monitoring para-
site loads in the different populations is an essential ele-
ment for their conservation and management (Stuart and
Strier, 1995; Santos et al., 2004a, 2004b). Important too
is to monitor the muriquis for the presence of parasites of
humans and domestic animals. The northern muriqui is
largely limited now to forest fragments, with more or less
frequent intrusion and interference by people and their ani-
mals, both by their presence and the pollution of the streams
which run through them, where muriquis sometimes drink


(Santos et al., 2004a, 2004b). The disease risks are high,
making frequent parasitological monitoring a must. This
can only be done by institutions which have experience in
the collection and identification of primate parasites. With
the appropriate protocols for collection and preservation,
however, all researchers and field teams should carry out
campaigns for the collection of fecal material (systematical-
ly to allow for the detection of any trends), and send them
to appropriate participating laboratories. Ideal would be the
establishment of a muriqui parasite data bank, accessible to
all who work on the species. When infection with human
or domestic animal parasites is detected, measures should
be taken which would include health and environmental
education for the local communities, reducing or, better,
eliminating the sources of contamination of the streams,
and stopping domestic animals entering the forest.

Hormonal monitoring
The hormonal studies of the muriquis at the EBC/RPPN-
FMA by Strier and Ziegler (1997, 2000; also Strier et al.,
2003; Strier, 2005) have contributed enormously to our
understanding of the reproductive strategies of these pri-
mates, of immense utility for wise management and con-
servation. The data they can obtain allow us to assess the
reproductive potential of the small populations, besides
providing insights regarding stress levels, experienced by
the muriquis for whatever reasons. As hormonal analyses
are expensive, however, widespread monitoring is impracti-
cal in the short term, but they can provide significant in-
sights concerning questions about the reproductive health
of specific populations and groups. For example, we can
study the variation in cortisol levels in different muriqui
populations to understand how they may relate to ecologi-
cal or demographic stress.

Population management
Some of the muriqui populations are very small, and
probably not viable in the long term. This is the case for
the Fazenda C6rrego de Areia, Ibitipoca State Park, the
Fazenda Esmeralda, and a number of fragments at Santa
Maria de Jetibi. It is possible the viability of some can be
maintained, if only minimally, with some sort of popu-
lation management, such as the introduction of animals
from elsewhere (reintroduction or translocation). Solitary
females have been found in forest fragments in Santa Maria
de Jetibi. They have dispersed from their natal groups and,
for lack of other groups to join, end up remaining alone.
In these cases, we should consider translocating muriquis
from other groups to join them-females not reproducing
are a significant loss to a species so threatened. The man-
agement of wild populations is a complex task, requiring
caution in terms of the medical and genetic health, and the
social stability of the animals involved.

Populational viability simulation
The risks of local extinction need to be assessed using the
population viability models now available. It is possible to
predict the persistence of the populations based on a variety







of parameters, and also to model the basic structure for the
metapopulation for the purposes of management planning.
Strier (1993/1994), for example, assessed the persistence
likelihood of the muriquis at the EBC/RPPN-FMA over
100 years, using the program VORTEX, and concluded
that the probability of extinction was low. The chances of
error are there, however, especially as the program used only
the first 12 years of data from the site. The analysis showed
that the carrying capacity (area of forest available) was the
main factor limiting population growth. Running a similar
model for the muriqui population at Santa Maria de Jetibdi,
P. De Marco Jr., using the same biological parameters as
those of the simulations made by Strier (1993/1994) but
including the real initial population sizes of each area,
found that the persistence probabilities were higher than
95% over 100 years in forests of more than 120 ha. The
simulation also indicated that if hunting pressure, endo-
gamic depression, and the probabilities of catastrophes are
low, the population tends to grow and reach stable levels
quite quickly. Even if the parameters used are to some
extent unreal, the simulations are of enormous value in de-
fining management priorities, and should be done for all
the existing populations being studied.

Captive breeding program
The establishment and maintenance of a captive breed-
ing program for muriquis should be seen as an important
measure complementary to efforts for their conservation
in situ (Pissinatti et al., 1998; Pissinatti, 2005). The aim
would be to rescue the muriquis being kept as pets and
in illegal menageries and zoos, as well as solitary females
in isolated forest fragments otherwise lacking a reproduc-
tive future. Isolated groups too small to be viable could
also contribute as founders. There needs, of course, to be
institutions with the conditions in terms of both person-
nel and infrastructure to receive these animals and to col-
laborate in a formal breeding program. For B. '... -'..
the Rio de Janeiro Primate Center (Centro de Primatologia
do Rio de Janeiro CPRJ/FEEMA), the first institution to
breed muriquis in captivity (Coimbra-Filho et al., 1993;
Pissinatti, 2005), and the Belo Horizonte Zoo (Fundadao
Zoo-Botdnica de Belo Horizonte) are already fully capable
of initiating a program of this sort. The principal aims of
these institutions with the capacity to maintain muriquis in
captivity would be rehabilitation and research.

Environmental awareness and education
Due to its charm, its size (the largest of the Neotropical
monkeys), and the fact that it is endemic, the muriqui is a
flagship species for the conservation of the Atlantic forest
(Valladares-Padua et al., 2003; Pinto et al., 2005). It can
be used very effectively for the 'call to arms' to conserve
a location or promote conservation actions in a region.
The rural communities where muriquis still survive inter-
fere to a greater or lesser degree just with their presence
and their use of natural resources, and in the case of parks
and reserves, tourists and visitors do the same. And there is
still clandestine hunting in many of the muriqui localities.


Neotropical Primates 13(Suppl.), December 2005

Awareness campaigns and environmental education pro-
grams are vital, and networking is important to exchange
experiences, success and failures in what are by their nature,
extremely creative initiatives, consistently requiring renewal
and modification. Another important aspect is advertising
the plight of the muriquis and their forests with all the rich
propaganda material and gadgets available today. Costs can
be reduced if the different partners share the material they
need. One model of a muriqui T-shirt for all, for example.
A third line of action is working with the media, reaching
a broader public, and more directly influencing the opin-
ions and attitudes of the local and regional communities:
something which of course needs careful and measured
planning so as to instill a lasting and solid appreciation for
the conservation measures that are required not just for the
muriquis but for the health of the natural landscapes as a
whole, benefiting the people living there.

Socioeconomic alternatives
In many cases the probabilities of the muriquis surviving in
the long term is low; because of their isolation or because
of the limited forest available to them. Landscape man-
agement, providing for the permanence and expansion of
the forests of the region, along with connectivity between
them, is as such vital. Interference in the natural landscape
requires socio-economic measures often sensitive and com-
plex. For this reason, the socio-economic realities of all the
regions where muriquis occur should be studied so as to
obtain the basic understanding of the context and poten-
tial for promoting initiatives which will favor biodiversity
conservation. One example is ecotourism and scientific
tourism that, when set up appropriately, can provide for
income and livelihoods but with low impacts on the wild-
life and forests. These activities can even provide incentives
and income for conservation measures such as habitat res-
toration. Businesses and sources of livelihoods can become
the allies, not the enemy, in working for the conservation
of the region. Besides its economic contribution, tourism is
educational, making landowners see the value of preserving
their forests and the muriquis. Small-scale tourism projects
need to be planned in collaboration with the people study-
ing the muriquis, with clear protocols to minimize the
impact on the muriquis and their forests, avoiding stress to
the animals, disease risks zoonosess), and the potential for
pollution and degradation of their habitats.

Habitat restoration
Habitat restoration is clearly an essential measure for the
muriqui populations residing in small and isolated forest
fragments. As mentioned, socio-economic considerations
are paramount in this case, besides thorough evaluations
of the technical and financial commitments involved, so
as to maximize the benefits to both the muriquis and local
communities. Studies in the EBC/RPPN-FMA, in Santa
Maria de Jetibi, C6rrego de Areia and the RPPN Mata do
Sossego, have shown that increasing the habitat available,
not just by planting and restoration but by providing cor-
ridors to neighboring forest patches, is fundamental for the





Neotropical Primates 13(Suppl.), December 2005

survival of the muriquis. Ample research and preparation
has to be made in each case, however, not just to develop
the appropriate reforestation techniques, but taking into
account the socio-economic and agropastoral context and
vocation of the land and the region.

Integration of results
We suggest that a formal information, data-sharing, net-
work be established among muriqui researchers and the in-
stitutions involved (NGOs and universities, for example).
This would make the transfer of, and access to, relevant
information and data more efficient and agile, and would
involve the commitment of researchers and institutions to
take on specific roles in compiling, organizing, and synthe-
sizing information for the benefit of all. The first step would
be the integration/connection of various specific data banks
already existing. A researcher or institution would take on
the responsibility for the maintenance of specific sections
of the overall data bank- one on the size and demography
of muriqui populations, another on ecological data, on ge-
netic data and analyses, on protected areas, and on regional
socioeconomics of different muriqui locations, for example.
The data can be classified in two distinct groups-one for
public access through a web site, and another for limited
access by qualified researchers and conservationists, mem-
bers of a muriqui conservation network.

Institutional Articulation

Any initiative to produce a management strategy for
a threatened endemic species must include collabora-
tion and partnerships of the institutions necessarily
involved-government, non-governmental organizations,
teaching and research institutions, and the private sector.
It is necessary to secure the enthusiasm of the local and
working communities. Combining forces and expertise,
and eliminating duplication of efforts, it is possible to
develop an inclusive approach for the protection of the
muriqui with a strong scientific underpinning. A signifi-
cant step was the Population and Habitat Viability Analysis
(PHVA) workshop (Rylands et al., 1998). The PHVA gave
rise to the Committee for the Conservation and Manage-
ment of the Muriqui (Comit para a Conservafao e Manejo
do Muriqui), the role of which is to discuss and suggest
strategies for ex situ and in situ conservation of the genus as
an advisory body to the Brazilian Institute for the Environ-
ment (IBAMA). In 2001, IBAMA created the Center for
the Protection of Brazilian Primates (Centro de Protefao de
Primatas Brasileiros), which also has a most important role
in providing for institutional articulation in relation the
conservation of the muriqui. The Center's mission is the
compilation, management and analysis of relevant infor-
mation concerning Brazilian primates to enable appropri-
ate decisions on, and measures for, their conservation.

In recent years, numerous non-governmental organiza-
tions have been addressing issues and elaborating global
and regional conservation strategies, focusing on aspects of


landscape ecology and biogeographic patterns for identify-
ing priority areas for the conservation of threatened and re-
stricted range species (Fundagao Biodiversitas, 1998; Con-
servation International do Brasil et al., 2000; Brazil, MMA,
2002). A number of NGOs have set up partnerships within
the campaign for "Zero Biodiversity Loss", and current
conservation initiatives for the northern muriqui provide a
good example. They are supported by three subprojects of
the Ministry of the Environment's Project for the Conser-
vation and Sustainable Use of Brazilian Biological Diver-
sity (Projeto de Conservacao Sustentdvel da Diversidade Bi-
oldgica Brasileira-PROBIO) coordinated by three NGOs,
the Instituto de Pesquisas da Mata Atlhntica- IPEMA, the
Fundagao Biodiversitas, and the Instituto Driades, in part-
nership with other NGOs and public and private institu-
tions, all of which have made a commitment to produce a
comprehensive action plan for the northern muriqui.

Universities and research institutions have also played a
fundamental role in generating information, in capac-
ity building, and in the design and execution of research
and conservation projects for the species. Notable is the
University of Wisconsin, which, in partnership with the
federal universities of Minas Gerais (UFMG) and Espirito
Santo (UFES), has been supporting studies of the muriquis
at the EBC/RPPN-FMA since 1982; the longest-running
of any primate field research program (Strier, 1999, 2005).
The muriqui conservation projects are also contributing to
progress in training researchers in population genetics and
its application to conservation biology. Universities and
NGOs are establishing centers for molecular biology as
applied to biodiversity conservation within the geographic
range of the northern muriqui.

It is important to point out the need for integration between
research and in situ conservation with ex situ conservation
measures, as exemplified in the work of the Rio de Janeiro
Primate Center (CPRJ/FEEMA). In situ conservation ini-
tiatives must work together with zoos and other research
centers to maintain representative sample collections of the
genetic variation of the species ex situ, to allow for future
interventions in depleted wild populations. Information
exchange is fundamental to establish the appropriate part-
nerships among the zoos, research centers and universities,
both in an outside of Brazil. Institutional articulation has
too been an essential element of private and public funds
for species protection.

Besides the PROBIO of the Ministry of the Environment
mentioned above, and the primate conservation projects
financed by the Margot Marsh Biodiversity Foundation,
there is also the more recent "Program for the Protection
of Threatened Species of the Atlantic Forest" (Programa de
Protecao das Espicies Ameafadas de Extinfdo da Mata Atldn-
tica Brasileira), a component of the Critical Ecosystems
Partnership Fund (CEPF) for biodiversity conservation
in the hotspots that have been identified by Conserva-
tion International (Myers et al., 2000; Mittermeier et al.,







2004)-a partnership of Conservation International, the
Global Environment Facility (GEF), the MacArthur Foun-
dation, The World Bank, and the Japanese Government,
that promotes alliances among organized communities,
NGOs, teaching institutions and the private sector. The
threatened species program of the CEPF, coordinated by
the Fundagao Biodiversitas and Centre for Environmental
Research of the Northeast (Centro de Pesquisas Ambientais
do Nordeste), was created to support projects for the protec-
tion and management of threatened species in the Atlantic
forest, with initial investments of about US$450,000. The
northern muriqui received funding for three projects within
the program. Lastly, the Committee for the Conservation
and Management of the Muriqui coordinated by IBAMA
has already approved the creation of a fund to support the
conservation of Brachyteles. The fund will be managed by
the committee itself, and will strive to obtain both private
and institutional donations from Brazil and overseas (O1-
iveira et al. 2005).

We have information sufficient to indicate the measures
necessary to maximize the chances of the local and regional
persistence of the northern muriqui populations in the At-
lantic forest of Bahia, Espirito Santo and Minas Gerais, but
this will serve for little if we cannot move forward now
and carry them out, combining forces, as we have to, to
promote the changes necessary for protection and conser-
vation of the species.

Acknowledgments

We are most grateful to E. F. Barbosa, L. S. Moreira, C. L.
S. Mendes, B. Coutinho, E Pontual, the late E. M. Veado,
J. A. Meira Neto, L. C. Bede, and M. M. Gomes for their
help. The work was supported by the Project for the Con-
servation and Sustainable Use of Brazilian Biological Di-
versity (Projeto de Conservacdo e Utilizacdo Sustentdvel de
Diversidade Biologica Brasileira -PROBIO) of the Brazilian
Ministry of the Environment (MMA), the Brazil Science
Research Council (Conselho Nacional de Desenvolvimento
Cientifico e Tecnoldgico- CNPq), the Gordon & Betty
Moore Foundation, the Zoological Society of San Diego,
the Brazilian Institute for the Environment (IBAMA), the
State Forestry Institute of Minas Gerais (IEF/MG) (Insti-
tuto Estadual de Florestas / Minas Gerais), the Fundagao
Biodiversitas, the Instituto Driades, the Centro de Estudos
Ecol6gicos e Educacao Ambiental (CECO), Bioprotegao,
Conquista, and Timex.

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Strier, K. B. 1987b. Ranging behavior of woolly spider
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Neotropical Primates 13(Suppl.), December 2005


MURIQUI POPULATIONS REPORTED IN THE LITERATURE OVER THE LAST 40 YEARS

Fabiano R. Melo1 and Luiz G. Dias2

'Universidade Federal de Goias, Campus Jatai, BR-364, Km 192, No. 3.800, Parque Industrial, Jatai 75801-615, Goias,
Brazil, e-mail:
2Tropical Ecology, Assessment and Monitoring Network- Rio Doce, Universidade Federal de Minas Gerais, Av. Ant6nio
Carlos 6627, Belo Horizonte 31270-901, MG, Brasil, e-mail:


Abstract

Aguirre (O mono Brachyteles arachnoides (E. C. ..r .., Situacao Atual da Espicie no Brasil. Acad. Brasil. Cienc., Rio de Janei-
ro, 1971) identified 61 localities for the occurrence of the muriqui (Brachyteles arachnoides) in the states of Bahia, Espirito
Santo, Minas Gerais, Rio de Janeiro, Sao Paulo and Parand. He estimated a total population of 2,791-3,226 muriquis, con-
trasting with a population of about 400,000 he reckoned would have existed in 1500. Accepting the position that there are
two species, Aguirre's (1971) data suggested a maximum of 996 individuals for the northern muriqui (Brachyteles hypoxan-
thus) and about 2,230 for the southern muriqui (B. arachnoides). Current population estimates for the northern muriqui
have indicated at least 864 individuals in the wild. Data available for the southern muriqui, suggest a minimum population
of about 1,300. These numbers combined approximate to the total population of 2,230 estimated by Aguirre (1971).
Further population surveys for muriquis in the states Sao Paulo, Rio de Janeiro and Bahia are urgently needed, along with
comparative studies on their basic ecology, diet and behavior in the different-sized forest fragments and the more extensive
forests. Although stochastic effects could rapidly eliminate the very small isolated populations of the northern muriqui, in
larger forests, persistent threats, such as hunting, could gradually but invidiously reduce those of the southern muriqui.

Key Words primates, muriqui, Brachyteles, population, distribution, conservation, Atlantic forest, Brazil


Introduction

Aguirre (1971) identified 61 localities for the occurrence of
the muriqui (Brachyteles arachnoides) in the states of Bahia,
Espirito Santo, Minas Gerais, Rio de Janeiro, Sao Paulo
and Parand. Twenty-eight of them were based on museum
specimens that had precise collection locations. Of these
61 localities, Aguirre (1971) considered that muriquis
could still be found in only 30 at the time of his survey:
seven in the state of Bahia, seven in Espirito Santo, four in
Minas Gerais, six in Rio de Janeiro and six in Sao Paulo.
Aguirre (1971) had no information on any possible remain-
ing populations in Parand. He estimated a total population
of 2,791-3,226 muriquis, contrasting with a population
of about 400,000 he reckoned would have existed in 1500.
Accepting the position that there are two species (Rylands
et al., 2000), Aguirre's (1971) data suggested a maximum
of 996 individuals for the northern muriqui (Brachyteles
.. ... and about 2,230 for the southern muriqui
(B. arachnoides).

Approximately 10 years later, Mittermeier et al. (1982)
revisited some of the areas cited by Aguirre (1971). They
were doubtful that B.' .. .-.'... had survived in two
of them, the Rio Doce State Park in Minas Gerais and
the Nova Lombardia Biological Reserve in Espirito Santo,
and were able to confirm just two populations, those of
the Caratinga Biological Station (EBC) (now the Private


Natural Heritage Reserve "Feliciano Miguel Abdala"
(RPPN-FMA)), in Minas Gerais, and the Fazenda Barrei-
ro Rico, in Sao Paulo (B. arachnoides). The total numbers
actually recorded did not exceed 100 individuals (Mitter-
meier et al., 1982). They failed to locate any new popula-
tions. That same year, Kinzey (1982) provided a general
review of the Atlantic forest primates, but mentioned no
new localities for Brachyteles. His study examined particu-
larly primate biogeography in relation to the Pleistocene
refuge theory then in vogue, looking at evidence for cent-
ers of primate endemism in eastern, south-eastern and
southern Brazil (Kinzey, 1982; for a review see Rylands
et al., 1996). Alves (1986) found two populations which
had not been reported previously; the first a forest in the
municipality of Manhuacu, Minas Gerais, now the Mata
do Sossego Private Natural Heritage Reserve (RPPN),
with 21 individuals counted, and the second in the Ca-
para6 National Park, where 19 muriquis were seen at the
C6rrego do Calgado, in the municipality of Ibitirama in
Espirito Santo.

On the basis of the accumulating literature on muriquis,
Mittermeier et al. (1987) estimated a minimum popula-
tion of 386 (northern and southern forms combined), in
11 localities, all previously cited by Aguirre (1971) except
for Cunha State Park in Sao Paulo, (contributing 16 indi-
viduals). The review by Nishimura et al. (1988) provided a
synthesis of what was then known of the populations and







distribution of the genus. Their population estimate, based
on the same sources, was similar-385.

Rylands et al. (1988) identified two places in the Rio
Jequitinhonha valley in Minas Gerais and Bahia, where
local people reported that muriquis were present until
the 1970s or 80s. They indicated further forest patches
where local people reported that muriquis could still be
found, but they remained unconfirmed. Oliver and Santos
(1991), likewise, indicated two localities in the far south
of Bahia-the Boca do C6rrego, in the municipality
of Belmonte, and the Serra da Onga, near Arataca and
Jussari-where muriquis might still survive. Oliver and
Santos (1991) concluded from their extensive surveys that
the muriqui was virtually extinct in Bahia. On the basis of
interviews, Mendes (1991), suggested that muriquis could
be found in some parts of the mountainous interior of
central Espirito Santo, in the region of Domingos Martins
(district of Pedra Azul) and Itarana, but reported that a
large part of the populations reported by Aguirre (1971)
had been lost (Forno Grande State Park, for example).
Mendes (1991) also indicated the extinction of muriquis
in the Santa Ldcia and Sao Lourengo biological stations, in
the municipality of Santa Teresa, even though both were
cited by Aguirre (1971).

Paccagnella (1991) carried out a census of the muriquis in
the Carlos Botelho State Park (PECB), in the municipali-
ties of Sao Miguel Arcanjo, Capao Bonito and Sete Barras.
Walking 214 km of trails in the park, Paccagnella (1991)
estimated a population of 500 to 800 muriquis, taking
into consideration 24,152 ha of the 37,432 ha of the park
(about 65% of the PECB) that was believed to provide
suitable habitat.

Pinto et al. (1993) reported the presence of muriquis in
the Augusto Ruschi Biological Reserve (formerly called
Nova Lombardia), municipality of Santa Teresa, Espirito
Santo, even though in very low numbers) (see Vieira and
Mendes, 2005). A year later, Martuscelli et al. (1994) indi-
cated 14 new locations for muriquis in Sao Paulo, Parand
and Rio de Janeiro, noting the first record for an oceanic
island, in the Ilha do Cardoso State Park off the coast of
Sao Paulo), where five muriquis were seen on two occa-
sions. Martuscelli et al. (1994) made further attempts to
find the muriquis there, but considering that hunting on
the island has always been intense, and despite the fact that
it is now a State Park, they believed the species was already
extinct there. Martuscelli et al. (1994) summed 303 "new"
muriquis in the state of Sao Paulo, but were unable to see
any in Rio de Janeiro, even though they discovered two
localities not reported by Aguirre (1971): Bocaina National
Park and Cairugu Environmental Protection Area (APA).
Martuscelli et al. (1994) also found evidence for the pres-
ence of muriquis in two localities in Parand: Jaguariaiva and
Guaraquegaba Environmental Protection Area (APA). Two
muriquis were seen in this latter locality, providing the first
register for the state of Parand. Martuscelli etal. (1994) also


Neotropical Primates 13(Suppl.), December 2005

collected a skull and partial skeleton of a recently hunted
animal in Guaraquegaba.

A number of new records appeared in the years following,
most especially of the southern muriqui (B. arachnoides).
Antonietto and Mendes (1994), for example, saw 15 in-
dividuals in the municipal Environmental Protection Area
(APA) Sao Francisco Xavier, in Sao Paulo. CSmara (1995)
obtained an entire skeleton from Itatiaia National Park,
Rio de Janeiro), and Oliveira and Manzatti (1996) counted
22 muriquis in the Fazenda Sao Sebastiao do Rio Grande,
em Pindamonhangaba, Sao Paulo.

Strier and Fonseca (1996-1997) re-assessed the numbers of
muriquis seen in the wild and counted 19 areas for the oc-
currence of the two species; eight new areas since the listing
Mittermeier et al. (1987). Strier and Fonseca (1996-1997)
summed 1,158 individuals in all; 234 northern muriquis
and 924 southern muriquis-numbers still far lower than
were estimated by Aguirre (1971).

Auricchio (1997) found three dead muriquis in the Serra da
Escorregosa, municipality of Sertao do Poruba, Sao Paulo.
Auricchio and Silva (2000) subsequently saw a group of at
least 10 in the Cubatao section (municipality of Cubatao)
of the Serra do Mar State Park. Koehler et al. (2002, 2005)
recorded eight muriquis in the municipality of Castro,
Parand, later confirmed as part of the only group in the
area, totaling 23 individuals (Pereira et al., 2005).

In Rio de Janeiro, Garcia and Andrade Filho (2002; Garcia,
2005) counted 17 muriquis, in two groups in the Serra dos
Orgaos National Park (municipalities of Teres6polis, Gua-
pimirim, Mag6 and Petr6polis). They were seen at the high-
est altitude ever recorded for the species (2,000 m above
sea level). Cunha (2003, 2004) again recorded B. arach-
noides in the park, counting 16 individuals in one group.
Romanini-Oliveira et al. (2005) also attempted, unsuccess-
fully, to habituate a group of 20-40 muriquis resident in
the Serra dos Orgaos National Park.

In 2006, Macedo (2006) confirmed the record of Camara
(1995) sighting a group of at least 35 adults and 10 juve-
niles and infants in the Itatiaia National Park, although still
unable to ascertain which of the two species they belonged.
A skin kept in the Visitor's Center of the park is identifiable
as B..'-i.... .-.'... (S. L. Mendes, pers. comm.), but this
being at the supposed limits of the ranges of both species,
further surveys are needed.

It is evident that B. .'A .... .-.'.. is the more threatened of
the two muriquis, even though a number of new popula-
tions have been found in recent years. Fontes et al. (1996)
saw two lone females in a forest fragment in the Ibitipoca
State Park, in Lima Duarte, Minas Gerais, one of them in
a group howler monkeys (Alouatta guariba). The popula-
tion estimate for B..'-\.... .-.'.. increased somewhat with
its discovery in Santa Maria do Jetibi, Espirito Santo,





Neotropical Primates 13(Suppl.), December 2005


Table 1. Locality records for Brachyteles registered by Aguirre (1971) and Martuscelli et al. (1994), compared with those listed in the
review of Strier and Fonseca (1996-1997) and findings in the last decade.
Aguirre (1971) Marstucelli et al. (1994) Strier and Fonseca (1996-1997) New localities: 1997 to 2006


Minas Gerais (4)
1. Fazenda Rochedo, Rio Casca
2. Serra do Brigadeiro, ErvAlia &
Carangola
3. Rio Doce State Park, Coronel
Fabriciano
4. Fazenda Montes Claros, Caratinga
Espirito Santo (7)
1. Brejetuba, Afonso ClAudio
2. C6rrego Sao Fernando, Domingos
Martins
3. Nova Lombardia, Santa Teresa
4. Pico do Tamanco and Pedra Azul,
Domingos Martins & Alfredo
Chaves
5. Forno Grande, Castelo
6. Jatibocas, Itarana
7. Barra Encoberta, Itarana
Rio de Janeiro (6)
1. Matas Morumbeca, Santa Maria
Madalena, Sao Fidelis & Campos
2. Rio Bonito, Silva Jardim,
Cachoeiras de Macacu, Casimiro
de Abreu & Friburgo
3. Fazenda do Subaio & Fazenda do
Carmo, Cachoeiras de Macacu
4. Serra dos Orgaos National Park,
Mag6 & Teres6polis
5. Itatiaia, Rezende
6. Horto Florestal Mambucaba,
Angra dos Reis
Sao Paulo (6)
1. Fazenda do Veado & Serra da
Bocaina, Sao Jos6 do Barreiro &
Bananal
2. Alto Paraibuna, Ubatuba, Sao Luis
de Paraitinga & Parati (Rio de
Janeiro)
3. Serra Paranapiacaba, Iporanga,
Eldorado, Capao Bonito, Sete
Barras, JuquiA, Itanhem & others
4. Nascentes dos rios Pardo,
Jacupiranga & Serra Negra,
Jacupiranga, Barra do Turvo &
Guaraqueqaba (Parand)
5. Dep. Agua e Esgoto (DAE), Santos,
Mogi das Cruzes & Sales6polis
6. Fazenda Barreiro Rico, Anhembi
Bahia (7)
1. Chapori, Una
2. C6rrego Mundo Novo, Pau Brasil
3. Riacho Duas Barras, Caatiba
4. Serra Couro d'Anta, Itapetinga
5. Serra Pateirao, Encruzilhada
6. Serra da Gabiarra, Santa Cruz de
Cabrilia
7. Farinha Lavada e Agua Limpa,
Guaratinga & Jucurucu


Rio de Janeiro (2)
1. APA Cairugu, Parati
2. Bocaina Natinal Park,
Parati, Sao Jos6 do
Barreiro & Angra dos
Reis
Sao Paulo (10)
1. APA Municipal de
Sao Francisco Xavier,
Pindamonhangaba
2. MonganguA Nucleus,
Serra do Mar State Park
3. Nucleus Curucutu, Serra
do Mar State Park
4. N6cleo Pedro de Toledo/
Itariri, Serra do Mar State
Park
5. JuruparA State Park,
Ibi6na
6. Ilha do Cardoso State
Park, Cananeia
7. Turistico do Alto Ribeira
State Park, Iporanga,
Apiai
8. Jacupiranga State Park,
Cananeia, Jacupiranga,
Barra do Turvo &
Eldorado
9. Macico da Jureia, Jureia-
Itatins Ecological Station
10. Macico Itatins, Jureia-
Itatins Ecological Station
Parand (2)
1. Jaguariaiva, Jaguariaiva
2. APA Guaraquecaba,
Guaraqueqaba


Minas Gerais (7)
1. Ibitipoca State Park1, Lima
Duarte
2. Sossego Private Reserve
(RPPN) Simonesia2
3. Rio Doce State Park, Marlieria
4. Serra do Brigadeiro State Park,
Araponga
5. Feliciano Miguel Abdala
Private Reserve (RPPN)
(former Caratinga Biological
Station EBC), Caratinga
6. Fazenda Esmeralda, Rio Casca
7. Fazenda C6rrego de Areia,
Peqanha
Espirito Santo (2)
1. Augusto Ruschi Biological
Reserve, Santa Teresa
2. Capara6 National Park2,
Divino de Sao Lourenco
Sao Paulo (10)
1. Fazenda Sao Sebastiao do Rio
Grande3,
Pindamonhangaba
2. Serra do Mar State Park
3. Sao Francisco Xavier,
Pindamonhangaba
4. Fazenda Barreiro Rico,
Anhembi
5. Jureia-Itatins Ecological
Station, Iguape
6. Jacupiranga State Park,
Cananeia
7. JuruparA State Park, Ibi6na
8. Carlos Botelho State Park, Sao
Miguel Arcanjo
9. Intervales State Park, Capao
Bonito
10. Turistico do Alto Ribeira State
Park, Iporanga, Apiai


Minas Gerais
1. Fazenda Duas Barras 4,
Santa Maria do Salto
2. Mata Escura Biological
Station Jequitinhonha
Espirito Santo
1. Santa Maria do Jetiba5,
Santa Maria do Jetiba
Sdo Paulo
1. Serra da Escorregosa6,
Sertao do Poruba
2. N6cleo Cubatao7, Serra do
Mar State Park
Parand
1. Castro8


30 localities 7 new localities 4 new localities 6 new localities

Obs.: Fontes etal. (1996); 2Alves (1986); 3 Oliveira & Manzatti (1996); 'Melo etal. (2004); 'Mendes (este volume); 6Auricchio (1997); 7Auricchio &
Silva (2000); 'Koehler etal. (2002).







where Mendes et al. (2005b) found groups in a number of
partially isolated forest fragments, 15 in all, with numbers
ranging from one to 20 individuals, providing an estimate
of at least 115 overall. Recently, Melo et al. (2004) located
two new populations in the Rio Jequitinhonha valley, one
with a minimum of 28 individuals, Mata Escura Biologi-
cal Reserve, municipality of Jequitinhonha, Minas Gerais,
another, with seven individuals in large remnant forest cov-
ering the state limits of Minas Gerais and Bahia, in the
Fazenda Duas Barras, between Santa Maria do Salto, Minas
Gerais and Guaratinga, Bahia. This last is currently the only
known population in Bahia (Melo et al., 2004).

An intensive survey carried out by Strier et al. (2002) in
the Feliciano Miguel Abdala Private Reserve (RPPN-FMA)
resulted in a population count of 157. More recently,
Strier and Boubli (2006) confirmed four groups, totaling
230 muriquis. The occurrence of muriquis in the Fazenda
C6rrego de Areia in the municipality of Peganha, Minas
Gerais, was reported by Aguirre (1971), but the fate of the
population remained unknown (Mittermeier et al., 1987)
until Hirsch et al. (2002) visited the area and counted
13 muriquis there, including some infants.

Mendes et al. (2003) identified a group of 12 muriquis in
the vicinity of the Ibitipoca State Park, an area known as the
Mata dos Luna, in Santa Rita do Ibitipoca, Minas Gerais.
This population has been studied by Ferraz et al. (2005),
who accompanied its decline to just five males. More criti-
cal has been the situation of the small group of the Fazenda
Esmeralda, Rio Casca Minas Gerais, where Melo et al.
(2005) found only three individuals remaining. Aguirre
(1971) had estimated seven or eight muriquis there, and
there were 18 in the group when Lemos de Sa (1991) was
studying them in 1986 and 1987. In 2006, only one male
remained, who was living with a band of capuchin mon-
keys (Cebus nigritus) (E R. de Melo, unpublished data).

Further studies in Minas Gerais have allowed for a re-
count of the key populations of the northern muriqui in
three key areas. Dias et al. (2005) estimated a minimum of
370 in: the Serra do Brigadeiro State Park, the RPPN Mata
do Sossego Private Reserve (RPPN) in Simon6sia and, de-
spite the fears of Mittermeier et al. (1982), the Rio Doce
State Park. Marlikria. Gomes and Melo (2005) have also
confirmed the occurrence of at least three groups, a total
of 135 individuals, in the Capara6 National Park, all in the
part in Espirito Santo.

Conclusions

Current population estimates for the northern muriqui are
examined in more detail by Mendes et al. (2005a), who
have indicated at least 864 individuals in the wild. Data
available for the southern muriqui, suggest a minimum
population of about 1,300. These numbers combined ap-
proximate to the total population of 2,230 estimated by
Aguirre (1971). Table 1 compares the populations listed by


Neotropical Primates 13(Suppl.), December 2005

Aguirre (1971) and Strier and Fonseca (1996-1997) and
the most recent information we report here.

Further population surveys for muriquis in the states of
Sao Paulo, Rio de Janeiro, and Bahia are urgently required
for a better understanding of the conservation status of the
two species. Comparative studies are needed on their basic
ecology, diet and behavior in the different-sized forest frag-
ments and more extensive forests, to better understand how
they occupy degraded forests and the relation of these as-
pects, especially diet, to their demography and, hopefully,
population growth and stability in protected areas (Talebi
et al., 2005a, 2005b). Lacking long-term studies of this
sort, along with regular population monitoring, it will be
difficult to revert the constant threat of imminent extinc-
tion that both species faces. They are present in numerous
protected areas-national, state and private-that should
at least provide some protection from forest loss and hunt-
ing. The Carlos Botelho, Serra do Mar and Intervales state
parks, in Sao Paulo, and the Serra do Brigadeiro and Rio
Doce state parks in Minas Gerais now hold the largest pop-
ulations of the two species. Stochastic effects could rapidly
eliminate the very small isolated populations of the north-
ern muriqui, and albeit in larger forests, persistent threats,
such as hunting, could gradually but invidiously reduce
those of the southern muriqui.

Brito and Grelle (2006) have analyzed the northern
muriqui populations using the program VORTEX. They
concluded that they need areas larger than 11,570 ha to
maintain genetic viability. Their results indicated that the
majority of the populations are currently too small (even
though they are able to persist for some time) to be geneti-
cally viable in the long term, due to the inevitable gradual
loss of heterozygosity.

References

Aguirre, A. C. 1971. 0 mono Brachyteles arachnoides
(E. C .. Situaado Atual da Especie no Brasil. Academia
Brasileira de Ciencias, Rio de Janeiro. 53pp.
Alves, M. C. 1986. Novas localizagoes do mono carvoeiro,
Brachyteles arachnoides (Cebidae, Primates) e situadao
atual do Parque Nacional do Capara6. In: A Primatologia
no Brasil- 2, M. T. de Mello (ed.), p.367. Sociedade Bra-
sileira de Primatologia (SBPr), Brasilia.
Antonietto, L. A. and Mendes, F D. C. 1994. Sao Fran-
cisco Xavier: A new site for primatological research and
conservation in the Brazilian Atlantic Forest. Neotrop.
Primates 2(3): 3-4.
Auricchio, P. 1997. A new locality for Brachyteles arach-
noides and the urgency of finding new directions for
muriqui conservation. Neotrop. Primates 5(3): 78-80.
Auricchio, P. and Silva, M. A. F 2000. Nova ocorrencia de
Brachyteles arachnoides no Parque Estadual da Serra do
Mar, Sao Paulo, Brasil. Neotrop. Primates 8(1): 30-31.
Brito, D. and Grelle, C. E. V. 2006. Estimating minimum
area of suitable habitat and viable population size for the





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Neotropical Primates 13(Suppl.), December 2005


POPULATION DENSITY AND VERTICAL STRATIFICATION OF FOUR PRIMATE SPECIES AT
THE ESTACAO BIOLOGICAL DE CARATINGA/RPPN-FMA, MINAS GERAIS, BRAZIL

Bairbara Almeida-Silva1, Andre A. Cunha2, Jean P. Boubli3, Sergio L. Mendes' and Karen B. Strier4

1Departamento de Ciencias Biol6gicas, Universidade Federal do Espirito Santo (UFES), Vit6ria, Espirito Santo, Brazil,
email:
2Laboratorio de Vertebrados, Departmento de Ecologia, Univerisdade Federal do Rio de Janeiro (UFRJ), Rio de Janeiro,
Brazil
3Zoological Society of San Diego, USA. Current address: Department of irli...p. ...-;,, The University ofAuckland, Private
Bag 92019, New Zealand
'Department ofAnrl-. .p. .1..;,, University of Wisconsin-Madison, Madison, WI 53706, USA


Abstract

In 2003, we carried out a line-transect sampling for all the primates (Alouatta guariba clamitans, Brachyteles .' ...
Cebus nigritus, and C.-"' .' at the Estagao Biol6gica de Caratinga (EBC) to estimate the sizes of their populations.
Our goal was to examine whether the trend in population growth observed in the northern muriqui population was accom-
panied by similar trends in the other three species, or if there was a decline which could indicate the possible effect of com-
petition with northern muriquis. In addition, we studied stratification to verify if the different species use the forest strata
in different ways to avoid direct competition. We registered a total of 78 sightings of primates: 33 for A. guariba clamitans,
23 for C. nigritus, 18 for B. A' ,... .-'o.. and four for C. flaviceps. Our results indicated that A. guariba clamitans continued
to be the most abundant primate at the EBC. Cebus nigritus and B. .':,.... .'.. occur at almost the same abundances, being
half of that of brown howlers. C .-'. flaviceps is the least common primate in this forest fragment. Compared to previous
studies, our census shows a decline in the abundance of howlers. This study confirms the prediction that larger primates use
higher strata of the forest while smaller species move in the lower strata.

Key Words- Abundance, distance-sampling, mammals, space use of space, Atlantic forest, Neotropical primates


Introduction

The Brazilian Atlantic Forest has one of the highest pri-
mate diversities in the Neotropical Region, including two
endemic genera, muriquis (Brachyteles) and lion tamarins
(Leontopithecus) (Pinto et al., 1993; Rylands et al., 1996).
This biome has been severely ruined over the last five hun-
dred years to the extent that, today, only 7% of its original
area remains (Myers et al., 2000). As a result, the endemic
primate populations have been drastically reduced. Since
the early 1980s, Strier and collaborators, have been moni-
toring an isolated population of northern muriquis B. hy-
poxanthus in a 957-ha forest fragment in Minas Gerais pre-
viously known as the Caratinga Biological Station (EBC),
but now the Private Natural Heritage Reserve Feliciano
Miguel Abdala (RPPN-FMA) (Strier et al., 2006; Strier
and Boubli, 2006).

In the early 1980s, only 50 northern muriquis, in two
social groups, were known to inhabit the EBC (Valle et al.,
1984). Since then, there has been a remarkable increase in
the size of this population, now numbering 226 muriq-
uis (Strier et al., 2006). Three other primates occur there:
the buffy tufted-marmoset, C flaviceps; the brown
howler monkey, Alouatta guariba clamitans; and the tufted


capuchin Cebus nigritus. Little is known about the demo-
graphic trends of these other primate populations at the
EBC, but several studies have attempted, at different times,
to determine their sizes (Valle et al., 1984; Fonseca, 1983;
Ferrari, 1988; Mendes, 1989; Hirsch, 1995; Strier et al.,
1999, 2002).

In 2003, we carried out a line-transect sampling of all pri-
mates at the EBC to estimate the sizes of their populations.
Our goal was to examine whether the trend in population
growth observed in the northern muriqui population was
accompanied by similar trends in the other three species.
In addition, we studied stratification to verify if the dif-
ferent species use the forest strata in different ways. Forest
strata selection has been identified as an important form
of niche partitioning by sympatric species to reduce direct
competition (MacArthur, 1958; Cunha and Vieira, 2004
and references therein).

Methods

Study area
The EBC is a 957-ha Brazilian Atlantic forest fragment,
in the municipality of Caratinga, Minas Gerais, Brazil
(19044'S, 4149'W). The area is surrounded by pasture and







plantations of coffee, sugar cane and other crops. The al-
titude ranges from 400 m to 680 m, and the topographic
relief is a series of hills and valleys. The forest is mostly
secondary and is composed of a mosaic of habitats in dif-
ferent stages of regeneration (Hatton et al., 1984; Boubli
et al., 2003).

Data collection: the line transect census
The census was carried out over 20 days in July and August
of 2003, during the middle of the dry season in this region.
Thirteen trails from the Ja6 Valley were chosen for the
census work. Eight were along hillsides, following the top-
ographic contours, with lengths ranging from 280 m to
2,700 m (mean = 750.76 m; SD = 812.73 m). Three trails
were along the hilltops and ranged from 260 to 1,000 m in
length (mean = 753.33 m; SD = 427.24 m). The remain-
ing two trails were along the valley floor and ranged from
800 m to 960 m in length. The choice of trails was based
on our decision to: 1) cover the largest area possible in one
day; and 2) insure that trails were far enough apart to pre-
vent the observer from counting the same individuals twice
during the same sampling period. Trails were walked daily
at an average speed of 1 km/h between 0600 and 1700 h,
with a rest from 1200 to 1400 h, when primates tend to
be least active and thus less detectable by the observer. The
following data were collected when we sighted a primate
group: 1) time at beginning of the observation; 2) species;
3) location; 4) number of individuals; 5) perpendicular
distance from the trail of the individual seen; 6) height
in the forest of the first individual seen; and 7) the time
when observation finished. Observations did not exceed
10 minutes. A total of 100 km was walked over the 20 day
sampling period.

Data Analysis
We used the software DISTANCE 3.5 (Thomas etal., 1998)
to run the analysis. All models with respective adjustments
were tested. When necessary, data were grouped in classes
and truncated to a better model fit. After goodness-of-fit
test acceptance, model selection was based on the mini-
mum values of the Akaike Criterium Information (AIC)
and of the Percent Coefficient of Variation (CV%) of the
density estimates. Due to the small number of sightings


Neotropical Primates 13(Suppl.), December 2005

(n = 4), for the density estimate of C. flaviceps we used a
general Estimated Standard Width (ESW) calculated from
all observations of all species, after testing that there were
no differences in the perpendicular distances between spe-
cies with ANOVAs (all with p>0.05).

Differences in the use of the forest strata by the primates
were evaluated using a Chi-square test with Yates correc-
tion, using absolute number of observations in each class of
5 m, between one and 35 m. C .-'. flaviceps was again
excluded from this analysis due to the small number of
observations.

Results

A total of 78 sightings of primates were registered in the
100 km of transects walked: 33 for A. guariba clamitans,
23 for C. nigritus, 18 for B. '.i;... .-.'i.. and four for
C flaviceps. The best model and adjustment to estimate pri-
mate abundances were the uniform-cosine, grouped into
four classes with AIC = 87.48 and CV% = 24.47 and seven
classes with AIC = 76.06 and CV% = 27.01, respectively
for A. guariba clamitans and C. nigritus. For B. .' ..
the best model was uniform-polynomial, with data grouped
in four classes with an AIC = 30.44 and CV% = 33.2. De-
spite the fact that the statistical distribution of these model
criteria values was not ideal, particularly in the Coefficient
of Variation, they were considered valid for basic estimates
and comparisons.

Our results indicated that the brown howler monkey
(A. guariba clamitans) continues to be the most abundant
primate in EBC. The capuchin monkey (C. nigritus) and
the northern muriqui (B..'.:.... .-K'... ) occur at almost the
same abundances, being half of that of brown howlers. The
buffy-headed marmoset is the least common primate in
this forest fragment, with an estimated population size of
one quarter of that of howlers (Table 1).

The EBC primates occupy a wide range of heights in the
forest; from one to 35 m. There is a clear relation between
body size and the height of the forest strata occupied
(Fig. 1). C nigritus was seen mostly in the understorey and


Table 1. Estimates of population densities and population size with confidence intervals (95%) for the four primates at the Estayao
Biol6gica de Caratinga (EBC), Minas Gerais, Brazil. n = number of observations; ESW = Effective Strip Width; Density = individuals per
km2; N = population size for 900 ha of EBC forest fragments.
Species n ESW (m) Density (ind./km2) N
8.71 50 480
Alcuatta claitans 33 (6.55-10.1) (38-68) (365-643)
13.18 29 279
Brachvteles hypoxanthus 18
(9.99-17.38) (22-39) (212-369)
8.93* 13 123
Calhlthnrxfavceps 4 (7.32-10.91) (11-16) (101-150)
8.12 29 277
Cebusnigritus 23 (6.53-11.55) (23-36) (223-344)

*Estimated from all primate sightings combined (see "Data analysis").





Neotropical Primates 13(Suppl.), December 2005


Vertical Stratification

04 Chi-square= 23,97; P= 0.02; d.f.= 12

0.2


0 2-I L Ii
1-1m 6-10m 11-1i5m 1-a2H 21-25m 26,30m 31-3Sm

M C. nigritus M A. guariba B. hypoxanthus

Figure 1. Relative frequencies of sightings of Cebus nigritus,
Alouatta and Brachyteles at different heights
in the forest at EBC. Chi-square values were calculated with ab-
solute numbers and Yates correction. Callithrixflaviceps was not
included due to the low number of sightings.


lower canopy (6-15 m) (65%), A. guariba clamitans occu-
pied mainly the canopy (16-25 m) with 55% of sightings
in this stratum, and B..',;... .-.'... was found mostly in
the canopy and emergent trees (16-35 m; 61%). All of the
species were observed in more than one strata, but only the
northern muriqui was observed above 26 m.

Discussion

Comparing our results to those of previous studies
(Table 2), our findings suggest that C nigritus is as abun-
dant as it was in the previous census, eight years ago. For
A. guariba and C flaviceps there appears to be a drop in
population, although our results for C flaviceps may well
be underestimates given the small number of sightings.
In contrast to A. guariba, however, B. .',;... .-.'.. shows
a clear increase in numbers (Table 2). Despite the high
CV% of density estimates (33.2%), the point estimate
(N = 279) for the northern muriqui was very close to the
actual number of individuals known to be alive at the time
of the survey (N = 226; Strier et al., 2006), confirming the
efficiency of distance sampling in population abundance
studies for Neotropical primates such as this.

It is possible that the opposing trends-a decline in howler
monkeys and an increase in the abundance of muriquis
(since at least the last forest-wide census carried out by
Hirsch (1995) -result from competition between the two
species. They overlap considerably in their diets and pre-
ferred habitat (Mendes, 1989; Hirsch, 1995), and Dias and
Strier (2000) have reported that muriquis were dominant
in interspecific agonistic interactions, which occur prima-
rily in food patches. Thus, one could make a case for either
or both scramble and interference competition. However,
we are presently unable to test this hypothesis as we have
data for only one site and at one point in time, thus static
or dynamic regression approaches commonly used to esti-
mate competition coefficients from census data are not ap-
plicable in our study (Pfister, 1995; Fox and Luo, 1996).


Table 2. Density estimates for the EBC primates over the last two
decades (1981-2004). Estimates with 95% confidence intervals
between parentheses for the present study.
Species Density (ind/ha) Reference
Alouatta
A1.17 Mendes (1989)
clamitans
Alouatta^ 0.922 and 1.493 Hirsch (1995)
clamitans
Alouattan 0.502 (0.381-0.672) This study
clamitans

Brachyteles hypoxanthus 0.047 Valle et al. (1984)
Brachyteles hypoxanthus 0.034 Fonseca (1983)
Brachyteles hypoxanthus 0.072 and 0.762 Hirsch (1995)
Brachyteles hypoxanthus 0.292 (0.221-0.385) This study

Cebus nigritus 0.197 to 0.35 Hirsch (1995)
Cebus nigritus 0.289 (0.233-0.360) This study

Callithrixflaviceps 0.4 Ferrari (1988)
Callithrixflaviceps 0.019 to 0.699 Hirsch (1995)
Callithrixflaviceps 0.13 (011-0.16) This study



The detection of a drop in the population of C flaviceps
could simply be an artifact of poor sampling, and also due
to the possibility that this primate shows a very patchy
distribution throughout the forest, being more abundant
in very disturbed areas where bamboo and 'angico' trees
(Anadenanthera sp.) are abundant (Ferrari, 1988). Such
areas tend to be located on the forest edges, which were not
sampled in this study. The evident stability in the popu-
lation of C nigritus is also consistent with the idea that
muriqui and howler monkey densities are more directly
related to one another than to those of the other species,
as discussed above. The capuchin monkeys at EBC have a
very distinct feeding ecology, and do not appear to be in as
much direct competition with the two atelids as the two
atelids are with each other (Dias and Strier, 2000).

The positive relationship between body size and the vertical
strata used by the primates at the EBC is consistent with
the general patterns observed in other Neotropical primate
communities in Amazonia (Fleagle et al., 1981; Mitter-
meier and Van Roosmalen, 1981; Charles-Dominique,
1983; Terborgh, 1983; Peres, 1993), and in the Atlantic
forest (Rylands et al., 1996; Cunha et al., in press). This
relationship results in some partitioning of strata according
to body size, and may contribute to the stronger effects of
the two largest species (muriqui and howler monkey) on
one another.

In conclusion, we observed the same general pattern of
abundance in the primate community at the EBC re-
corded by previous researchers, with A. guariba clamitans
the most abundant species, followed by B. .'







and C. nigritus almost equally abundant, and C flaviceps
continuing to be the rarest primate in this forest fragment.
Additionally, we recorded a decline in A. guariba clamitans
abundance, in contrast to the increase in B. ', .. .-'
abundance. This study confirms that larger primates use
higher strata while smaller species move on lower strata.

Acknowledgments

We are indebted to the Abdala family for granting permis-
sion to work on their property. The late Eduardo Veado of
the Associacao Pr6-Estagao Biol6gica de Caratinga was im-
mensely helpful and kind in his support for this research.
We also thank all of the staff involved. This work was
funded by the Zoological Society of San Diego, USA, the
Brazilian Research Council (Conselho Nacional de Desen-
volvimento Cientifico e Tecnoldgico- CNPq), and Conserva-
tion International-Brazil.

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occupy the same place at the same time, or the impor-
tance of space in the ecological niche. Bull. Ecol. Soc. Am.
85: 25-26.
Cunha, A. A.; Vieira, M. V. and Grelle, C. E. In press. Pre-
liminary observations on habitat, support use and diet in
two non-native primates in an urban Atlantic forest frag-
ment: the capuchin monkey (Cebus sp.) and the common
marmoset (C .-' jacchus) in the Tijuca Forest, Rio de
Janeiro. Urban Ecosystems.
Dias, L. G. and Strier, K. B. 2000. Agonistic encounters
between muriquis, Brachyteles arachnoides 'i... -'..
(Primates, Cebidae), and other animals at the Estagao
Biol6gica de Caratinga, Minas Gerais, Brazil. Neotrop.
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Ferrari, S. F. 1988. The Behavior and Ecology of the Buffy-
headed Marmoset, C .- / '. . Thomas, 1903).
PhD thesis, University College, London.
Fleagle, J. G., Mittermeier, R. A. and Skopec, A. L. 1981.
Different habitat use by Cebus apella and Saimiri sciureus
in central Surinam. Primates 22: 361-367.
Fonseca, G. A. B. da. 1983. The Role of Deforestation
and Private Reserves in the Conservation of the Woolly
Spider Monkey (Brachytele arachnoides). Master's thesis,
University of Florida, Gainesville.
Fox, B. J. and Luo, J. 1996. Estimating competition coef-
ficients from census data: A reexamination of the regres-
sion technique. Oikos 77: 291-300.


Neotropical Primates 13(Suppl.), December 2005

Hatton, J., Smart, N. and Thomson, K. 1984. In urgent
need of protection-habitat for the woolly spider
monkey. Oryx 18: 24-29.
Hirsch, A. 1995. Censo de Alouattafusca Geoffroy, 1812
(Platyrrhini, Primates) e Qualidade do Habitat em Dois
Remanescentes de Mata Atlintica em Minas Gerais.
Master's thesis, Universidade Federal de Minas Gerais,
Belo Horizonte.
MacArthur, R. H. 1958. Population ecology of some
warblers of northeastern coniferous forests. Ecology 39:
599-619.
Mendes, S. L. 1989. Estudo ecol6gico de Alouattafusca
(Primates: Cebidae) na Estagao Ecol6gica de Caratinga,
MG. Rev. Nordest. Biol. 6(2): 71-104.
Mittermeier, R. A. and Van Roosmalen, M. G. M. 1981.
Preliminary observations on habitat utilization and diet
in eight Surinam monkeys. Folia Primatol. 36: 1-39.
Myers, N., Mittermeier, R. A., Mittermeier, C., Fonseca,
G. A. B. and Kent, J. 2000. Biodiversity hotspots for con-
servation priorities. Nature, Lond. 403: 853-858.
Peres, C. A. 1993. Structure and spatial organization of
an Amazonian terra firme forest primate community.
J. Trop. Ecol. 9: 259-276.
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from census data: A test with field manipulations of tide-
pool fishes. Am. Nat. 146: 271-291.
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primates in Brazilian tropical Forest. Folia Primatol. 61:
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meier, R. A. 1996. Primates of the Atlantic forest: origin,
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Brasilia.








Neotropical Primates 13(Suppl.), December 2005 31

CONSERVING THE NORTHERN MURIQUI IN SANTA MARIA DE JETIBA, ESPIRITO SANTO

Sergio L. Mendes1'2, Rogerio R. Santos2 and Luciano P. Carmo3

1Departamento de Ciencias Biol6gicas, CCHN, Universidade Federal do Espirito Santo, Vitoria, Espirito Santo, Brazil.
E-mail:
2IPEMA- Instituto de Pesquisas da Mata Atlantica, Santa Teresa, Espirito Santo, Brazil
3Programa de P6s-Graduacao em Biologia Animal, Universidade Federal do Espirito Santo, Vit6ria, Espirito Santo, Brazil


Abstract

The northern muriqui is known to occur in only 12 localities, with small populations restricted to isolated forest frag-
ments. In the state of Espirito Santo the species is currently confirmed in only three localities: in and around the Augusto
Ruschi Biological Reserve; the Capara6 National Park (which extends into the state of Minas Gerais); and forests in the
municipality of Santa Maria de Jetibi. We are studying the muriquis in these last two areas. Both are in the central-southern
montane region of the state. In the Capara6 Natoinal Park the aim is to census the population and to estimate its social and
demographic composition. The muriquis have been found in part of the 18,200 ha on the Espirito Santo side of the park,
and we believe that this population is the largest in the state. In Santa Maria de Jetibi, we hope to improve the prospects
for the survival of the muriquis through the following activities: 1) monitoring and managing the populations; 2) studying
genetic variability and endogamy; 3) developing a conservation education program, 4) testing the potential for ecotourism;
and 5) promoting actions to improve the conservation and restoration of Atlantic Forest fragments. To date, we have found
84 individuals living in 13 fragments, with subpopulations varying from 1 to about 16 individuals. We have information on
their presence in another 11 fragments. We have successfully translocated one young female and are monitoring its behav-
ior. The current population and genetic data suggest that we need to improve the forest connectivity in order to reduce the
fragmentation and isolation of the muriqui groups. The combined efforts of scientists, government, and the local people will
be fundamental to achieve this.


Key Words- primates, muriqui, Brachyteles, Atelidae, conservation, Atlantic Forest, Espirito Santo


Introduction

The northern muriqui, Brachyteles .'. .... .'.. is listed as
Critically Endangered on the IUCN Red List of Threat-
ened Species, and by the Brazilian list of animals threatened
with extinction (Brazil, MMA, 2003) and is considered to
be among the world's 25 most endangered primates (Strier
et al., 2006). Until recently considered a monotypic genus,
Brachyteles is treated now as having two species based on
differences in the facial pigmentation (spotty and lack-
ing pigmentation in ';... -'.. but darkly pigmented
in arachnoides) and the presence ,'\:.. I .-'.. or absence
(arachnoides) of a vestigial thumb (see Vieira, 1944; Lemos
de Sa et al., 1990, 1993; Leigh and Jungers, 1994). There
may also be genetic differences (Pope, 1998).

Prior to the widespread destruction of the eastern Brazilian
Atlantic forest that has taken place largely over the last cen-
tury, the geographical distribution of muriquis was almost
continuous, from the state of Bahia to Parand, including
eastern Minas Gerais, Espirito Santo, Rio de Janeiro and
Sao Paulo. It ranged from the coastal hills, to the west-
ern limits of the Atlantic forest where it is replaced by the
Cerrado or bush savanna of central Brazil. The northern
muriqui's range extended from southern Bahia, near to


Salvador, to southern Minas Gerais, at least to the Serra da
Mantiqueira that accompanies the state border with Rio de
Janeiro and Sao Paulo. It seems that it never occurred in the
lowland forests of extreme southern Bahia and northern
Espirito Santo (Aguirre, 1971). In Espirito Santo, the his-
torical and current records restrict it to the southern mon-
tane forests (Fig. 1).

Hunting and deforestation mean that today the species is
known to occur in only 12 localities, with a total popula-
tion minimum of about 855 individuals. Many of these
muriquis are restricted to small isolated forest fragments
(Mendes et al., 2005). The largest known population has
about 200 individuals, and even in the larger fragments,
the populations are small. In this paper we present a strat-
egy to conserve the muriqui in the forest fragments of
Santa Maria de Jetibi, Espirito Santo, where muriquis can
be found in very small fragments. Their survival depends
on the cooperation of scientists, government and the local
people.

Muriquis in the State of Espirito Santo

We are studying the muriquis in two places in the state
of Espirito Santo: the Capara6 National Park and in







the municipality of Santa Maria de Jetibi, both in the
central-southern mountainous region. Besides these areas,
the muriquis occur also in the Augusto Ruschi Biologi-
cal Reserve and surrounding forests (Fig. 1; Vieira and
Mendes, 2005), and have been reported for a number of
other localities that have yet to be confirmed (Mendes and
Chiarello, 1993). This mountainous region is characterized
by an enormous number of small forest fragments, more
or less connected to each other, and surrounded by differ-
ent forms of land use, creating as such a complex land-
scape. The project in the Capara6 National Park is just
beginning. The aim is to census the population and to es-
timate its social and demographic composition. The Park
encompasses 31,853 ha, straddling the state border with
Minas Gerais. The muriquis have been found in part of
the 18,200 ha of the park on the Espirito Santo side. The
muriqui population there is certainly the largest in the state
and is, consequently, the least threatened.

The project in Santa Maria de Jetibi began in 2001 with
a preliminary survey that revealed a peculiar situation in
which several small muriqui populations live in almost iso-
lated forest patches, relatively close to each other. Consider-
ing that all the forest fragments are in a mosaic of private
properties, it was evident that the conservation of their
muriquis would require a more complex strategy than one
of just creating and managing a protected area.

Conserving the Muriquis in Santa Maria de Jetiba

We are carrying out a plan to improve the prospects for the
survival of the muriqui that involves five distinct but inte-
grated activities: 1) Monitoring and managing the muriqui


Figure 1. Historical and current records of muriquis in Espirito
Santo State.


Neotropical Primates 13(Suppl.), December 2005

populations; 2) studying genetic variability and endogamy;
3) developing a conservation education program; 4) test-
ing the potential for ecotourism; and 5) promoting actions
to improve the conservation and restoration of Atlantic
Forest.

In our efforts to census and monitor the population, we
found 84 individuals, living in 13 fragments, with subpop-
ulations varying from 1 to about 16 individuals (Table 1;
Fig. 2). These numbers will tend to increase, not only as we
get more information about the presence (or otherwise) of
muriquis in 11 other fragments, but also because more in-
tensive censuses are necessary in a number of areas. In gen-
eral, there is only one social group in each forest fragment,
and, sometimes, only a solitary individual. Strier (1996)
and Printes and Strier (1999) found that young female
muriquis disperse from their natal group to another group
where they reproduce. We have observed that although in
Santa Maria de Jetibi females leave their natal groups, they
become solitary when they reach adulthood, probably be-
cause of the lack of opportunities to disperse to other social
groups. For this reason, we plan to translocate solitary
females to forest fragments where other muriqui groups

Table 1. The muriqui population in Santa Maria de Jetibi, Espiri-
to Santo. The estimated population is based largely on informa-
tion from local people. The numbers correspond to the localities
shown in Figure 2.
# Locality Confirmed Estimated
# Locality population population
1 Rio Plantoja 05 13
2 C6rrego Simao 05 06
3 Rio Lamego 01 01
4 Alto Santa Maria 10 11
5 Alto Rio Posmousser 05 05
6 C6rrego do Ouro 1 11 12
7 C6rrego do Ouro 2 05 07
8 Rio Claro / Rio Triunfo 03 03
9 Rio das Pedras 2 09 09
10 Rio das Pedras 1 11 11
11 Rio das Pedras / Jequitiba 02 02
12 Jequitiba 01 01
13 Sao Sebastiao de Belem 16 16
Rio Sabino 0 01
Rio das Pedras / Rio Triunfo 0 01
Rio das Pedras 3 0 01
Alto Rio Lamego 0 ?
Rio Claro 0 ?
Alto Jequitiba 0 ?
Garrafao 0 ?
Alto Sao Sebastao 0 ?
Rio das Pedras 4 0 ?
Rio das Pedras 5 0 ?
Rio das Pedras 6 0 ?
Total 84 100





Neotropical Primates 13(Suppl.), December 2005

live. If this works well, then we can predict that this will be
beneficial to the metapopulation as a whole, increasing the
reproductive component of the population and promoting
gene flow. Our first attempt to capture a solitary female,
using darts delivered by an air rifle, has indicated that the
task is not easy, however. Having dispersed, the then solitary
female was more secretive and shy than when she was a part
of our study group, and she avoided the capture team. We
reasoned that it might be easier to capture and translocate
a female just before her dispersal. In our second attempt,
we chose a young female from our study group, estimated
to be 6 years old, and in this case we were successful. The
female was fitted with a radio collar, and taken to another
forest fragment about 10 km away, where there was another
muriqui group with only two adult females and four adult
males. We are presently monitoring the female to evaluate
the effectiveness of this management procedure.

Analyzing the distribution of the muriqui groups in the
landscape (Fig. 2), we concluded that we needed a better
knowledge of the sizes and shapes and the connectivity of
the forest patches, as well as a better understanding of the
use of the land surrounding them. We, therefore, select-
ed a core area to take aerial photographs and classify the
land use. The analyses demonstrated the complexity of the
landscape and showed that the forest fragments remained


mainly on the middle-sized hills and higher, while crops
and roads dominated the foothills and valleys. We estimat-
ed that 36% of the forest fragments in this core study area
were surrounded mainly by coffee plantations, followed by
pasture, and other crops. There is some connectivity be-
tween the fragments where muriquis live, but in some cases
the groups are isolated, not only by non-forested areas, but
also because the distance is too far to disperse.

Simulating the viability of the populations in nine forest
fragments using Vortex (Lacy et al., 1995), we found that
that the probability of extinction over the next 100 years
was high for the smaller fragments (less 150 ha), but low in
the larger ones. The simulation used somewhat optimistic
demographic data based on Strier (1994/1995), however,
and did not take into account the effects of endogamy and
the loss of young females that disperse from their groups.
The results did show that the species persistence in such a
landscape is mainly determined by the fragment size and
connectivity, emphasizing the importance of maintaining a
metapopulation system.

To analyze the genetic traits of the muriqui populations
we are extracting DNA from their feces. The work is co-
ordinated by V. Fagundes, from the Federal University of
Espirito Santo, in collaboration with A. Di Fiori, from


Figure 2. Current records of muriquis in Santa Maria de Jetiba, Espirito Santo. The numbers correspond to the localities listed in Table 1.







New York University. To develop protocols and standard-
ize techniques and make comparisons, we are using feces
collected in Santa Maria de Jetibi, as well as feces from
of the muriqui population at the Feliciano Miguel Abdala
Private Reserve (RPPN) in Caratinga, Minas Gerais, in
collaboration with K. B. Strier, J. P. Boubli, and C. Pos-
samai. To date, we have extracted and analyzed DNA from
the feces of 20 individuals from Santa Maria and of 126
from Caratinga, and the first data, using mitochondrial
DNA, indicates the presence of specific markers between
the Santa Maria de Jetibi and Caratinga populations (Fa-
gundes, 2005).

Our project is in a region where the human community
is composed of Pomeranian descendants, which migrated
from Europe to Brazil about 100 years ago. They usually
have holdings farmed by the entire family. Because a single
forest fragment is often shared among different farms, we
have to deal with numerous people in order to work with
muriquis. Fortunately, Pomeranians in general do not have
hunting traditions, which may explain the survival of muri-
quis in such small fragments. We believe that conservation
education will help us to study the muriquis, and also to
promote actions to conserve and restore the Atlantic Forest
in this region.

In addition to working with schools, training teachers and
young people, and cooperating with the local government,
we are also trying to develop good relationships with the
farmers. In order to reach a broader audience, we are using
the local radio station to transmit information about muri-
quis, producing and distributing t-shirts, posters and fold-
ers, and presenting the project to different kinds of local
and national media. The experimental plan for ecotour-
ism is focusing on the development of a low impact tour-
ism, bringing small tourist groups to see the muriquis and
other threatened mammals of interest, such as the brown
howler monkeys, titi monkeys, buffy-headed marmosets
and maned sloths, which are also easy to see in these forest
fragments. We plan to analyze whether this kind of tour-
ism is viable, and whether it can bring advantages to the
project and to the local communities. We have prepared a
trail for tourists and a guide about the threatened birds and
mammals in the region. We are testing an itinerary with
volunteers and also establishing setting up a partnership
with a travel agency.

The project's main challenge is to conserve and restore the
remnant patches of Atlantic Forest, improving the connec-
tivity between the fragments and reducing the risk of ex-
tinction. To promote forest conservation we have a middle
to long-term goal, which involves actions including:
1) diagnosing the social-economic profile of the region;
2) identifying alternative forms of land use; 3) stimulat-
ing local youth to learn techniques to help in combating
forest fires; 4) conducting a program of reforestation in
public and private areas; 5) proposing the creation of pro-
tected areas; and 6) prioritizing partnerships with the local


Neotropical Primates 13(Suppl.), December 2005

society in the search for solutions. In summary, to con-
serve the muriqui over the long term in such a fragmented
landscape, we need a strategic plan that draws on scientific
knowledge and community participation, and promotes
the training of personnel, and institutional partnerships,
aiming at a broader perspective for biodiversity conserva-
tion, that fully considers the socio-economic particulari-
ties of the region.

Acknowledgments

Our conservation initiatives in Santa Maria de Jetibi and
Capara6 are supported by the Project for the Conservation
and Sustainable Use of Brazilian Biological Diversity (Pro-
jeto de Conservafdo e Utilizafdo Sustentdvel de Diversidade
Bioldgica Brasileira-PROBIO) of the Brazilian Ministry
of the Environment (MMA) and Center for Biodiversity
Conservation of Conservation International with support
of Gordon and Betty Moore Foundation, with the collabo-
ration of the Museu de Biologia Prof. Mello Leitao, Pre-
feitura Municipal de Santa Maria de Jetibi, Bombeiros Vol-
unt~rios de Santa Teresa, Instituto de Defesa Agropecuiria
e Florestal (IDAF-ES), and the Associacao de Certificadao
Chao Vivo. We are grateful for the help of V. Fagundes, P.
De Marco Jr., A. Paula, D. M. Vianna, P. Angonesi, K. B.
Strier, M. M. Furtado, P. Mangini, J. P. Boubli, C. Possa-
mai, A. Stange, B. Coutinho, F Dazilio, J. Dalla, H. Car-
reco, L. V. Monteiro, M. E Paes, M. N. Paes, J. C. Roma,
P. B. Chaves, I. S. Bergher, A. G. Aradjo, L. D. Santos, V.
0. Guimaraes, B. Almeida Silva and J. Stange.

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Neotropical Primates 13(Suppl.), December 2005 37

PRESENCE OF THE MURIQUI (BRACHYTELES HYPOXANTHUS) IN A RURAL PROPERTY
IN THE VICINITY OF THE AUGUSTO RUSCHI BIOLOGICAL RESERVE, SANTA TERESA,
ESPIRITO SANTO

Luciano A. Vieira and Sergio L. Mendes

Laborat6rio de Biologia da Conservagao de Vertebrados, Programa de P6s-graduacao em Biologia Animal CCHN, Uni-
versidade Federal do Espirito Santo (UFES), Av. Marechal Campos 1468, Maruipe, Vit6ria 29040-090, Espirito Santo, and
Museu de Biologia Professor Mello Leitao, Santa Teresa, Espirito Santo, Brazil, e-mail:


Abstract

This note reports on three sightings, in 2005, of muriquis in a forest on private land to the north of the Augusto Ruschi
Biological Reserve. The forest there is dense montane evergreen forest. The sightings were of four, three and four individuals
respectively, one of them including a female with an infant. We emphasize the importance of maintaining forest patches on
private land and their role in enhancing the survival of populations of threatened species in small protected areas such as the
Augusto Ruschi Biological Reserve.

Key words- muriqui, Brachyteles, Augusto Ruschi Biological Reserve, Atlantic forest, Espirito Santo


The occurrence of the muriqui in the montane region of the
state of Espirito Santo was documented by Aguirre (1971),
who registered their presence in five municipalities, includ-
ing Santa Teresa, for which he estimated a population of
about 150 to 180 individuals in and around the Augusto
Ruschi Biological Reserve (originally called Nova Lom-
bardia). Over the last two decades it has been possible to
record only about 10 individuals in the biological reserve
(Mittermeier et al., 1987; Pinto et al., 1993), along with
unconfirmed reports from park guards of the continued
presence of muriquis in a private property just to the north
(Mendes and Chiarello, 1993).

The Augusto Ruschi Biological Reserve is a federal protect-
ed area of 3,573 ha of dense montane evergreen forest. The
relief is of steep mountain slopes and valleys at altitudes
ranging from 780 to 1,050 m (IPEMA, 2005). About
280 families live in the vicinity, their livelihoods depend-
ant on plantations of coffee, banana, and eucalyptus. There
are a number of forest patches on these private properties.
Many of them, of small to medium size, are still well pre-
served and extend to the biological reserve, and are impor-
tant as such for the conservation of the local wildlife.

In this note we report on the occurrence of Brachyteles
S... in a forest on private land to the north of the
Augusto Ruschi Biological Reserve. They were seen three
times on a forested slope on the property of Sr. Nelson
Furlani, in a location called Alto Santo Ant6nio. The
forest there has a number of small streams which converge
to form a waterfall, the Cachoeira do Stork, flowing into
the Rio Lombardia, one of the main tributaries of the Rio
Piraqu&-Acu. The sightings of the muriquis were all within


two kilometers of the coordinates 1949'S and 4032'W
(Fig. 1).

The first time they were seen was in the afternoon of
17 February 2005, during fieldwork for the project "Plan-
ning Sustainable Landscapes in the Central Corridor of the
Atlantic Forest" (Planejando Paisagens Sustentdveis no Corre-
dor Central da Mata Atldntica). They were on a slope lead-
ing to a forested valley bottom. An individual was heard
calling and four muriquis were then seen in the canopy at
around 15 m. They remained there for four minutes before
they saw the observers and fled to the top of the hill where
the forest was denser. The second record was in the morn-
ing of 19 February 2005, about 300 m from where they
had been seen two days earlier, in a tree of about 17 m. On
this occasion, it was possible to identify a male, a female
with an infant, and two others. The male was very agitated
giving alarm calls, and rapidly moved away (A. C. Corndlio,
pers. comm.). The third occasion was in the morning of
25 August 2005 during a bird census. A group of three in-
dividuals was spotted in the canopy of a tree on the slope
across a small valley. They continued feeding quietly, appar-
ently unworried by the presence of the observers.

The local farmers reported seeing these muriquis quite fre-
quently, always in small groups of three or four, feeding
and moving through the trees along the mountain slopes.
Two of our sightings were documented: the first with a
tape recording of the alarm call ("mpg" file), and the third
by photographs. The photographs and the mpg file are in
the possession of the first author. These records emphasize
the importance of conserving the forest patches on the pri-
vate lands around the Augusto Ruschi Biological Reserve.





Neotropical Primates 13(Suppl.), December 2005


4CW360"W

Legenda:
A Muriqui localities
Rivers and streams
----- Roads
EJ IAugusto Rusch Biological Reserve
I Municipal boundary j
Forest in middle and late succession


r

1* '4~
^ - I" '


S,.


1,0,7 W


-U


L.


0 0.5 1


Figure 1. Location of the records of muriquis (Brachyteles '
Teresa, Espirito Santo.


I to the north of the Augusto Ruschi Biological Reserve, Santa


r


40D3CrO'W


3 4


iKm





Neotropical Primates 13(Suppl.), December 2005

They evidently serve as refuges for remnant populations of
threatened species such as the muriqui, and contribute sig-
nificantly to the conservation potential of such relatively
small reserves as that of Augusto Ruschi. Maintaining and
increasing the connectivity of these forest patches, especial-
ly with the larger forest of the biological reserve, is vital to
avoid the isolation of their populations and their inevitable
resulting extirpation. The discovery of these muriquis also
underlines the need to carry out research and wildlife sur-
veys on private lands as a complementary strategy to the
creation of public protected areas.

Acknowledgments

We are grateful to the Brazilian Higher Education Author-
ity (Fundafdo Coordenafdo de Aperfeicoamento de Pessoal
de Nivel Superior CAPES) for a grant to the first author.
The Brazilian State Petroleum Company (PETROBRAS)
financed the project "Planejando Paisagens Sustentdveis no
Corredor Central da Mata Atldntica". We thank Ana Caro-
lina Cornelio for providing information on these sightings
of B. 'i..' ..-'-.. and Ricardo Kawada for his suggestions
on this manuscript.

References

Aguirre, A. C. 1971. 0 mono Brachyteles arachnoides
(E. C.. o..- .). SituaadoAtualda Espcie no Brasil. Academia
Brasileira de Ciencias, Rio de Janeiro. 53pp.
IPEMA. 2005. Conservacdo da Mata Atlantica no Estado
do Espirito Santo: Cobertura Florestal e Unidades de
Conservacdo. Institute de Pesquisas da Mata Atlantica
(IPEMA), Vit6ria. 152pp.
Mendes, S. L. and Chiarello, A. G. 1993. A proposal for
the conservation of the muriqui in the state of Espirito
Santo, southeastern Brazil. Neotrop.Primates 1(2): 2-4.
Mittermeier, R. A., Valle, C. M. C., Alves, M. C., Santos,
I. B., Pinto, C. A. M., Strier, K. B., Young, A. L., Veado,
E. M., Constable, I. D., Paccagnella, S. G. and Lemos
de Sa, R. M. 1987. Current distribution of the muriqui
in the Atlantic Forest region of eastern Brazil. Primate
Conserv. (8): 143-149.
Pinto, L. P. S., Costa, C. M. R., Strier, K. B. and Fonseca,
G. A. B. 1993. Habitat, density and group size of pri-
mates in a Brazilian tropical forest. Folia Primatol. 61:
135-143.








Neotropical Primates 13(Suppl.), December 2005


REPRODUCTIVE BIOLOGY AND CONSERVATION OF MURIQUIS

Karen B. Strier

Department of Anr'..p..1..',, University of Wisconsin-Madison, 1180 Observatory Drive, Madison, WI 53706, USA,
e-mail:


Abstract

This paper summarizes some of the major findings on the reproductive biology of one group of northern muriquis
(Brachyteles .'. ,... .-.'.. "i at the RPPN Feliciano Miguel Abdala (previously known as the Estagao Biol6gica de Caratinga).
Long-term monitoring of individual members of the Matao group, combined with non-invasive fecal sampling to measure
hormone levels, provide insights into ovarian function, reproductive seasonality, and factors that influence individual and
population reproductive rates. All of these parameters have direct applications for assessing the long-term viability of this
population, and for conservation of this critically endangered species. These findings were presented at the first meeting of
the Committee for the Conservation and Management of the Muriqui (IBAMA), held in Teres6polis, Rio de Janeiro, in
October 2002; more recent data have been added or are included in the references.


Key Words primates, Brachyteles, reproductive biology, conservation


Introduction

Systematic research on muriquis at the Estagao Biol6gica
de Caratinga (EBC) in Minas Gerais, Brazil, has been un-
derway since 1982. The goals of the long-term project have
always been two-fold: i) To collect basic data on the behav-
ior, ecology, and reproduction of muriquis for the develop-
ment of informed conservation efforts on their behalf; and
ii) to train Brazilian students in methods of non-invasive
field research and its applications to conservation (Strier,
1999). Publications generated from this research through
1997 are included in the PHVA Briefing Book (Rylands et
al., 1998). A list of publications from the project from 1998
to the present can be obtained from the author. A list of the
students who have participated in the field study of the
Matao group from its onset is provided in the Appendix.

In 2001, the forest was officially transformed into a pro-
tected reserve, now known as the RPPN Feliciano Miguel
Abdala (RPPN-FMA). The muriquis there are now con-
sidered a species distinct from populations to the south:
Brachyteles .',.... .-.'o.. (Kuhl, 1820) is the northern
muriqui of Minas Gerais and Espirito Santo, and B. arach-
noides (E. Geoffroy, 1806) is the southern muriqui, occur-
ring in the states of Rio de Janeiro, Sao Paulo and Parana.

Northern muriquis have been ranked among the World's
25 Most Critically Endangered primates (Strier et al.,
2006a), and the population at the RPPN-FMA is one of
the largest populations known (Strier et al., 2002, 2006b).
The Muriqui Project of Caratinga has documented the
remarkable recovery of this population, which has nearly
quadrupled in size to more than 226 individuals over the
past 23 years (Strier et al., 2006b). Demographic data


obtained from the Matao group provided the basis for the
first Population Viability Analysis (PVA) (Strier, 1993/94),
and the subsequent Population and Habitat Viability Anal-
ysis (PHVA) Workshop on Muriquis in May 1998 (Ry-
lands et al., 1998).

The success of the RPPN-FMA muriquis to date can be
attributed to the low mortality and female-biased infant
sex ratio documented in the main study group (the Matao
group), which increased in size from 22 to 84 individu-
als from July 1982 to October 2005. Here, I summarize
new findings on the reproductive biology and demogra-
phy of the Matao group, and discuss their implications for
the conservation of the northern muriquis at the RPPN-
FMA.

Reproductive Biology

Typically, females in this population transfer out of their
natal groups when about six years old (prior to becoming
sexually active), and give birth to their first infants at about
nine years old (Strier and Ziegler, 2000). Births are con-
centrated during the dry season months, from May to Oc-
tober, with a peak from June to August (Strier et al., 2001).
Females begin to wean their infants some 12-24 months
post-partum, and resume sexual activity during their in-
fants' second year of life. The annual mating season usually
begins at the end of the dry season to early rainy season,
and the median interbirth interval is three years when in-
fants survive to weaning age. Extrapolating from what we
now know to be the age at first reproduction in females
at the RPPN-FMA, females that were carrying infants in
1982 are now estimated to be more than 30 years old. They
are still sexually, and in most cases reproductively, active.







Results from non-invasive fecal steroid analyses have pro-
vided additional insights into the reproductive biology of
wild female and male muriquis (Strier and Ziegler, 1994,
1997, 2000, 2005a; Strier et al., 1999, 2003; Ziegler et al.,
1997). Specifically:

* The seasonal onset of copulations coincides with the
onset of female ovarian cycling. Intervals between
periovulatory periods average 21.0 5.4 days (n = 7),
and females experience from 2-7 ovarian cycles prior
to their conception cycles.
* Gestation length averages 216.4 1.5 days, or
7.2 months (n = 5).
* Females disperse from their natal groups prior to the
onset of puberty. The onset of sexual activity in their
new group coincides with the onset of their ovarian
cycles.
* Inexperienced females do not conceive before their
second mating season.
* There is no evidence of seasonal fluctuations in male
testosterone levels, despite the seasonal concentration
of copulations, conceptions, and births.
* Cortisol levels in males, but not females, exhibit sea-
sonal elevations that coincide with the conception
season.
* Females appear to require minimum levels of estradiol
to resume post-partum cycling and to conceive.

Fecal steroid analyses are time-consuming and costly, and
numerous samples from specific, recognized individu-
als have been necessary to yield meaningful results to ad-
dress the kinds of questions we have examined in muriquis


Neotropical Primates 13(Suppl.), December 2005

(Strier and Ziegler, 2005b). Nonetheless, they emphasize
the importance of hormonal data to the accurate interpre-
tation of behavioral observations. For example, we now
know that females frequently copulate during the intervals
between their ovulations when conceptions are unlikely to
occur. Thus, although observations of mating behavior may
be a reliable indicator of the onset of ovarian cycling at the
onset of the mating season, they do not necessarily coin-
cide with ovulation over the duration of the mating season.
Moreover, although all of the oldest females in our study
group still cycle and copulate, two of them appear to be ex-
periencing reduced fertility similar to that of inexperienced
females during their first mating seasons. This indicates the
importance of considering female age and reproductive his-
tory when evaluating variance in female muriqui fecundity
from behavioral observations alone.

Demography of the Matio Group

Despite the late age at which female muriquis reproduce
and their relatively slow (3-year) rate of reproduction, the
Matao group has increased steadily in size (Fig. 1). This
increase can be attributed primarily to their low mortality
rates relative to birth rates.

Mortality has been low for all age-classes, but particularly
among infants, immature males and adult females. Until
recently, 94% of all infants survived their first 12 months
of life (Strier et al., 2001), but in recent years first-year sur-
vival has dropped in this group (Strier et al., 2006b). Two
13-month-old infants (1 male, 1 female) are suspected to
have died due to predation (Printes et al., 1996).


85 -
85
80 -
75 -
70 -
"E 65 -*mm m
60 E M
| 55 -
50 No
a M
45 ".
4 40 -
E .
Z 35 m*..
30
25 .
2 5 i I I ^ I I I I I I I I I I I I I I I I I I I I I I I I I I I I I I I I I I I I I I I I
20
'82 '83 '84 '85 '86 '87 '88 '89 '90 '91 '92 '93 '94 '95 '96 '97 '98 '99 '00 '01 '02 '03 '04 '05
Year

Figure 1. The Matao study group, RPPN-Feliciano Miguel Abdala, Caratinga, Minas Gerais. Growth in size from July 1982 to 2005.





Neotropical Primates 13(Suppl.), December 2005

All of the males born since 1982 that have survived to
3 years of age are still alive and present in their natal group.
Survival rates of immature females are more difficult to
document because only three of the natal females that
survived to six years of age have remained and reproduced
in this group (Strier et al., 2006b; updated from Martins
and Strier, 2004). Data on female survivorship after dis-
persing from the Matao group are limited for females that
dispersed prior to 1994. However, 17 of the 22 natal Matao
females that dispersed between 1994 and 2004 have been
confirmed in their new groups, and 16 of these 17 females
are still alive as of October 2005 (Strier et al., 2006b). Ages
at first birth are now known for six of these females, and
are consistent with those estimated for females that immi-
grated into the Matao group (Strier et al., 2006b, updated
from Strier et al., 2002).

Seven of the eight adult females present in 1982 are still
alive. By contrast, all of the six adult males and both of
the old juvenile/subadult males present in 1982 have died,
with the longest surviving of these adult males dying in
September 2005.

The number of female immigrations into the Matao group
matched or exceeded that of Matao emigrants until 1993.
Since then, however, female emigrations have outpaced im-
migrations (Fig. 2).

There are a number of possible explanations for this phe-
nomenon, each of which requires close and continuous
monitoring of infant and immature females in the entire
population. For example, the higher emigrant-to-immigrant


ratio for the Matao group might reflect a high mortality rate
(-43%) characteristic of dispersing females. To evaluate
whether this is the case, we need to monitor all females that
disperse from their natal groups to determine whether they
succeed in joining another group, or die during the process
of dispersing. Alternatively, it could reflect differences in
infant sex ratios and survivorship in different groups. The
high emigrant-to-immigrant ratio would then be a prod-
uct of the disproportionate number of females born and
surviving in the Matao group relative to other groups in
the forest. It will be important to document the long-term
survivorship of Matao emigrants, including those that are
confirmed to have joined new groups. Until recently, the
Matao group appeared to be a "source" of females in this
population, but it was not possible to determine whether
natal Matao females were dispersing into a "sink." We now
know that a disproportionate number of dispersing females
from other natal groups prefer to transfer into the Matao
group, and that most recent Matao emigrants survive and
reproduce in their new groups (Strier et al., 2006b).

One of the strongest results to emerge from the long-term
demographic data is the female-biased infant sex ratio that
has characterized the Matao group since the onset of the
study (Strier, 2000). A total of 118 infants have been born
from June 1982 to October 2005, of which 114 have been
sexed. Of these 114 infants, 65, or 55.26%, were female.
The number of females born was equal to or greater than
the number of males born in most of the annual birth co-
horts until 2000, when this female-bias in infant sex ratios
began to reverse (Fig. 3).


Figure 2. Dispersal patterns of females, Matao study group, RPPN-Feliciano Miguel Abdala, Caratinga, Minas Gerais. 1982-2002.


28
26 -
24 -- Emigrants from Matao group (if > 4 years)
* 22 Immigrants to Matao group
E 20
S18 0
S16 0
E 14
S12 ii n
> 10 11 l

E 6
) 4 0
2 I [ I I I I I I I I I I I I I I I I I I
0
'82 '83 '84 '85 '86 '87 '88 '89 '90 '91 '92 '93 '94 '95 '96 '97 '98 '99 '00 '01 '02


Year





Neotropical Primates 13(Suppl.), December 2005


2005
2004
2003
2002
2001
2000
1999
1998
1997
1996
M 1995
1994
1993
1992
1991
1990
1989
1988
1987
1986
1985
1984
1983
1982 I I I
-10 -8 -6 -4 -2 0 2 4 6
Males Females
Figure 3. Sex by birth cohort in the Matao Group, RPPN-Feliciano Miguel Abdala, Caratinga, Minas Gerais. 1982-2005.


It is too soon to evaluate whether this recent shift from
female to male-biased infant sex ratios will persist over
time. Nonetheless, if this trend continues, it will have a
dampening effect on the RPPN-FMA muriquis' popula-
tion growth (Strier et al., 2006b). This effect will not be
evident for another 10 years or so, when females from these
birth cohorts begin to reproduce, as the PVA analyses in-
dicated (Strier, 1993/94). Nonetheless, it may be an early
indication that this population is beginning to stabilize.

Monitoring the behavioral changes that accompany chang-
es in the demography of the RPPN-FMA muriquis is now
a priority for our ongoing research on the Matao group (for
example, Dias and Strier, 2003). The demographic data-
base is particularly important to maintain, not only for the
insights on infant sex ratios and survivorship, but also be-
cause of the indications of declining fertility among some
of the oldest females (>30 years) in this group. At the same
time, understanding the ecological variables that contrib-
ute to the carrying capacity of the forest at the RPPN-FMA
is a priority of the recent collaborative project initiated on
the Ja6 group in 2001 (Strier and Boubli, 2006).

The long-term viability of the RPPN-FMA muriquis is
critical to the future survival of this species. Our ongoing
studies here will continue to provide valuable insights into
the reproductive ecology and population demography of
this vital population.


Acknowledgments

The long-term research at the RPPN-FMA would not have
been possible without the permission and support of the
Abdala family, beginning with Sr. Feliciano and continuing
with his grandson, Ramiro. I am grateful to them, as well as
to the Brazil Science Council (Conselho Nacional de Desen-
volvimento Cientifico e Tecnolkgico- CNPq) and the Brazil-
ian Institute for the Environment (Instituto Brasileiro do
Meio Ambiente e dos Recursos Naturais Renovdveis IBAMA)
for the licenses they have provided me over the years. Drs.
Cdlio Valle, Csar Ades, Gustavo da Fonseca, and S&rgio
L. Mendes have served essential roles as sponsors. Jairo
Gomes and the late Eduardo Veado provided essential lo-
gistical support and friendship over the years. E. Veado,
J. Gomes, F. Mendes, J. Rimoli, A. 0. Rimoli, E Neri, P.
Coutinho, A. Carvalho, L. Oliveira, C. Nogueira, S. Neto,
W Teixeira, R. Printes, and M. Maciel, C. Costa, A. Oliva,
L. Dib, D. Carvalho, N. Bejar, C. Coelho, L. Dias, V. 0.
Guimaraes, W P. Martins, J. C. da Silva, C. de Borba Pos-
samai, Regiane R. de Oliveira, F P. Paim, M. E Iurckk, K.
Tolentino, V. Souza, D. Guedes, J. Fidelis de Oliveira, F
Tabacow, and M. Loucenga contributed to the long-term
demographic data. The long-term research has received
support from NSF grants BNS 8305322, BNS 8619442,
and BNS 8959298, the Fulbright Foundation, grant no.
213 from the Joseph Henry Fund of NAS, Sigma Xi, the
L. S. B. Leakey Foundation, the World Wildlife Fund, the





Neotropical Primates 13(Suppl.), December 2005

Seacon Fund of the Chicago Zoological Society, the Liz
Claiborne and Art Ortenberg Foundation, the Scott Neo-
tropic Fund of the Lincoln Park Zoo, the National Geo-
graphic Society, the Margot Marsh Biodiversity Founda-
tion, Conservation International's Primate Action Fund,
and the Graduate School of the University of Wisconsin-
Madison. I am grateful to IBAMA and Tereviva for hosting
the Workshop at which an earlier version of this paper was
presented, and for the opportunity to serve as a member of
the Muriqui Committee.

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liciano Miguel Abdala, Minas Gerais, Brazil. Am. J. Phys.
Anthropol. 130: 227-237.
Ziegler, T. E., Santos, C. V., Pissinatti, A. and Strier, K. B.
1997. Steroid excretion during the ovarian cycle in cap-
tive and wild muriquis, Brachyteles arachnoides. Am. J.
Primatol. 42: 311-321.





Neotropical Primates 13(Suppl.), December 2005


Appendix

Student participation in the Muriqui Project of Caratinga, Matao Project. Strier and Boubli (2006) provide a list of all
student participants in muriqui research at the RPPN-FMA through 2005.

2005-2006 Fernanda Tabacow (Bachelors from Universidade Federal de Espirito Santo)
2005-2006 Maira de Loucenco Assunmao (Undergraduate at Pontificia Universidade Cat61lica de Minas Gerais)
2004-2005 Janaina Fidelis de Oliveira (Undergraduate at Pontificia Universidade Cat61lica de Minas Gerais)
2004-2005 Danusa Guedes (Bachelors from Pontificia Universidade Cat61lica de Minas Gerais)
2003-2004 Karynna T. de Souza (Bachelors from Pontificia Universidade Cat61lica do Parana; currently MA student)
2003-2004 Vagner de Souza (Bachelors from Universidade Federal de Espirito Santo; currently MA student)
2002-2003 Fernanda P. Paim (Bachelors from Universidade do Vale do Rio dos Sinos, Rio Grande de Sul)
2002-2003 Maria Fernanda E E lurck (Bachelors from Pontificia Universidade Cat61lica do Parana)
2001-2003 Carla de Borba Possamai (Bachelors from Pontificia Universidade Cat61lica do Parana; currently MA student)
2001-2002 Regiane Romanini de Oliviera (Bachelors from Universidade Federal de Vicosa; currently MA student)
2000-2001 Jos6 Cassimiro da Silva J6nior (Bachelors from Universidade Federal de Minas Gerais)
1999-2001 Waldney E Martins (Bachelors from Universidade Federal de Minas Gerais, currently MA student)
1999-2001 Vanessa O. Guimaraes (Bachelors from Universidade Gama Filho, Rio de Janeiro)
1998-1999 Luiz Gustavo Dias (Bachelors and Masters from Universidade Federal de Minas Gerais)
1998-1999 Cristiane C. Coelho (Bachelors and Masters from Pontificia Universidade Catolica de Minas Gerais)
1998-1999 Claudio P Nogueira (Doctorate from Universidade Federal de Minas Gerais)
1997-1998 Dennison Carvalho (Bachelors from Universidade Federal de Minas Gerais)
1997-1998 Nilcemar Bejar (Bachelors from Universidade Federal de Minas Gerais)
1996-1997 Andreia Silene de Oliveira (Bachelors from Faculdades Metodistas Integradas Izabela Hendrix, Belo Horizonte)
1996-1997 LaienaT. Dib (Masters from Universidade Federal de Minas Gerais)
1995-1996 Claudia G. Costa (Masters from Universidade Federal de ParS)
1994-1996 William A. Teixeira (Bachelors from Pontificia Universidade Cat6lica de Minas Gerais)
1994-1995 Maria Amelia E Maciel (Bachelors from Universidade Federal de Vicosa)
1994-1995 Rodrigo Cambara Printes (Bachelors from Universidade Federal de Rio Grande de Sul; Masters from Universidade Federal de
Minas Gerais, currently PhD student)
1993-1994 Sebastiao da Silva Ramos Neto (Bachelors from Universidade Federal de Vicosa)
1993-1994 Adriana Oddlia Rimoli (Doctorate from Universidade de Sao Paulo)
1992-1994 L6cio P de Oliveira (Bachelors from Universidade Federal de Juiz de Fora)
1992-1994 Claudio P Nogueira (Masters from Universidade de Guarulhos)
1992-1993 Ana Rosa Dias de Carvalho (Bachelors from Universidade de Taubate)
1991-1992 Paulo Coutinho (Universidade Federal de Pari, Masters earned)
1991-1992 Fernanda Neri (Universidade Federal de Minas Gerais, Masters earned)
1990-1991 Francisco D. Mendes (Doctorate from Universidade de Sao Paulo)
1987-1990 Jos6 Rimoli (Masters from Universidade de Sao Paulo)
1989-1990 Adriana Odalia Rimoli (Masters from Universidade de Sao Paulo)
1986-1987 Francisco D. Mendes (Masters from Universidade de Sao Paulo)
1983-1984 Eduardo M. V. Veado (Bachelors from Universidade Federal de Minas Gerais)





Neotropical Primates 13(Suppl.), December 2005


THE CARATINGA ALLIANCE: COMMUNITY-BASED CONSERVATION EFFORTS TO
INCREASE FOREST FOR THE MURIQUIS AND WATER FOR THE FARMERS

Francisco B. Pontual1'2'3 and Jean P. Boubli4

' Conservagao Internacional -Brasil, Av. Getdlio Vargas 1300, Belo Horizonte 30112-021, Minas Gerais, Brazil
2 Sociedade para a Preservagao do Muriqui, Caratinga, Minas Gerais, Brazil
3Department of Environmental Science, Policy and Management, 345 Giannini Hall, Berkeley, CA, 94720-3114, USA,
e-mail:
'Department of Anr-i. .p. .1..,, The University of Auckland, New Zealand


Abstract

The northern muriqui is Critically Endangered. About 25% of the known population lives in the 1,200 ha of secondary for-
ests of the Caratinga Biological Station (EBC) Feliciano Miguel Abdala Private Natural Heritage Reserve (RPPN-FMA) and
neighboring farms. Long-term survival of the muriquis there depends on an increase in the availability of suitable habitat.
Widespread deforestation has depleted soil fertility and dried up the streams in the region. Community-based conserva-
tion actions were carried out: 1) to protect and restore degraded areas to increase the availability of forests for the muriquis,
and 2) to implement reforestation to improve the water balance vital for the regional recovery of rural production. Rural
extension courses were provided for the local communities, which introduced modern production techniques to increase
efficiency while decreasing environmental impacts. A new plant nursery was built and a pilot project to test forest restoration
techniques was initiated.

Key Words- northern muriqui, Brachyteles .':.... .-o'.. community-based conservation, restoration of degraded areas,
rural capacity-building, Atlantic forest


Introduction

Socio-environmental panorama
The once-continuous Atlantic Forest in the east of the state
of Minas Gerais, is now extremely fragmented. Coffee
drove the conversion of enormous tracts of semi-decidu-
ous forests, with extremely high socio-environmental costs
(Dean, 1995). The northern muriqui (Brachyteles hypoxan-
thus) was one of many that suffered. It is now considered
one of the 25 most endangered primates in the world (Strier
et al., 2006a). Today, more than 230 northern muriquis, or
25% of the known population, inhabit an island of about
1200 ha of secondary forest at the Estagao Biol6gica de
Caratinga / Reserva Particular de Patrim6nio Natural Feli-
ciano Miguel Abdala (EBC/RPPN-FMA) and neighboring
farms. The long-term survival of this population depends
on increasing the area of forest available for the muriquis
(Strier, 1993-1994).

Widespread deforestation and obsolete agricultural tech-
niques have depleted soil fertility in the region and severely
reduced the availability of water in the streams that run
through the neighboring farms of the EBC/RPPN-FMA.
Numerous people have become aware of this; most of them
practicing family-based agriculture of coffee, corn, sugar
cane, rice and beans. Cattle-ranching is also a common ac-
tivity in the region. With soils depleted of their nutrients,


farmers turn to milk production for some income. The
extensive ranching, in turn, contributes to the compacting
and erosion of the remaining land that could otherwise be
used for agriculture if correctly managed (IDEA, 1996).

Traditionally, the forest has been seen as an almost infinite
source of timber, firewood, and game but, most important-
ly, as something to get rid of in order to initiate any 'real'
economic activity. Deforestation was seen as the essential
first step in 'developing' an area, and for centuries, the rev-
enues provided by ecosystem services were almost entirely
neglected by most of the local farmers and land owners.
Today, the more aware recognize soil fertility, water main-
tenance and pest control as some of the most useful ecosys-
tem services, now lost due to deforestation. Although some
conservation-oriented perceptions are shared by many local
people, neither muriquis nor their conservation are consid-
ered a top-priority (Bueno, 2005).

As is typical of human nature, an environmental crisis is
necessary before people can perceive that, instead of an
obstacle, the forest can be helpful for maintaining rural
production. Understanding the socio-economic and en-
vironmental contexts that influence the local communi-
ties, their lives and perspectives is essential prior to pro-
posing any practical solutions that could reverse this
dramatic panorama. Encouraging the adoption of more







sustainable-oriented production techniques may require
above all a demonstration of its practicality: "seeing is be-
lieving" (Goodwin, 1998; Twyman, 2000).

Initial conservation efforts
Karen Strier's research on the northern muriqui at the
EBC/RPPN-FMA began in the early 1980's (Strier,
1999). The initial focus was centered on their ecology
and behavior, but was gradually expanded to encompass a
much wider perspective on the conservation needs of the
muriqui population and the forest remnants (Strier, 1999;
Strier and Boubli, 2006; Strier et al., 2006b). In 1988,
the first local environmental NGO, Associafdo Prd-Estadao
Bioldgica de Caratinga (ApEBC), was created and became
involved in a number of conservation projects and initia-
tives. In 1994, the ApEBC initiated its first contacts with
the local communities, and worked with the Instituto de
Ecodesenvolvimento Agricola (IDEA) to conduct the first
socio-environmental diagnosis in the region surrounding
the EBC/RPPN-FMA. At the same time, ApEBC built a
nursery to produce seedlings of native species to be used
for the recuperation of degraded areas in the EBC/RPPN-
FMA. In 2001, as an honor to the late conservationist and
patriarch, Feliciano Miguel Abdala, his family decided to
turn the 957-ha forest of the Fazenda Montes Claros into
a Private Natural Heritage Reserve (RPPN), an officially
recognized category of protected area in Brazil. A three-
year floristic inventory and phenology study was begun in
2002, which served to demonstrate the botanical and eco-
logical importance of the muriqui's forest habitat (Boubli
et al., 2003). In 2002, the Sociedade para a Preservafao do
Muriqui (SPM) was founded to manage the EBC/RPPN-
FMA and propose other conservation projects to protect
the northern muriqui and restore its local habitat.

Muriqui Conservation Project
In mid-2003, we invited the then Director of the ApEBC,
the late Eduardo Veado, to collaborate on a proposal for
a comprehensive conservation project. Eduardo contrib-
uted with the concepts of fencing the RPPN to protect the
forest from cattle invasions and of developing a new nurs-
ery to produce seedlings for the restoration of degraded
areas. The proposal was approved as a PROBIO/Brazilian
Ministry of the Environment/GEF project entitled Muriq-
ui Conservation (MC). The project created a network of
partnerships that included ApEBC, SPM, Conservation
International's regional Brazil office (CI-Brazil), the Insti-
tuto Driades, the Caratinga city council, and the National
Rural Extension Service (Servico Nacional de Aprendizagem
Rural- SENAR-MG), among others. Synthesizing current
information on the muriquis, and the plans and measures
for their conservation in Caratinga, it resulted in a pro-
posal for community-based, grass-roots development that
should work towards the common goals of both scientists/
conservationists and farmers (Pontual et al., 2005).

The Muriqui Conservation project had four components:
1) a macroecological synthesis of the genus Brachyteles;


Neotropical Primates 13(Suppl.), December 2005

2) an in-depth study of muriqui ecology; 3) the develop-
ment of a community-based conservation action plan; and
4) a pilot project for the recuperation of degraded areas. In
this paper, we present the preliminary results and future
perspectives of the socio-environmental activities initiated
or expanded in February 2004.

Methods

Conceptual tripod
Although the Muriqui Conservation project was based on
the experiences and knowledge gathered throughout the
past two decades of conservation efforts in Caratinga, a
new approach to the socio-environmental problems was
proposed. This has been the adoption of three conceptual
tenets upon which all our initiatives were based: 1) the
need for the definition of common goals; 2) for ground-
up development; and 3) for collaborative group efforts
(mutirdo). The common goals were the recuperation of de-
graded areas to increase the availability of habitat for the
muriquis and the need improve the regional water balance
to support rural production. We began with free extension
courses to improve rural production efficiency. Members of
the local communities volunteered their support as partners
in the project. Decisions were made by consensus together
with the landowners involved.

Community mobilization
We initiated community mobilization by inviting the
EBC/RPPN-FMA neighbors to attend free rural extension
courses (Fig. 1). The courses were conducted by the Rural
Extension Service (SENAR-MG), a private, rural capacity-
building institution sponsored by the state of Minas Gerais
Agriculture Federation, an increasingly important partner
of MC. The course instructors were skilled, retired Univer-
sity professors that taught theoretical and practical classes
totaling 40 hours per course. All students had to achieve
high standards of understanding and hands-on techni-
cal abilities to be awarded the certificate for the course.
Although such courses are usually offered to farmers that
live closer to urban centers, our project was able to make
these courses available to the isolated communities sur-
rounding the reserve.

The MC mobilization team consisted of two local people,
Ant6nio Braganga and Janaina Mendonga, both communi-
cative and already well known in all the communities. The
first reactions were a little skeptical but, after the first exten-
sion course was concluded, the picture changed and many
participants volunteered for the following courses. The MC
team designed practical exercises during the courses to show
the farmers the advantages of recuperating degraded areas
in protecting springs and restoring fertility to the soils. The
idea was to show how habitat recovery had a direct effect on
water availability, soil fertility and pest control.





Neotropical Primates 13(Suppl.), December 2005 49

Recuperation of degraded areas 4) conducting a pilot experiment to test recuperation tech-
The recuperation of degraded areas involved four lines of niques. Fences were built with chemically treated, auto-
action: 1) fencing off springs and forest remnants to pre- claved, 2.2-m eucalyptus stakes, using 250 stakes/km with
vent the entry of cattle; 2) building a new plant nursery; four lines of galvanized, smooth wire. A circle of a mini-
3) transplanting seedlings to enrich degraded areas; and mum of 40 m diameter was fenced off around the springs to


Figure 1. Map of the RPPN-FMA and its neighbors (Eduardo M. Veado, ApEBC).







protect them. The new nursery was built in an enclosure of
75 x 85 m, using gravity powered water aspersers, and natu-
ral sunlight with the appropriate shade, and fertilizer NPK
04-14-08. The estimated production was 80,000 seedlings/
year. Seedlings to enrich degraded areas were planted with
a 3 x 3-m spacing, using 40 x 40 x 40 cm pits prepared with
18 liters of cattle dung and 50 g of calcareous powder.

The pilot experiment was begun in an 8,400 m2 fenced
area to test different recuperation techniques. The area was
divided into 16 plots of 21 x 25 m. The plots were arranged
in four groups to test the efficiency of different recuperation
techniques: 1) seedlings transplanted to high diversity is-
lands; 2) artificial perches to encourage birds to drop forest
seeds; 3) translocation of soil from the reserve, importing,
as such, the forest seed bank; and 4) natural regeneration
(no treatment). A fifth plot group was maintained outside
the fenced area to compare the grazing and trampling ef-
fects over the other techniques of regeneration (Boubli and
Strier, 2004; Pontual et al., 2005).

Results and Discussion

Rural capacity building
From May 2004 to July 2005, 13 SENAR-MG courses
were run for the locals with the support of a number of
local partners, including the Ipanema Rural Union, and
the Cooperative of Producers of Ipanema (CAPIL). The
courses were varied: 11 involved rural extension (five
on the fundamentals of cattle-ranching, four concern-
ing bovine nutrition and two about artificial insemina-
tion) and two taught fabric painting techniques. In total,
184 students from 12 local communities participated, and
were subsequently awarded a federally-recognized certifi-
cate for the completion of the course, issued by SENAR-
MG. Following our commitment to let the locals choose
their options, most of the courses requested were related
to livestock management. We hoped that this would help
increase productivity, while decreasing environmental
impacts. Cattle-ranching may be one of the least sustain-
able economic activities for tropical forest regions (Belsky
and Blumenthal, 1997; Fortney, 2000), but we decided
it would be better to improve the efficiency of the more
traditional and current production activities before sug-
gesting the introduction of exotic alternatives (Savage,
1997). This seemed especially important after the frustrat-
ing experiences that some of the farmers had suffered in
attempts at organic coffee farming (Roberto Abdala, pers.
comm.). The information gathered during the courses was
immediately put into practice.

The traditional concept that forest should be replaced by
open areas to increase rural production was challenged
from the perspective of the farmer's economics. A change
in attitude was based on a "less is more" concept. In other
words, local people learned that it is more productive to
have fewer livestock, to feed them correctly using less
pasture, providing better nutrition, and to use artificial


Neotropical Primates 13(Suppl.), December 2005

insemination techniques to breed animals of better quality.
This ultimately will account for an increased milk produc-
tion with a decrease on environmental impacts and unpro-
ductive work for the farmers. Artificial insemination may
be the key for this socio-environmental improvement.

An insemination nitrogen bottle with 80 doses of high
quality Frisian PO semen was donated by the Caratinga
City Council to the Sao Vicente community. Supported
by MC, two other communities, Boa Esperanga and Pouso
Alegre, received a commitment from the Ipanema City
Council that a second insemination bottle would be do-
nated. Also supported by MC was the training of a local
Animal Health Agent, Albino Modesto de Souza, who has
been visiting the communities, providing official vaccina-
tion and other animal health programs.

Protection and Recuperation
The Muriqui Conservation Project provided for the con-
struction of 14 km of fences around the EBC/RPPN-FMA
and five other properties, to protect springs and forests that
were under pressure from cattle grazing. Funding limitations
have impeded the protection of more areas. Many other
landowners were willing to have their springs and forest
remnants fenced because their water supply from the creeks
had diminished, and the cattle were eating poisonous lianas
in the forests causing numerous deaths and abortions.

The new nursery has produced 40,000 seedlings from
35 native species. Seeds were collected in the forest. Some
6,000 seedlings of 31 species were transplanted to enrich
degraded areas around springs and forest edges. In six
months of field work, 30 ha was protected and planted. The
recuperation pilot project is still in progress. The growth of
the seedlings is being measured every 90 days, but it is too
early to report on any results.

Regional partners and alliances
Used to isolation and a lack of any official support, the com-
munities around the EBC/RPPN-FMA would rely on their
traditions to survive. Most local people are skeptical about
change. The mutirao is a local concept commonly used to
repair a broken bridge or refurbish an old chapel, for in-
stance. Nonetheless, our invitation to join in a group effort
to protect and restore degraded areas was a strange novelty,
especially after we explained that brand new, highly qual-
ity fences would be built inside the partners' properties, in
areas that both project staff and farmers would agree upon.
Some people suspected that they would have to pay for the
fences. Thus, the first protection and restoration measures
were carried out in the EBC/RPPN-FMA, so as to demon-
strate that there were no tricks, and to help the local people
understand what MC was proposing.

When Jos6 Alcino, a local landowner, accepted the terms
and became our first partner, his neighbors told him he
was unwise to trust us. They were sure that, after fencing
his spring and forested border, we would take his land





Neotropical Primates 13(Suppl.), December 2005

from him. However, after a couple of extension courses
many farmers offered their land to be the next recipients
of MC fences. Of the 47 neighboring properties of the
EBC/RPPN-FMA, 45 declared themselves our partners,
although only a small number actually received any fence
or seedlings due to funding limitations.

On 27 August 2005, the I Festival do Muriqui took place in
Santo Ant6nio, the closest town to the EBC/RPPN-FMA.
The festival was organized by local people and MC staff as
a celebration of the mutirdo. During three days of festivi-
ties, there were regional music shows, horse parades, and a
barbecue, with the participation of more than 8,000 people
from the region. For a more select group, the highlight was
the formal ceremony in which local authorities and com-
munity representatives gave the 184 course conclusion cer-
tificates to the people that attended the extension courses.
All were invited to receive the diploma, issued by SENAR-
MG, in front of thousands of witnesses.

The Muriqui Conservation (MC) is working on further
proposals to continue the program for the protection and
recuperation of degraded areas. Twenty landowners have
signed legal documents attesting that they were willing
partners in providing for the conservation and recovery of
the Areas of Permanent Protection (forest on steep slopes
and along water courses) on their properties as they should
according to Brazilian environmental law. The activities of
the MC brought new insights and perspectives to the local
communities, and they became real partners. Isolation and
lack of training has been gradually replaced by dignity and
recognition. An alliance between conservationists and the
EBC/RPPN-FMA neighbors has been initiated to work for
a more sustainable future for the muriquis and the local
communities (Pontual et al., 2006).

Acknowledgments

This project was financed by the Project for the Conserva-
tion and Sustainable Use of Brazilian Biological Diversity
(Projeto de Conservacao e Utilizafao Sustentdvel de Diversi-
dade Biologica Brasileira PROBIO) of the Brazilian Min-
istry of the Environment (MMA), the International Bank
for Reconstruction and Development- World Bank (Banco
International de Reconstrufdo e Desenvolvimento-BIRD),
the Global Environment Facility (GEF), the Brazil Science
Research Council (Conselho Nacional de Desenvolvimento
Cientifico e Tecnoldgico CNPq) and the Zoological Society
of San Diego. We thank the Sociedade para a Preservagao
do Muriqui (SPM) for authorization and support to carry
out our research and conservation activities in the Estagao
Biol6gica de Caratinga (EBC) / RPPN Feliciano Miguel
Abdala (EBC/RPPN-FMA), the staff of the project Muriq-
ui Conservagao (MC), the local communities, Instituto
Driades, the Associacao Pr6-Estagao Biol6gica de Caratin-
ga (ApEBC), Conservagao Internacional do Brasil, Servigo
Nacional de Aprendizagem Rural (SENAR-MG), and the
Caratinga City Council.


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Neotropical Primates 13(Suppl.), December 2005


CONSERVATION RESEARCH ON THE SOUTHERN MURIQUI (BRACHYTELES
ARACHNOIDES) IN SAO PAULO STATE, BRAZIL

Mauricio Talebi and Pedro Soares

Associacao Pr6-Muriqui, Parque Estadual Carlos Botelho, Sao Paulo, Brazil, e-mail:


Abstract

In this paper we present an overview of the past and current conservation research on southern muriquis, Brachyteles
arachnoides, in the state of Sao Paulo, most particularly in the forests of the Serra de Paranapiacaba, in four connected
protected areas, which comprise the so-called Paranapiacaba Ecological Continuum: the state parks of Carlos Botelho,
Intervales, and Alto Ribeira and the Xitu6 Ecological Station. These areas are the major stronghold for this species, and we
discuss particularly the history of research on the muriquis of the Carlos Botelho State Park and the importance of statewide
surveys and the establishment of further long term research sites to understand better its status and for the elaboration of
management plans for its conservation.

Key Words primates, southern muriqui, Brachyteles, Serra da Paranapiacaba, ecology, field studies, conservation


Introduction

Among the best-preserved and largest remnants of Brazil's
Atlantic forest are found on the slopes of steep mountain
ranges in Sao Paulo, a state which is also the most industrial-
ized and populous in the entire country (Mittermeier etal.,
1987). The forests run parallel to the coastline and in the
south turn inland. Most are officially protected, being part
of the protected area system administered by the Sao Paulo
State Forestry Institute (Morellato and Haddad, 2000).
The single largest forest tract, known as the Paranapiacaba
Ecological Continuum (PEC) (see Table 1; Fig .1), is of
major biological importance and comprises 140,000 ha of
continuous forest of numerous types and in all stages of
ecological succession. It consists of four protected areas,
and is the core of a World Heritage Site, "The Southeast
Reserves of Atlantic Forest" (UNESCO, 1999).

The maintenance of large expanses of natural habitat un-
derlies any broad biodiversity conservation strategy (Pisci-
otta, 2002). In the case of the Atlantic forest, the Parana-
piacaba Ecological Continuum is probably the last natural
area for numerous endemic species and provides, besides,
the potential to harbor the largest remnant populations of
the southern muriqui.

Threats

The geographical distribution and status of the southern
muriqui populations in Sao Paulo are still poorly known.
Although it would appear that they occur naturally at lower
densities in large expanses of forest than in smaller, frag-
mented forests, these wild muriqui populations are quickly
declining. The following are the current principal threats
to the muriquis.


Forest loss. Less than 7% of the muriqui's forests remain,
and much of what does is highly fragmented. Deforestation
has occurred as a result of logging, intensive land-use for
subsistence and commercial farming (for example, coffee),
timber plantations (eucalyptus and pine) and cattle ranch-
ing, through urban expansion, and highway construction
and general infrastructure development, both regional and
national, such as dams and the leisure industry. Despite its
protected status, the Paranapiacaba Ecological Continuum
will always be under threat from developmental pressures
such as these.

Hunting for sport. Historically, and even today in some
areas, the muriqui is hunted for sport, a cultural trait that
has remained from the earliest days of the colonization of
Sao Paulo State by Europeans.

i,L',;og in the buffer zones of protected areas. This refers par-
ticularly to bauxite, sand, clay, and granite. These activities
result in deforestation, erosion, flooding, and the silting
and pollution of rivers and streams.

Lack ofan adequate captive breeding program. Captive breed-
ing has been problematic due to low levels of reproduc-
tion and poor infant survival. Some zoos in Sao Paulo (for
example, Sorocaba and Santos) receive wild-born muriqui
pets every year, originating mostly from palm-harvesters
and hunters who have killed the mother. Investment in a
well-managed breeding program would greatly enhance
our understanding of the primates and provide a backstop
for population extinctions in the wild.

Illegal palm-harvesting in large areas of forest. The palm
tree, Euterpe edulis, is endemic to the Atlantic Forest,
and an economically important forest product. Palm tree







harvesters, palmiteiros, camp in the forest and transport
and process the palm hearts in glass jars, while still in the
forest. Thousands of palm trees can be felled in just a few
days. Populations of E. edulis are declining everywhere in
areas where they used to be the dominant understorey tree.
Palmiteiros hunt game, including muriquis, during their
sojourns in the forest.

In spite of little official concern, palm tree harvesting is
today one of the main threats to wild muriqui populations.
The presence of palmiteiros in Sao Paulo state's protected
forests is reported by villagers, but few arrests result. We
cannot afford to ignore these long-term anthropogenic
pressures on the remaining populations of wild muriquis
in Sao Paulo (Talebi, 2004). Due mainly to hunting, it
is probable that wild muriqui populations are declining
everywhere.


Neotropical Primates 13(Suppl.), December 2005

Research on the Southern Muriqui in Sio Paulo

Following the distribution-wide survey of Aguirre (1971),
the first behavioral and ecological studies on the genus were
begun in the early 1980s. Torres de Assumpcao (1983a,
1983b) and Milton (1984, 1985a, 1985b, 1986) established
a field site for the southern muriqui at the Fazenda Barreiro
Rico in Sao Paulo (Fig. 3), and Strier, following the initial
studies by Nishimura (Nishimura et al., 1988), began her
research on the northern muriqui at the Fazenda Montes
Claros, subsequently the Caratinga Biological Station, in
Minas Gerais in 1982 (Strier, 1999). Both sites were small
forest fragments in regions otherwise heavily farmed but
where, perchance, the landowners had provided for the sur-
vival of the muriquis by prohibiting hunting. The terrain in
both was favorable for the typically arduous work involved.
Strier and Fonseca (1996-1997) listed 19 sites where muri-
quis were known to occur, 10 of them in the state of Sao
Paulo. Of these, all but one (the Fazenda Barreiro Rico in
east-central Sao Paulo) were in large expanses of remote for-
ests in the Serra do Mar, where muriquis naturally occurred


Table 1. Protected areas of the Paranapiacaba Ecological Continuum (see Fig. 1).
Official denomination Area (ha) Main Features Reference
A Carlos Botelho State 37,432 Largest population of muriquis in Brazil Mittermeier et al. (1987)
B Intervales State Park 45,000 Highest diversity of flora of Sao Paulo State Petroni (2000)
C Alto Ribeira State Park 55,000 Large caves, ecotourism infrastructure UNESCO (1999)
D Xitue Ecological Station 3,095 High levels of disturbance, regenerating forest Gonzalez-Solis et al. (2001)





























Figure 1. Map showing the protected areas of the "Paranapiacaba Ecological Continuum" and the study areas ( ) of wild southern
muriquis in the Carlos Botelho State Park. A = Carlos Botelho State Park, B = Intervales State Park, C = Alto Ribeira State Park, and
D = Xitud State Ecological Station (see Table 1).





NeotropicalPrimates 13(Suppl.), December 2005

at very low densities. Surveys and field studies of muriquis
in these montane habitats, however, were, and still are, se-
verely hampered by the rugged topography (Pinto et al.,
1993; see Fig. 2), and attempts to establish field sites in the
Serra do Mar in both Rio de Janeiro and Sao Paulo have
severely tested the endurance of many (see, for example,
the difficulties in even finding the muriquis as related by
Garcia, 2005).

Following initial surveys by Paccagnella (1991), the Carlos
Botelho State Park in Sao Paulo began to emerge as the best
option for field studies in these montane habitats. Strier
(1999) set up a field base there in 1986 (see below), estab-
lishing the only long-term site for muriquis in less-disturbed
and continuous rather than fragmented forest-providing
information which is vital for comparative studies and a
full understanding of their demography and ecological
needs (Rylands et al., 1998).

Southern Muriqui Research Field Sites in Sio
Paulo

There are five important field sites in the state of Sao Paulo
where research has been carried out on the behavior and
ecology of B. arachnoides (Fig. 3). We have character-
ized them according to 1) Forest condition -forest frag-
ments (FF) or more extensive (continuous) forest (CF),
2) Duration of studies- Short-term (2-3 years at most)
(ST), or Long-term (LT), and 3) Current status offield re-
search- Discontinued (Dis) or Ongoing (On).

Fazenda Barreiro Rico (FF, ST, Dis) (2241'S, 4806'W)
While the other muriqui field study sites are all in moun-
tainous areas of the Serra do Mar, the Fazenda Barreiro
Rico is a cattle ranch in the central plateau at the juncture
of the Rios Piracicaba and Tiete, in the municipalities of
Anhembi and Santa Maria da Serra. Altitude ranges from
450 to 586 m above sea level. Milton and de Lucca (1984)
described five fragments of semideciduous forest there, cov-
ering 3,259 ha, and surrounded by pasture and agriculture.
Today the forest is reduced to three fragments totalling


Figure 2. Aerial view of Parque Estadual Carlos Botelho (37,644
ha), part of the "The Southeast Reserves of Atlantic Forest"
UNESCO World Heritage Site, the largest and most extensive
single tract of Atlantic forest in Brazil (UNESCO, 1999).


2,325 ha. Muriqui research started at this location with
the work of Torres de Assumpcao in 1979-1980 (Torres
de Assumpcao et al. 1982, Torres de Assumpcao 1983a,
1983b) followed by Milton from 1980 to 1989 (see refer-
ences) and, after a hiatus, Martins who investigated popu-
lation parameters of the primates there (Martins, 2005a),
along with feeding strategies and seed dispersal by Alouatta
guariba and B. arachnoides (Martins, 2003a, 2003b, 2005b,
2006). The future of this important area is undetermined,
as logging continues and the ranch-owners are unwilling to
discuss its future in terms of conservation research. Access
is currently restricted even to conservationists.

Region of Sdo Francisco Xavier (FF, ST, Dis) (2312'S,
4552'W)
In the east of Sao Paulo, municipality of Sao Jos6 dos
Campos, in the Rio Paraiba valley, near the state boundary
with Rio de Janeiro, this is a region of steep forested hills of
the Atlantic escarpment of the Serra da Mantiqueira. Alti-
tudes range from 800 to 2,000 m. Antonietto and Mendes
(1994) reported the presence of muriquis in this region, es-
timating a population of at least 15 animals. The Instituto
de Pesquisas Ecol6gicas (IPE), initiated a research program
there (1997-2001), resulting in a study by Silva (1999) on
their habitat and population structure. Silva (1999) esti-
mated 70-90 individuals. At the present time, a program
is underway, with the participation of local communities,
universities and private foundations, to promote increased
awareness and continued research activities in the region,
with an overall focus on muriquis as the flagship species
(Vale Verde Associacao do Meio Ambiente, 2006).

Fazenda Sdo Sebastido do Ribeirdo Grande (FF, ST, On)
(2245'S, 4528'W)
This is a private reserve in eastern Sao Paulo, municipality
of Pindamonhangaba, in the Rio Paraiba valley, near the
state boundary with Minas Gerais, and neighboring the
Campos de Jordno State Park in the Serra da Mantiqueira.
It is administered by VCP Florestal. Oliveira and Manzatti
(1995) reported on the presence of at least 22 muriquis
there, and a research program began in early 2006. The
initial aims were to establish the size of the population of
southern muriquis there and to habituate them. Currently,
the minimum number of southern muriquis there is 32.

Intervales State Park (CF, LT, Dis) (2412'-2425'S,
4803'-4813'W)
Created in 1995, the Intervales State Park (49,000 ha)
is narrowly connected to the Carlos Botelho State Park
(Figs. 1 and 3). It is administered by the Fundagao Flore-
stal of Sao Paulo State (http://www.fflorestal.sp.gov.br).
This area has hosted southern muriqui research for about a
decade through the work of Petroni (1993, 2000). In addi-
tion to the seasonal data on habitat use, muriqui research
in Intervales has provided the most thorough and detailed
study of the vegetation composition and structure of their
habitat for these continuous forests. Intervales has the high-
est diversity of plant species recorded for the Atlantic forest





Neotropical Primates 13(Suppl.), December 2005


Fazenda Barreiro Rico
Torres (1979-1980)
S. Milton (1982-1989)
Martins (2001-2003)



*Ribeirlo Grande Reserve
-" Oliveira& Manzatti, 1996
S- 7'. .. Talebi, 2006 -present


0 1 1 in Francisco Xavier
..-. .., Silva (1997-2001)
Intervales State Park
Petroni (1990-1999) MI AeOrIMl AlMnt For e
Itrmnd of Abt Foret


Carlos Botelho tate Park
Talebi (1993-present)
Carvalho (1990-1993)
Moraes (1988-1990)
Pacagnella (1985-1986)

Figure 3. Field sites for research on the southern muriqui in the state of Sao Paulo. Solid arrows represent ongoing studies.


in Sao Paulo: 55 families, 114 genera and 190 species, with
a predominance of Myrtaceae, Lauraceae, and Legumi-
nosae (Petroni, 2000).

Carlos Botelho State Park (CF, LT, On) (2415'-2444'S,
4746'-4810'W)
The Carlos Botelho State Park (37,644 ha) was created in
1982 in the municipalities of Sao Miguel Arcanjo, Sete
Barras, Capno Bonito and Tapirai, and, like Intervales is
administered by the Instituto Florestal of Sao Paulo (http://
www.iflorestal.sp.gov.br/). The mountains and steep val-
leys are covered by dense montane forests; altitudes range
from 500 to 1,000 m above sea level (Cust6dio-Filho et al.,
1992; Talebi, 1996). Capuchin monkeys (Cebus nigritus)
and howler monkeys (Alouatta guariba) also occur there
(Talebi, 2005). For additional information on this field
site and the muriqui groups under study, see Pacagnella
(1991), Moraes (1992a, 1992b), Talebi (1996), Carvalho
et al. (2004), and Talebi et al. (2005).

Research on the Southern Muriqui at the Carlos
Botelho State Park

Strier (1999) set up the long-term project on the ecology
and behavior of the muriquis at the Carlos Botelho State
Park in 1986 with the proposition of obtaining compara-
tive data for her findings at the Caratinga Biological Sta-
tion, as well as promoting the development and training of
Brazilian conservationists. A number of researchers worked


at Carlos Botelho from that time (see Talebi, 1996; and
Fig. 3). By 1996, two groups had been fully habituated,
and three years later an NGO, the Associacao Pr6-Muriqui,
was founded to provide for the continuity of the research
on the muriqui and its habitats in the park, as well in
other locations in the Southeast Reserves of Atlantic Forest
World Heritage Site. The last 18 years of research at this
site have resulted in the habituation of four muriqui groups
in all, with 15 individuals now identified and named. An
extensive trail system of 210 km has been established and
mapped. The box presents a brief summary of southern
muriqui research at the Carlos Botelho State Park.

Of concern is that, although research has been carried out
at other sites in the past (Fig. 3), the systematic study in the
Carlos Botelho State Park is the only one still active, apart
from one that concentrates on environmental education in
the private reserve at the Fazenda Sao Sebastiao do Ribeirao
(Fig. 3). Our field team receives frequent requests to help
farm owners and researchers interested in developing the
logistics needed for starting muriqui research in other sites.
As a result, over the last four years the Associacao Pr6-
Muriqui has established a volunteer field-training program
for young conservationists and newly-graduated students.
More than 30 Brazilian and international students have
participated, for periods ranging from two to six months.

Additional activities with southern muriquis in Sao Paulo
include a three-year survey (in progress) of remnant





Neotropical Primates 13(Suppl.), December 2005


Research on the southern muriqui at the
Carlos Botelho State Park (PECB), S&o Paulo
(see Talebi [1996] for further details).

1985 Sandra G. Paccagnella carried out the first
population survey of the muriquis at the PECB
(Paccagnella, 1991).

1986 Karen B. Strier began a research program at
PECB to compare northern and southern muriquis,
their behavior and ecology in fragmented and large
forests, and the possibledifferences related to forest
habitats in different stages of succession.

1996 Mauricio Talebi took over the field research
at PECB (had been field-coordinator since 1993).

2000 The Associacao Pr6-Muriqui was created
to ensure the maintenance and growth of research
activities at PECB. The NGO counts on the partici-
pation of scientists, and students, working within
the administrative structure of the Carlos Botelho
State Park and the Forestry Institute of the state of
Sao Paulo.

2002 onwards Internship program was initiated
and logistical/research capacity within the Associ-
agao Pr6-Muriqui was increased. To date we have
had about 30 national and international students
complete the field internship program (minimum
six months), with a number staying on to continue
work in the project.

2005 A survey of southern muriquis in the park
was begun. Although still underway, initial findings
indicate that there are fewer muriquis than had been
estimated by Pacagnella in 1985 (1991).

2006 One more group of muriquis was fully ha-
bituated for systematic observations.


southern populations. The survey was begun in 2005,
and is investigating the most important areas in the state
where muriquis are expected to occur. The Associadao
Pr6-Muriqui is working to carry out long-term monitor-
ing along an altitudinal gradient from southern to north-
ern Sao Paulo, to update their geographical distribution
and understand better their conservation status. To date,
we have set up three field sites in different habitats so as
to provide comparative data on demography, feeding ecol-
ogy, reproduction, health, and behavioral plasticity. Target
populations have been identified, and preliminary arrange-
ments for long-term fieldwork have already been made at
a location in the Serra do Mar (Parque das Neblinas, Insti-
tuto Ecofuturo). Systematic field work has been underway
since 2006 in the Serra da Mantiqueira, at the Fazenda Sao
Sebastiao Ribeirao Grande (VCP Florestal), and there exists


an agreement with VCP Florestal for a long-term study of
muriquis there.

The Associacao Pr6-Muriqui has established links with gov-
ernmental and non-governmental agencies in both Brazil
and abroad in order to expand the operational logistical
basis at the field site in Carlos Botelho. A Muriqui Conser-
vation Research Plan for Sao Paulo State has been designed
and proposed within the Action Plan of Muriqui Conser-
vation endorsed by the International Committee for the
Conservation and Management of the Atlantic Forest
Atelids of the Brazilian Institute for the Environment
(IBAMA). Initial discussions are in progress for designing
a Muriqui Management Plan for Sao Paulo, to optimize
the use of the academic, logistical, and financial resources
available in the state.

Acknowledgments

We thank the Sao Paulo State Forestry Institute for per-
mission to work in the Carlos Botelho State Park (Proc-
ess SMA 41513/99). Financial support has been provided
by the Brazilian National Research Council (Conselho Na-
cional de Desenvolvimento Cientifico e Tecnoldgico- CNPq)
(Process 20025699-8), the Margot Marsh Biodiversity
Foundation, the Primate Action Fund of Conservation
International, WWF Brazil- Support for Postgraduate
Studies, the Metroparks Zoo-Cleveland, Idea Wild, USA,
the Center for Applied Biodiversity Science of Conserva-
tion International with support of the Gordon and Betty
Moore Foundation, Fundagao Biodiversitas, and the VCP
Florestal Environment Research Department. We are most
grateful for the support given to us byJ. L. C. Maia (Forest-
ry Institute), Pedro Scares and Raone Mendes (Pr6-Muriq-
ui Association), R. C. Coles (University of Cambridge,
UK), P. W. Lucas (George Washington University, USA),
P. C. Lee (Stirling University, Scotland, UK), and S. Roy
Choudhury (The Graded School, Brazil).

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the Primates of Southeastern Brazil, with a Reappraisal of
Cebus apella Races. PhD thesis, University of Edinburgh,
Edinburgh.
Torres de Assumpcao, C. 1983b. Ecological and behavio-
ral information on Brachyteles arachnoides. Primates 24:
584-593.
UNESCO 1999. Convention Concerning the Protection of
the World Cultural and Natural Heritage. World Herit-
age Committee, United Nations Educational, Scientific
and Cultural Organization (UNESCO), Marrakech,
Morocco.
Vale Verde Associacao do Meio Ambiente. 2006. Website:
.








Neotropical Primates 13(Suppl.), December 2005


THE SOUTHERN MURIQUI, BRACHYTELESARACHNOIDES: ECOLOGY OF A POPULATION
IN A SEMIDECIDUOUS FOREST FRAGMENT

Milene M. Martins

Laborat6rio de Biodiversidade Molecular e Cir..> nlric *. Departamento de Gen&tica e Evolucao, CCBS, Universidade Fed-
eral de Sao Carlos (UFSCar), Sao Carlos, SP, e-mail:


Abstract

Southern muriquis (Brachyteles arachnoides) inhabit evergreen and semideciduous forest fragments in southeastern Brazil.
Contrary to the broadleaf evergreen forests, the seasonal mesophytic forests experience a relatively severe dry season, which
affects the muriquis' diet. Through behavioral sampling of feeding activity, I determined the diet of a group of muriquis
in a semideciduous forest fragment. Leaves represented 55.3% of feeding records, flowers 16.1%, fruits 12.1%, and seeds
16.5%. Muriquis included 47 plant species in their diet. Leaf consumption was significantly higher in the dry season, but
there was no evident difference between seasons in their feeding on either flowers, fruits, or seeds. Muriquis in this study
shared only 11 taxa with groups in evergreen forests. The study group made consistent use of immature seeds. Dietary flex-
ibility and the consumption of alternative resources may likely be advantageous where there are repeated lean periods and
anthropogenic interference.

Key Words southern muriqui, Brachyteles arachnoides, feeding ecology, Sao Paulo, Atlantic forest, Brazil


Introduction

The original range of the southern muriqui (Brachyteles
arachnoides) extended through two forest types in the At-
lantic forest: the broadleaf evergreen forests on the eastern
slopes of the Serra do Mar in the states of Rio de Janeiro
and Sao Paulo, and the mesophytic, semideciduous forests
on the central plateau, in the interior of the states of Sao
Paulo and Parana. These seasonal forests were largely dev-
astated because the flat terrain favored the development of
farming and cattle-ranching. The ongoing process of habi-
tat fragmentation drastically reduced the populations of
southern muriquis, that now survive in only a few forest
fragments.

The pattern of rainfall determines differences in the flora
and climate of the two types of Atlantic forest. In the ev-
ergreen forests, annual rainfall is quite evenly distributed
through the year, but in the semideciduous forests there is
a relatively severe drought during part of the year (Morel-
lato and Haddad, 2000). The occurrence of two distinct
seasons leads to changes in food availability for the forest's
folivores. As such, it is possible to suppose that muriquis in
semideciduous forests face greater restrictions in relation to
the availability of fleshy fruits, most especially at times of
reduced rainfall, when fewer trees are fruiting. By contrast,
the diet of muriquis in evergreen forests remains relatively
unchanged through the year (Carvalho et al., 2004). In her
long-term study of southern muriquis in a semideciduous
forest fragment, Milton (1984a) found a high proportion
of leaves in their diet, which also included flowers, and


fleshy and dry fruits. However, Milton did not investigate
whether the muriquis' diet changed between seasons.

The aim of this study was to determine the dietary com-
position of a group of B. arachnoides in a semideciduous
forest fragment, examining particularly differences in food
preference compared to groups in more humid forests, and
the feeding strategies adopted during the dry season. The
study area was in the Fazenda Barreiro Rico, in a forest
fragment adjacent to that where Milton (1984a) carried
out her study.

Methods

Study area
Most of the area of the Fazenda Barreiro Rico (2241'S,
4806'W; 450-586 m above sea level) is now split into
several properties located in Anhembi and Santa Maria da
Serra, in the eastern side of the central plateau of the state of
Sao Paulo. Sandy quartzic soils of low fertility predominate
in the region (Magalhaes, 1999). Although the landscape
is dominated by a mosaic of urban centers, farmland and
pasture, the Fazenda Barreiro Rico maintains fragments of
semideciduous submontane forest: 1,450 ha, 501 ha and
374 ha in size. All these forest fragments have been sub-
jected to selective logging. As a result, they have broken
canopies, clearings, and dense tangles of lianas in some
parts. The predominant climate is mesothermic, with a dry
season from April to September when monthly rainfall is
below 70 mm. Sixty-year mean annual rainfall (1940-1999,
data from a local weather station) is 1,284.5 + 285.5 mm.







Further information on the area can be found in Martins
(2005).

Study group
The study was carried out in the 1,450-ha forest fragment
between June 2001 and May 2002. The muriqui group was
completely habituated to the presence of observers. The lack
of natural marks and unique attributes made it impossible
to precisely identify all of the group members. It was easier
to identify females with dependent infants than the males
of any age category because the size and sex of the infants
allowed me recognize them from one observation session
to the next. The muriquis traveled alone or in subgroups
with a mean size of 3.25 + 1.65 individuals. A group size of
25-30 was estimated by counting the number of adult fe-
males with their young, summed with the largest grouping
of males that I saw (11 at one time) (Martins, 2003).

Data colic, .on
The observation and recording method used was instan-
taneous scan sampling (Altmann, 1974). I scanned the
group every five minutes and registered the behavior of
each individual I could see. The behavior categories I re-
corded were: moving, resting, ingesting food, and inter-
acting socially. The foods were classified as leaves, flowers,
fruits and seeds. Although separating fruits from seeds is
not usual in studies of muriqui feeding ecology, I had to
include it as a category due to the frequency with which I
saw them eating the seeds of dry (non-succulent) fruits. As
such, when I saw them eating fruits I noted especially the
treatment they gave to the seeds, which I classified in one
of three categories: seeds ingested (passive), seeds discarded,
or seeds eaten (predated). When I saw them ingesting seeds
passively while eating the entire fruit or parts of it, or dis-
carding the seeds, I scored the individual as eating fruit,
but when the muriqui was evidently targeting the seeds,
chewing on them, I scored seed predation. I collected fecal
samples from the adults to check whether the seeds were
intact or chewed up and fragmented. The plants used in
the muriqui's diet were marked, and herbarium samples
were collected subsequently for identification. The muri-
quis were accompanied for three to four days each month,
totaling 534 hours of observation, including 38 complete
days. I made 5,984 scans which resulted in 2,532 feeding
records.

Statistical analysis
The time spent eating different food items and species was
calculated as a proportion of the total feeding records for
each of the complete days of observation in each month, and
expressed as monthly means (number of days varying from
three to four). Proportions of different food items and spe-
cies were also calculated as a proportion of the overall total
feeding records. The seasons were determined according to
the mean monthly rainfall for the area. Months when pre-
cipitation was below 100 mm were classified as dry season
months (June to September 2001 and April to May 2002).
Months with rainfall above 100 mm were considered to be


Neotropical Primates 13(Suppl.), December 2005

rainy season months (October to December 2001 and Jan-
uary to March 2002). Seasonal differences in the amount
of time spent eating leaves, flowers, fruits and seeds each
day were tested with ANOVA. Homogeneity among vari-
ances was examined using the Levene test, the proportions
being transformed to the arcsine of the square root when
the variances were not homogeneous. I used the program
STATISTICA 5.0 to carry out the test. Significance levels
were pre-assigned to 0.05.

Results

Leaves took up 55.3% of the feeding records of the group,
flowers 16.1%, fruits 12.1% and seeds 16.5%. The muri-
quis included 47 species of plants in their diet during the
study (Table 1). Records for five of the species were inci-
dental (seen outside of the formal observation sessions, or
recorded through the presence of seeds in the fecal samples).
Intact seeds of 18 species of plants were found in 117 fecal
samples. Of the total of 31 food species recorded during
observation sessions, Aspidosperma polyneuron (Apocynace-
ae) was most frequently registered, followed by Duguetia
lanceolata (Annonaceae), Hymenaea courbaril (Caesalpi-
noideae) and Esenbeckia leiocarpa (Rutaceae) (Table 1).
Aspidosperma polyneuron and H. courbaril supplied mainly
leaves, while D. lanceolata and E. leiocarpa were important
sources of immature seeds.

The consumption of leaves differed significantly between
the seasons, but this was not so for flowers, fruits or seeds.
The muriquis spent more time eating leaves in the dry
season than in the wet (F = 7.33; p = 0.01). Variation in
the daily contribution of flowers (F = 0.31; p = 0.57), fruits
(F = 1.11; p = 0.29) and seeds (F = 3.12; p = 0.08) was
higher between the months of each season than between
seasons (Fig. 1). The muriquis made use of temporarily
available resources. For example, flowers and nectar were
eaten when Mabea fistulifera (Euphorbiaceae) was flower-
ing in April (Fig. 1). Only four succulent fruits were in-
cluded in the diet for the four months of the dry season; the
liana Pereskia aculeata (Cactaceae), which fruited in June
and July, was eaten most. Immature seeds were eaten in
all months except October. There was an increase in seed
consumption between January and March (Fig. 1) when
E. leiocarpa was fruiting.

Discussion

The diet of the muriquis in this study showed some con-
siderable differences to those recorded for groups in more
humid forests. Of the 47 species of plants the muriquis
ate, only 11 were also recorded in the studies of muriquis
in the montane evergreen forests of the Carlos Botelho
and Intervales state parks (Table 1). Ten of the species,
members of the families Apocynaceae, Euphorbiaceae
and Rutaceae, were eaten only by the muriquis at Bar-
reiro Rico. In terms of their relative frequency, these three
families are well represented in the area (Cesar and Leitao-





Neotropical Primates 13(Suppl.), December 2005


Table 1. Percentage of feeding records on each species (N = 2,532) by Brachyteles arachnoides in the Fazenda Barreiro Rico, and coin-
cidence with records from two other study sites-Carlos Botelho State Park (PECB) and Intervales State Park (PEI), both of dense
evergreen forest.
Species Family Percentage of records PECB1 PEI2
Arrabidea sp. Bignoniaceae 1.72
Aspidosperma nemorale Apocynaceae 2.47
Aspidosperma polyneuron Apocynaceae 12.47
Astronium graveolens Anacardiaceae 0.07
Campomanesia sp. Myrtaceae 0.11
Cariniana estrellensis Lecythidaceae 0.51 x
Celtis spinosa Ulmaceae 0.71
Copaifera Caesalpinoideae 0.51 x
Cordia sellowiana Boraginaceae 0.19 x
Croton floribundus Euphorbiaceae 2.63
Cryptocaria moschata Lauraceae IO x x
Diclidanthera sp. Polygalaceae 1.81
Dolichandra unguis-cati Bignoniaceae 1.42
Duguetia lanceolata Annonaceae 6.5 x
Esenbeckia leiocarpa Rutaceae 5.84
Eugenia ligustrina Myrtaceae 2.48
Eugenia pyriformis Myrtaceae 0.77
Eugenia sp. Myrtaceae 0.27 x x
Ficus sp. Moraceae SF x x
Fridericia samydoides Bignoniaceae 0.11
Gonatogyne brasiliensis Euphorbiaceae 0.19
Hymenaea courbaril Caesalpinoideae 6.15 x
Inga striata Mimosoideae 0.74
Jacaratia spinosa Caricaceae 0.46
Lundia obliqua Bignoniaceae 0.15
Mabea fistulifera Euphorbiaceae 1.3
Metrodorea nigra Rutaceae 0.7
Mouriri glaziowiana Melastomataceae SF
Myrciaria sp.a Myrtaceae
Neomithrantes obscura Myrtaceae 0.55
Ocotea catharinensis Lauraceae 0.27 x
Ocotea corymbosa Lauraceae 0.81 x
Ocotea velutina Lauraceae 1.42
Pachystroma ilicifolium Euphorbiaceae 0.23
Pereskia aculeata Cactaceae 4.62
Pithecoctenium sp. Bignoniaceae 0.55
Philoadendron sp. Araceae 0.42 x
Psidium sp. Myrtaceae SF
Qualeajundiahy Vochysiaceae 4.69
Rudgea sp. Rubiaceae 1.45
Savia dictyocarpa Euphorbiaceae 2.84
Sloanea monosperma Elaeocarpaceae 0.07
Styzophyllum riparium Bignoniaceae 0.98
Syagrus Arecaceae SF
Tanaecium seloi Bignoniaceae 0.98
Xylopia brasiliensis Annonaceae 4.54
Zanthoxylum rhoifolium Rutaceae 0.19

- Recorded by Milton only (1984a). PECB Carlos Botelho State Park, PEI Intervales State Park. References: 'Moraes (1992), Carvalho etal. (2004),
Talebi etal. (2005); 2Vieira and Izar (1999), Petroni (2000). 10 Incidental observation; SF seeds in a fecal sample.








100-

75 O Leaves
o Flowers
50 m Fnuits
Seeds
25 -

0 . .. .
J J A S O N D J F M A M

Figure 1. Monthly percentages of feeding records for four food
items (leaves, flowers, fruits, and seeds) for Brachyteles arachnoides
between June 2001 and May 2002 in the Fazenda Barreiro Rico,
Sao Paulo.


Filho, 1990). The floristic composition of broadleaf ev-
ergreen and semideciduous forests in southeastern Brazil
are distinct (Oliveira-Filho and Fontes, 2000), explaining
the low overlap of food species between Barreiro Rico on
the one hand and the Carlos Botelho and Intervales state
parks on the other.

The consumption of immature seeds was seen frequently,
and yet this food resource would appear to be rare or even
absent from the diets of the muriquis in the broadleaf ev-
ergreen forests to the south (Moraes, 1992; Carvalho etal.,
2004; Talebi et al., 2005). Milton (1984a) also recorded
seed predation in the group she studied in the neighbor-
ing forest patch in Barreiro Rico. Milton (1984a) did not
record the frequency of this behavior, however, which
may indicate that it was less frequent. There are differ-
ences (to be expected) in the diets we recorded. For ex-
ample, leaves of Xylopia brasiliensis accounted for 11% of
the diet of Milton's (1984a) group, but only 4.5% of the
records for the group I studied. Seeds ingested by primates
contain non-structural carbohydrates and lipids (Maisels
et al., 1994; Norconk, 1996; Heiduck, 1997), but also
nitrogen (Ayres, 1986). However, what it is that is at-
tracting the Barreiro Rico muriquis to eat seeds is unclear.
Acquisition of special skills to fracture or scrape the hard
pericarps of, for example, E. leiocarpa, D. lanceolata, and
P. ilicifolium, and the metabolic attributes to deal with the
secondary compounds are interesting questions for further
investigation.

The annual proportion of leaves in the diet recorded by
Milton (1984a) for her study group and that which I found
in my study group were similar (both more than 50%), and
much higher than that recorded by Carvalho et al. (2004)
(33%) and Talebi et al. (2005) (24%). The group at Bar-
reiro Rico lives in a forest which, for a fragment, is quite
large (1,450 ha), and it is relatively well conserved, despite
the occasional logging. I would believe that the higher con-
sumption of seeds and leaves may well be typical of muri-
quis occupying the more seasonal, semideciduous forests
of the central plateau when compared to those in the less


Neotropical Primates 13(Suppl.), December 2005

seasonal montane evergreen forests of the Serra da Parana-
piacaba, for example. The behavioral strategy of Brachyteles
is considered to be one of efficiency in exploiting dispersed
and isolated patches of food resources such as fruits (Rosen-
berger and Strier, 1989), but the consumption of leaves,
distributed more homogeneously, is still significant in the
larger expanses of forest such as that at the Carlos Botelho
State Park. Cecal fermentation (Milton, 1984b) and broad
post-canine teeth (Rosenberger and Strier, 1989) allow
these primates to process these low energy foods. Talebi
et al. (2005) suggested an association between the higher
contribution of leaves in the diet and the fact that animals
are living in forest fragments. However, independent of
and prior to any fragmentation, the muriquis would be se-
lected to adapt to the lower diversity of zoochoric fruits and
the greater seasonality in fruit availability that character-
izes these semideciduous forests. A comparison of groups
in fragmented and extensive semideciduous forests would
be ideal, but unfortunately none of the latter remain in the
range of the southern muriquis.

Muriquis at Barreiro Rico eat more leaves in the dry
season, but although very variable between months, eat
similar proportions of the other plant foods across sea-
sons. The adaptive abilities of the muriqui are demon-
strated by their increased consumption of leaves when
succulent fruits are scarce. This pattern is not evident for
the groups in the broadleaf evergreen forest, probably be-
cause of the larger number of species producing succulent
fruits and a more uniform fruit abundance over the year.
At Carlos Botelho, Carvalho et al. (2004) failed to detect
any significant differences in the composition of the diet
during the year.

The results suggest a greater variability in the diet of Brach-
yteles arachnoides than had been previously recognized.
I have identified differences in the diet of the group in Bar-
reiro Rico from those recorded for the groups in humid
broadleaf forests, not only in the plant species eaten, but
in the regular and considerable contribution of immature
seeds. The predator-plant interaction deserves further re-
search considering its effects on the recruitment of the
plant species involved, and the influence of Brachyteles as
a seed predator on the floristic communities of the forests
where they live. Reliance on seeds and dietary flexibil-
ity were probably crucial aspects enhancing the southern
muriqui's capacity to occupy seasonal semideciduous for-
ests. This plasticity may well be allowing them to adapt to
structural and floristic changes in the forests over recent
decades. For example, the muriquis may well have devel-
oped or increased their capacity to eat ruderal invasives
such as Croton floribundus (Euphorbiaceae) and Inga striata
(Mimosoideae) or species which respond positively to frag-
mentation and disturbance such as lianas. It is possible that
these feeding strategies provide an advantage for muriquis
to tolerate not only repeated dry season conditions, but
also anthropogenic effects over the remaining forests where
they live.





Neotropical Primates 13(Suppl.), December 2005

Acknowledgments

I am grateful to the Sao Paulo State Research Support Foun-
dation (Fundafdo de Amparo d Pesquisa do Estado de Sdo
Paulo FAPESP) for a research grant (99/06217-2) for this
study. Financial support was also provided by Conservation
International's Primate Action Fund, and Primate Con-
servation, Inc. I also thank Karin Barbarella, Jos6 Baitello,
Osny Aguiar, and Ldcia Lohmann for identifying the plant
species. Joao C. Lourengo and his family, owners of the Fa-
zenda Sao Francisco do Tiete, provided friendship and lo-
gistic support. Jos6 C. Oliveira helped in the data collection.
I am most grateful to Jean Boubli and Anthony Rylands for
their suggestions on a previous version of this article.

References

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Ayres, J. M. 1986. The White Uakaris and the Amazonian
Flooded Forests. Doctoral thesis, University of Cam-
bridge, Cambridge, UK.
Carvalho Jr. 0., Ferrari, S. F and Strier, K. B. 2004. Diet
of a muriqui group (Brachyteles arachnoides) in continu-
ous primary forest. Primates 45: 201-204.
Cesar, 0. and Leitao-Filho, H. E 1990. Estudo fitossocio-
16gico de mata mes6fila semidecidua na Fazenda Barreiro
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443-452.
Heiduck, S. 1997. Food choice in masked titi monkeys
(Callicebus personatus melanochir): Selectivity or oppor-
tunism? Int. J Primatol. 18(4): 487-502.
Magalhaes, J. C. R. 1999. As Aves na Fazenda Barreiro Rico.
Editora Pleiade, Sao Paulo. 215pp.
Maisels, F, Gautier-Hion, A. and Gautier, J. P. 1994. Diets
of two sympatric colobines in Zaire: More evidence on
seed-eating in forests on poor soils. Int. J. Primatol. 15(5):
681-701.
Martins, M. M. 2003. Estrategias Alimentares e Dispersao
de Sementes por Alouatta guariba e Brachyteles arachnoi-
des em um Fragmento de Floresta Semidecidua. Docto-
ral thesis, Instituto de Biociencias, Universidade de Sao
Paulo, Sao Paulo.
Martins, M. M. 2005. Density of primates in four semi-
deciduous forest fragments of Sao Paulo, Brazil. Biodiv.
Conserv. 14: 2321-2329.
Milton, K. 1984a. Habitat, diet, and activity patterns
of free-ranging woolly spider monkeys (Brachyteles
arachnoides E. Geoffroy, 1806). Int. J Primatol. 5(5):
491-513.
Milton, K. 1984b. The role of food-processing factors in
primate food choice. In: Adaptations for Foraging in Non-
human Primates. P. S. Rodman and J. G. H. Cant (eds.),
pp.249-279. Columbia University Press, New York.
Moraes, P. L. R. 1992. Especies utilizadas na alimentagao
do mono-carvoeiro (Brachyteles arachnoides E. Geoffroy,
1806) no Parque Estadual de Carlos Botelho.Anais Congr.
Nac. Essencias Nativas, IF, Sao Paulo, 1206-1208.


Morellato, L. P. C. and Haddad, C. E B. 2000. Introduc-
tion: The Brazilian Atlantic Forest. Biotropica 32(4b):
786-792.
Norconk, M. 1996. Seasonal variation in the diets of white-
faced and bearded sakis (Pithecia pithecia and Chiropotes
satanas) in Guri lake, Venezuela. In: Adaptive Radiations
of .'.J....- ... 'Primates, M. A. Norconk, A. L. Rosenberg-
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Oliveira-Filho, A. T. and Fontes, M. A. L. 2000. Patterns of
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Neotropical Primates 13(Suppl.), December 2005


THE SOUTHERN MURIQUI, BRACHYTELESARACHNOIDES, IN THE STATE OF PARANA:
CURRENT DISTRIBUTION, ECOLOGY, AND THE BASIS FOR A CONSERVATION STRATEGY

Alexandre B. Koehler1, Luiz Cesar M. Pereira2, Patricia A. Nicola3, Alessandro C. Angelo' and
Karla S. Weber'


1Pontificia Universidade Cat61lica do Parand, e-mail:
2Universidade Federal do Vale do Sao Francisco, e-mail:
3Pontificia Universidade Cat61lica do Parand, e-mail:
4Universidade Federal do Parand, e-mails: ;


Abstract

Primatologists have suspected the existence of remnant populations of the southern muriqui, Brachyteles arachnoides
(E. Geoffroy, 1806), in the state of Parand since the early 1970s. Only in 2002, however, was this confirmed, with the
discovery of a group in the upper Rio Ribeira valley. Here we report on some observations of this group, which totals
23 individuals living in a tiny remnant of the primary dense broadleaf forest that formerly extended in a continuous belt
into Parani's first planalto along the valleys of the rios Ribeira and Agungui. We also discuss possibilities for the occurrence
of muriquis elsewhere, and our ongoing efforts for the conservation of this threatened species in the state of Parand.

Key Words southern muriqui, Brachyteles arachnoides, Atlantic forest, conservation, state of Parand, Brazil


Introduction


The possibility of the continued presence of the southern
muriqui, Brachyteles arachnoides (E. Geoffroy, 1806), in the
state of Parani was reported by Aguirre (1971). He believed
that they might still occur in the region of Guaraquegaba,
because there could be found the largest expanses of well-
conserved forest in the state. This idea was subsequently
reinforced by Lange and Jablonski (1986) and confirmed
by Martuscelli et al. (1994).

Koehler et al. (2002) reported on a new locality for the
occurrence of B. arachnoides in the municipality of Castro,
Parand; a region with very few remaining patches of intact
forest. This unexpected discovery gave rise to renewed re-
search and conservation measures for the protection of the
southern muriqui in the state of Parand. It established a
new southern limit to the present-day range of the spe-
cies and drew the attention of primatologists and conser-
vationists to the middle valley of the Rio Ribeira where it
had been found. Besides initiating research on the group
discovered by Koehler et al. (2002), efforts were made to
find other groups surviving in the area, and two more were
discovered. Here we summarize our research and findings
since the discovery of the first group, and provide some
suggestions for a conservation strategy for a region that un-
fortunately has a long history of environmental abuse.


Current range of Brachyteles arachnoides in the
State of ParanA

According to Aguirre (1971), Brachyteles arachnoides was to
be found in climax montane forests at altitudes of 600 to
1,800 m above sea level, in well-preserved remnants of sea-
sonal and evergreen forests in the states of Bahia, Espirito
Santo, Sao Paulo, Minas Gerais and Rio de Janeiro. Based
on a reference of Krieg, cited by Hill (1962, pp.252-356),
Aguirre (1971) considered the southern limit of the range of
the species to be about 25S, in the region of the Rio Ribeira
in Parand. He concluded that the distribution center of the
species was the Serra do Paranapiacaba in Sao Paulo, well
known for its richness of plants in the Lauraceae family.
The Serra do Paranapiacaba today has the largest remain-
ing southern populations of Brachyteles in a continuous
stretch of forest covering some 100,000 ha, including the
Intervales and Carlos Botelho state parks, Xitud Ecological
Station and the Alto Ribeira State Tourism Park, together
now known as the "Paranapiacaba Ecological Continuum"
(Talebi and Scares, 2005).

The integrity of the "continuum" in the state of Parand was
broken several decades ago. Wachowicz (2002) recorded
that the valley of the Rio Ribeira, the headwater springs of
which are on Parani's Second Planalto, draining into the
Atlantic on the coast of Sao Paulo, was one of the principal
routes for miners and prospectors entering the Planalto in
the middle of 17th century.

Maack (1950) mapped the vegetation of the state and clas-
sified the forests in the Rio Ribeira valley as secondary along







the initial one-third and middle sections of the river. The
section known as the Rio Ribeirinha and, to the east, the
section in the Serra do Paranapiacaba, known regionally as
the Serra da Canha, are within the domain of tropical and
subtropical coastal rain forests. The primary forests have
been gradually destroyed, the only fragments remaining
being in the remotest and most inaccessible areas.

According to Roderjan et al. (2002), the dense evergreen
forest (Floresta Ombrofila Densa) extends into the Parandi
planalto, a region otherwise characterized as "Campos
Gerais" (grasslands), accompanying the courses of the rios
Ribeira and Agungui, and being increasingly delimited by
the Araucaria pine forest at altitudes of 700 m above sea
level. This penetration of the Atlantic forest, following the
courses of the principal rivers of the region, and invading,
so to speak, the open vegetation of the Planalto, is referred
to in Brazil as an Area of Ecological Tension (Area de Tensao
Ecoldgica). This floristic mixture continues until it reaches
elevations where Araucaria begins to appear and eventu-
ally predominate; a characteristic of mixed evergreen forest
(Floresta Ombrofila Mista) (see Fig. 1).

The muriqui group found in the Fazenda LagoaAlegre, mu-
nicipality of Castro, Parand (Koehler et al., 2002) was in a
tiny remnant of dense evergreen forest, within the domain
of the mixed forest along the courses of the rios Ribeira
and Agungui. The other two groups discovered later (L. M.
Pereira et al., unpublished) were in similar vegetation on
the banks of the Rio Turvo (Fig. 1).

Martuscelli et al. (1994) informed of two localities where
they found muriquis in Parand. One was in the mu-
nicipality of Jaguariaiva, the other in the Guaraquegaba
Environmental Protection Area (APA), near to 25S, and
corroborating the southern limit of Aguirre (1971). Ac-
cording to the coordinates provided by the authors, the
first locality is in the municipality of Seng6s, on the banks
of the Rio Jaguaricatu, and the second is in the south of
the state of Sao Paulo. The mixed forest types we have de-
scribed as being typical of the valleys of the Rios Ribeira,
Agungui and Turvo disappear at this point, and the species
which occur with Araucaria, and Araucaria itself, are lost
in the dense evergreen forest typical of the coastal Atlantic
forest, even at altitudes above 600 m. It is possible that
B. arachnoides could still be found in small remant forests
in the valleys of the rios Jaguaricatu (Martuscelli et al.,
1994) and Itarard to the north, in the region of Jaguari-
aiva and Sengds, where landscapes today are dominated
by extensive pine plantations, estepes (wooded grasslands),
and a small area of open savanna, besides secondary forests
with Araucaria.

The Muriqui Group at the Fazenda Lagoa Alegre

Group size
This group was found by chance, during a forest inven-
tory along power transmission lines. They were first seen


Neotropical Primates 13(Suppl.), December 2005

on 29 June 2002. After three further sightings in the same
area (Fazenda Lagoa Alegre), we were able to count only
eight individuals in the group (Koehler et al., 2002). By the
beginning of our systematic study in March 2003, how-
ever, we had registered 15 individuals, and after intensive
efforts to habituate the muriquis, in September 2003 we
registered 18, due to three dependant infants we had not
seen earlier, two of them still riding dorsally and the third
ventrally. In September the older two would occasionally
leave the mother to explore, and the third could sometimes
be seen on the mother's back. A new count in November
2003, recorded 22 muriquis; three adult females, four adult
males, three subadults, four infants and eight other indi-
viduals we were unable to classify by sex or age. At the end
of 2004, another infant was born, and in April 2005 there
were 23 muriquis in the group.

Home range
We studied the home range of the group from January
2004 to September 2005. The points of observation and
travel paths were plotted using a Geographic Position-
ing System (GPS). The data obtained from 246 hours of
ad libitum observation lead us to conclude that the group
used a core area of 38.14 ha, in four forest fragments of
24.69 ha, 3.44 ha, 5.96 ha, and 4.05 ha. The area covered
by the muriquis was estimated at 128.65 ha. The maxi-
mum travel distance observed was 1,862 m (September
2004; 20.3 hours of observation), and the minimum was
146 m (March 2005; 18.5 hours of observation) (Pereira,
2006).

Milton (1984) and Dias and Strier (2003) concluded that
the home range of muriqui groups varies according to dif-
ferences in forest structure and floristic composition, the
availability and abundance of food, and the presence or
otherwise of other groups. The home range of a group of
23-26 northern muriquis Brachyteles .'... .'.. at the
Caratinga Biological Station, Minas Gerais, increased from
168 ha to 309 ha due simply to an increase in the amount
of habitat available (regeneration at the forest borders)
(Dias and Strier, 2003).

Diet
The muriqui diet is very diverse, including fruits, leaves,
flowers, lianas and epiphytes (Milton, 1984; Nishimu-
ra et al., 1988; Petroni, 2000); the contribution of each
varying according to their availability and the time of
year (Dias and Strier. 2003). We examined the diet of the
muriqui group at the Fazenda Lagoa Alegre by collecting
feces and by direct observation. Between January 2004 and
July 2005 we registered 27 species of plants of 20 families
in their diet, including Myrtaceae, Annonaceae, Aquifo-
liaceae, Rubiaceae, Euphorbiaceae, and, most especially,
Lauraceae (six species). They also eat fruits and leaves of ep-
iphytes, especially cactuses and bromeliads. The most com-
monly eaten items were leaves, fruits and flowers. Once we
saw an individual pulling an orchid off a branch and eating
its bulbs (P. A. Nicola, unpublished data).





Neotropical Primates 13(Suppl.), December 2005 69

Our observations on the diet of the Fazenda Lagoa Alegre nature of the forest arising from the gradual transition to
group indicate that they are using the same plant families mixed evergreen forest [P. A. Nicola, unpublished data]).
and many of the same genera and species recorded in the
diets of muriquis elsewhere, in forests with similar physiog- Habitat quality
nomies, structure, and floristic composition (see, for exam- The forest cover in the home range of the muriquis is
ple, Moraes, 1992) (remembering, however, the ecotonal not uniform. The forests there are reduced to fragments


;,* -. - .,.


p-"" '" --L, . .



+ ,-, -, /- : t--,, ..- .'-'
'+: ,* + ^ V.- |^ ;' 'T




- n,_ .(, / ... ..- .
I--- *^ T^ v L- -
^^'-:'/<^^'^L-.V-
*:- ^ *';*^ '-* ; .-> ^ ^ .* *-.*--


Munlclplos
1- Senges
2 Jaguerialva
3 Doutor Ulisses
4 Cerro Azul
5- Castro
6- Ponta Grossa
7 Campo Largo
8- Itaperu9g
9- Rio Branco do StI
10 Tunas do Parana
'1 -Adrianopolis
12 BocaiOva do Su:
,3 Campina G.do Sul
14 Guaraquegaba





14i


Figure 1. Geographic distribution of Brachyteles arachnoides in the state of Parani.


.
. '. r


,'. fyi
I







surrounded by pasture, tree plantations (Pinus), and crops.
The fragment where the muriquis live, although intact
structurally, shows signs of past logging in some places.
Although only 50 ha, it is one of the best-preserved forests
of the region. Most of the forest in the valley is secondary,
resulting from abandoned farming plots and pasture, with
small patches of degraded primary forest in the valley bot-
toms and steeper slopes, and, rarely, in areas even of easier
access.

The proximity of some of the better-conserved secondary
forest patches to the 50-ha forest of the muriquis allows
them to use them for shelter, passage and food. Alone we
believe they would be inadequate to support muriquis; no-
where in the literature have we been able to find evidence
that muriquis could live in secondary forest only. The ad-
vance in succession and growth of these forests, however,
are no doubt vital for the long-term survival and growth of
the muriqui population there.

The secondary formations differ considerably from the pri-
mary forest, most markedly in the understorey, which is
very dense, and of course in the floristic composition. Bro-
meliads, orchids, epiphytic cacti, and Araceae are all rare.
On the other hand, Araucaria angustifolia is more abun-
dant, with mature trees in the first stratum of the forest.
There are floristic differences in the lower strata too, from
the lower canopy to the understorey. In both the primary
and secondary forests, gaps in the canopy favor the prolif-
eration of native bamboos (taquara) along trails and in tree
falls. The control of these taquaras is key to managing these
forests to favor the dissemination and growth of trees. The
edges of both primary and secondary forests are dominated
by bracken, Pteridium aquilinum, locally called samambaia
das taperas, which is prejudicial to regeneration, complicat-
ing the germination and survival of saplings which could
otherwise gradually advance the forest into the abandoned
fields and pasture. The control of bracken is very difficult,
not only because of the often steep terrain, but also be-
cause it is an aggressive disperser, an invasive species with a
strong regenerative capacity. As such, fire is the means most
used, which is invariably destructive too for all other sap-
lings and seeds that could contribute to the regrowth of the
forest. Fire is also used to clear bracken for pasture, which
is frequently unsuccessful because of the speed with which
bracken recovers and takes over once again.

These aspects restrict the regenerative capacity of the forest
patches. Many areas, farmed in the past and abandoned
could well have returned to forest if it were not for the
farming practices in neighboring areas. Increasingly pre-
dominant in the landscape are pine plantations, Pinus taeda
and Pinus elliottii, which limit the native forests to few trees
left standing and able to coexist. More and more land is
being given over to these pine plantations, so the possibili-
ties of forest regeneration are severely limited or nil. All ex-
isting native forest patches, primary and secondary, must,
therefore, be protected.


Neotropical Primates 13(Suppl.), December 2005

Selective logging in the area also has serious impacts. The
felling of some trees in small primary forest in a farm next to
the Fazenda Lagoa Alegre completely altered the micro-en-
vironment, and after four years the proliferation of bracken
in the understorey is still impeding any natural regenera-
tion. Unfortunately, the landowners are quite unwilling to
mitigate this process, even though it would so obviously be
of advantage for them to facilitate the regeneration of the
forest patches they find so useful as a provider of timber,
especially for fences. The cost they find unjustified. Despite
the patent degradation of these forests, lacking a continu-
ous canopy of any sort, the muriquis are still able to travel
through them, but predictably not for much longer.

The owner of the Fazenda Lagoa Alegre, the laborers and
staff, and some of the neighboring families have support-
ed our research in the region. All agree that the muriquis
should be protected, and they are strong allies in our at-
tempts to do this. There is a local cement company with
a large property in the region that has a forest of 200 ha.
Most is secondary, in the middle to advanced stages of
succession, and allowing this forest to expand, promoting
the establishment of a connection with the Fazenda Lagoa
Alegre forest, would be enormously beneficial to the muri-
quis. Some other property owners have small forest patches
which are accessible to, and used occasionally by, the muri-
quis, but their understanding of how important this is for
the muriquis conflicts with their dependence on these forest
patches as sources of timber and firewood. These marginal
forest patches, potential habitat for muriquis, are gradually
diminishing as a result.

Another important element is the management of the pine
plantations. The plantation companies need to fulfill legal
requirements in terms of the so-called "Legal Reserve"
(protection of a fixed portion of native forest on their land),
and the Areas of Permanent Preservation (areas that must
be left as forest, and natural vegetation along watercourses
and on steep slopes, according to the Forest Code). These
legal instruments could well be brought to bear as a means
of designing a forested landscape, which, with the collabo-
ration of the companies, could be more favorable to muri-
quis (and the accommodation and dispersal of wildlife in
general).

Although the muriquis enter the degraded and secondary
forest patches, moving through them, resting there and
even sometimes feeding, in the majority of our studies we
have been watching them in the primary forest, which is
evidently the habitat vital for their continued existence in
the region.

Future Research and Conservation Strategies

University teaching staff and students of the postgraduate
course in Forestry of the Universidade Federal do Parand
(UFPR), and also the Pontificia Universidade Cat61lica do
Parand, have been carrying out the research on the muriquis





Neotropical Primates 13(Suppl.), December 2005

of the Fazenda Lagoa Alegre. The Department of Zoology
of the UFPR should also be involved, as should the Museu
de Hist6ria Natural do Capao da Imbuia (MHNCI) in Cu-
ritiba. We hope that other universities and research institu-
tions may also be inspired to collaborate, besides the rel-
evant non-governmental conservation organizations. The
future of muriquis in the state of Parand will undoubtedly
depend on their participation. The creation of a protected
area, or areas, is vital, but not a simple prospect considering
the expense and the fragmentation of the remaining forest.
The means would be through, perhaps, a series of Private
Natural Heritage Reserves (RPPNs), combined with insti-
tutional programs for the socio-environmental develop-
ment of the region, working to preserve and connect the
forest patches and improving soil management and farm-
ing practices to promote their regeneration, would the best
plan for the short- to mid-term.

The search for more groups continues, with our expecta-
tions centered on the courses of the rios Agungui, Ribei-
ra, Turvo, Santana and Ponta Grossa and, farther east,
on the rios Grande and Sao Sebastiao; all affluents of the
Rio Ribeira marking the state limits of Parand with Sao
Paulo. Throughout the region, the only remnant forest of
any considerable size is that of the Lauriceas State Park of
23,000 ha, in a montane region of the municipalities of
Adrian6polis and Tunas do Parand. It is quite probable that
muriquis will be found there.

We believe that the establishment of a state committee for
the conservation of the muriqui in Parand and its integra-
tion with the national committee would be an important
step, providing as it would the principal forum for guiding
research on the animal, as well as promoting integration
with other institutions working on the southern muriqui,
most especially in Sao Paulo. The committee would be the
point of contact and articulation among non-governmental
organizations, universities and state and federal govern-
ments, besides dealing directly with landowners concern-
ing the creation of private reserves.

Improved policing for environmental crimes and abuses
and inappropriate land use and management in the Rio
Ribeira valley in Parand is urgent. If current practices do
not change, the tiny remaining forests in any reasonable
state of conservation will be lost, and with them the chanc-
es for survival of the muriqui there. Government meas-
ures to improve the livelihoods, education, and well-being
of the local communities in the region are also urgently
needed. Development in the region has been slow, but the
introduction of activities oriented towards reforestation
and the conservation of the forests there would undoubt-
edly be a viable option. A reforestation project of Bracat-
inga has already begun in the northern Parand section of
the Ribeira valley, an initiative of the Development Agency
for the Middle Ribeira Valley (Agjncia de Desenvolvimento
Mesorregiao Vale do Ribeira), in partnership with the Brazil-
ian Agricultural and Cattle-Breeding Research Company


(Empresa Brasileira de Pesquisa Agropecudria- EMBRAPA)
and the State Company for Technical Assistence and Rural
Extension (Empresa Estadual de Assistincia Tdcnica e Exten-
sao Rural- EMATER), financed by the Ministry of Nation-
al Integration (Ministerio de Integra;ao Nacional), in the
municipilaties of Bocaidva do Sul and Campina Grande
do Sul.

In conclusion, this is the moment to think of the strate-
gic re-establishment of wildlife corridors extending to the
Paranapiacaba Ecological Continuum, using these isolated
forest fragments of the Ribeira valley as stepping stones and
bridges. Diversified agrosilvicultural projects could well be
an excellent solution in the short- to medium term, besides
the implementation of agricultural policies to improve
farming practices, to end the predominant and pernicious
traditional systems, which include itinerant farming (slash-
and-burn) that has for years been degrading the soils and
ruining the landscapes of the region.

Acknowledgment

The authors are most grateful to the Fundagao 0 Boticario
de Protegao a Natureza, Sao Jos6 do Pinhais, Parand, for
financing our research during 2003 and 2004.

References

Aguirre, A. C. 1971. 0 mono Brachyteles arachnoides
(E. C ...o .. Situafao atualda Espicie no Brasil. Academia
Brasileira de Ciencias, Rio de Janeiro. 53pp.
Dias, L. G. and Strier, K. B. 2003. Effects of group size on
ranging patterns in Brachyteles arachnoides .'
Int. J. Primatol. 24(2): 209-221.
Hill, W C. 0. 1962. Primates Comparative Anatomy and
Taxonomy V Cebidae Part B. Edinburgh University Press,
Edinburgh.
Koehler, A., Pereira, L. C. M. and Nicola, P. A. 2002. New
locality for the woolly spider monkey, Brachyteles arach-
noides (E. Geoffroy, 1806) in Parand State, and the ur-
gency of strategies for conservation. Estudos de Biologia
24 (49): 25-29.
Lange, R. B. and Jablonski, E. E 1986. Lista prnvia dos
Mammalia do Estado do Parani. Estudos de Biologia 6:
1-35.
Maack, R. 1950. Mapa F'.-.._... 'F. .., do Estado do Parand.
Map 115 x 80 cm, scale 1:750.000. IBPT-SAIC/INP,
Curitiba.
Martuscelli, P., Petroni, L. and Olmos, E 1994. Fourteen
new localities for the muriqui Brachyteles arachnoides.
Neotrop. Primates 2(2): 12-16.
Milton, K. 1984. Habitat, diet and activity patterns of free-
ranging woolly spider monkeys (Brachyteles arachnoides
E. Geoffroy 1806). Int. J. Primatol. 5: 491-514.
Moraes, P. L. R. 1992. Esp&cies utilizadas na alimentagao
no mono-carvoeiro (Brachyteles arachnoides E. Geoffroy,
1806) no Parque Estadual de Carlos Botelho. Rev. Inst.
Florest. Sao Paulo 4: 1206-1208.





Neotropical Primates 13(Suppl.), December 2005


Nishimura, A., Fonseca, G. A. B., Mittermeier, R. A.,
Young, A. L., Strier, K. B. and Valle, C. M. C. 1988.
The muriqui, genus Brachyteles. In: Ecology and Behavior
of Neotropical Primates, Vol. 2, R. A. Mittermeier, A. B.
Rylands, A. E Coimbra-Filho and G. A. B. da Fonseca
(eds.), pp.577-610. World Wildlife Fund, Washington,
DC.
Pereira, L. C. M. 2006. Area de Vida e Padr6es de Deslo-
camento de Brachyteles arachnoides (E. Geoffroy, 1806)
(Primates: Atelinae) em Um Fragmento Florestal no
Municipio de Castro, Estado do Parand, Brasil. Master's
thesis, Universidade Federal do Parand, Curitiba.
Petroni, L. M. 2000. Caracterizagao da Area de Uso e Dieta
do Mono-Carvoeiro (Brachyteles arachnoides, Cebidae-
Primates), na Mata Atlintica, Serra de Paranapiacaba, SP.
PhD thesis, Universidade de Sao Paulo, Sao Paulo.
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bach, G. G. 2002. As unidades fitogeograficas do estado
do Parand. Cidncia e Ambiente 24: 75-92.
Talebi, M. and Scares, P. 2005. Conservation research on
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Imprensa Oficial do Parand, Curitiba.





Neotropical Primates 13(Suppl.), December 2005


STATUS OF THE MURIQUI (BRACHYTELES) POPULATIONS REMAINING IN THE STATE OF
RIO DE JANEIRO, BRAZIL: PROJETO MURIQUI-RIO

Vania Luciane Alves Garcia

Secao de Mastozoologia, Departamento de Vertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de
Janeiro, Brazil. E-mail:


Abstract

In his study of the status and geographic distribution of the muriqui, Brachyteles arachnoides, of the Atlantic forest, Aguirre
(0 mono Brachyteles arachnoides (E. C ... .. Situafao atualda Espicie no Brasil, Acad. Brasil. Cienc., Rio de Janeiro. 1971)
documented its widespread disappearance from the state of Rio de Janeiro, identifying only six localities where it could still
be found, and estimating a population of only 650 to 840 individuals. In this paper, I report on 25 survey expeditions car-
ried out from 1999 to 2003 to verify the continued presence of muriquis in six localities in the state of Rio de Janeiro: the
Serra dos Orgaos National Park, Desengano State Park, Paraiso Ecological Station, the Cairuyi Environmental Protection
Area (adjoining the Serra da Bocaina National Park), the region of Maca6 de Cima and the Itatiaia National Park. A total of
55 muriquis were seen in Serra dos Orgaos, Cairuyi, and Desengano. Local inhabitants reported that muriquis were now
very rare in the region of Maca6 de Cima and the Paraiso Ecological Station. No muriquis were seen in the Itatiaia National
Park, but three specimens on show in the museum indicate that it is the northern muriqui (B. .'- .... .-.'... i which occurs
there, rather than the southern muriqui (B. arachnoides) known from the rest of the state.


Key Words muriquis, Brachyteles, conservation, distribution, Atlantic forest, Rio de Janeiro


Introduction

In his study of the status and geographic distribution of
the muriqui, Brachyteles arachnoides (E. Geoffroy, 1806),
of the Atlantic forest, Alvaro Coutinho Aguirre (1971)
documented its widespread disappearance from the state
of Rio de Janeiro, identifying only six localities where it
could still be found, and estimating a population of only
650 to 840 individuals. Over the last 35 years, we have wit-
nessed an accelerated destruction of the Atlantic forest, not
just in the state of Rio de Janeiro, but in all of eastern and
southern Brazil. Forest covered 97% of the state in 1500,
but with the various economic cycles, based largely on the
exploitation of natural resources, today the forest is entirely
fragmented, and has been reduced to 7,346.29 km2, about
17% of its original extent (42,940 km2) (Fundagao S.O.S.
Mata Atlhntica / INPE, 2001).

Hunting has also been a major factor in the disappearance
of muriquis from the state and, although today minimal in
terms of its volume compared to the past (Lane, 1900), is
no less significant in its depredation of the tiny and isolated
populations remaining. According to Silva (1987), more
than 10 muriquis were shot in 1980 in the Serra do Subaio,
in the municipality of Guapimirim, and Martuscelli (1994)
recorded that five muriquis were killed by local hunters in
the vicinity of the Pico do Cairugi, municipality of Paraty,
in 1990.


Very little is known about the numbers or the location of
the remaining populations of muriquis in the state of Rio
de Janeiro. Morphological, genetic and social differences
have led a number of researchers to argue for the existence
of two subspecies of muriqui, one southern and the other
northern, divided by the Serra da Mantiqueira (Lemos de
Sa et al. 1990). Populations in Minas Gerais and Espirito
Santo (B. .' ... .-.'o.. [Kuhl, 1820]), have spotty, partially
depigmented faces and genitalia, and a vestigial thumb, but
those in Sno Paulo (B. arachnoides) have darkly pigmented
faces and genitals, and lack the vestigial thumb (Lemos de
Sa and Glander, 1993). Coimbra-Filho et al. (1993), Ry-
lands etal. (1995, 2000) and Groves (2001) consider them
to be distinct species.

As Rio de Janeiro marks the supposed range limits of the
two species, there are doubts even as to the taxonomic
identity of the muriquis there. The "Projeto Muriqui-Rio"
was created in 1999 to obtain information regarding the
whereabouts, identity, and population sizes of muriquis in
the state of Rio de Janeiro as well as to assess the threats
they are facing. This paper reports on the findings from a
series of surveys, including numerous interviews of local
people, carried out by a team led by the author from 1999
to 2003 specifically to address these questions.







Methods

From January 1999 to December 2003, we visited six pro-
tected areas in the potential range of the muriqui in Rio
de Janeiro. Each field trip lasted from 7 to 30 days and
our survey methodology included: 1) interviews with the
staff of the protected areas and people in nearby villages;
2) consultation of topographic maps at different scales to
locate and demarcate sites to be surveyed; 3) the hiring of
local guides in each locality; 4) daily walks along trails in
search of muriquis; 5) use of'play-back'-playing arecord-
ing of muriqui vocalizations ('long-calls') using a speaker,
walkman tape-recorder, a 200W amplifier and battery; and
6) use of a Geographic Positioning System (GPS) Garmin
12XL) to map the trails we walked and to pinpoint the
locations of primate sightings. When seeing muriquis, we
recorded the time and duration of the encounter, GPS co-
ordinates and altitude, group size, sex and age of the indi-
viduals seen (adults, juveniles and infants), the vegetation
type and height in the forest, and made descriptions of
their appearance and behavior (for example, their reactions
to us). We always accompanied the muriquis for as long as
we could. In general, we used already existing trails, but in
some cases it was necessary to open up new ones.

Results

We carried out 25 expeditions from 1999 to 2003. We
were able to verify the presence of muriquis in three of the
six protected areas we visited: the Serra dos Orgaos Na-
tional Park, Desengano State Park, and the Cairugi Envi-
ronmental Protection Area (adjoining the Serra da Bocaina
National Park).

Serra dos Orgdos National Park
The Serra dos Orgaos National Park of 11,800 ha (elevations
ranging from 300 to 2,263 m above sea level) is marked by
precipitous terrain, with steep cliffs rising above the dense
submontane forest typical of the Serra do Mar. We iden-
tified four vegetation types in the park: dense evergreen
submontane forest (floresta ombrofila densa submontana),
montane evergreen forest (floresta ombrofila montana), high
altitude evergreen forest (floresta ombrofila alto montana),
and high altitude grassland (campos de altitude).

The first expedition to the park in 1999 involved 30 days
of fieldwork. No muriquis were seen then, but we suc-
ceeded in finding them during intense fieldwork there over
10 months in 2002 (see Garcia and Andrade Filho, 2002;
Garcia, 2005). Groups were seen in four locations: forest
near to the Dedo de Deus ("Finger of God", a notable rock
formation), and in the vicinity of the headwater springs of
three rivers: the Rio Paquequer, Rio Soberbo (Garrafao),
and Rio Santo Aleixo. The first three locations are close to
each other, and were quite possibly sightings of the same
group. The maximum number of individuals seen in the
three areas was 22. At Santo Aleixo we saw another group


Neotropical Primates 13(Suppl.), December 2005

of at least 15 animals. As such, the minimum number of
muriquis seen was 37, we believe in two separate groups.

The muriquis in the Serra dos Orgaos National Park had
the appearance of B. arachnoides; all with dark faces. They
were very shy, and intolerant of our presence. On seeing
us, one of the adults would face us, apparently trying to
intimidate us, grimacing, shaking branches, and vocalizing
loudly while the other muriquis would slip away silently.

Three other primates were seen in the park: the horned ca-
puchin (Cebus nigritus), the brown howler monkey (Alouatta
guariba), and the black-tufted-ear marmoset (C
penicillata) (introduced). Cunha (2003) has also registered
the black-fronted masked titi (Callicebus nigrifrons) in the
region, but we never saw it in the park.

A number of hunter's hideouts (ranchos) were found in
the park, one of them (found by the team in 1999) near
the home range of the muriquis, with many shotgun traps
(trabucos) and rifles. At Santo Aleixo we found a capuchin
monkey in a trap for large animals. There are two other
threats to the muriquis in the park besides hunting: loss
of forest due to occasional wildfires, especially in the
dry season, and, as argued by Cunha (2004), adventure
tourism.

Paraiso Ecological Station
The Paraiso Ecological Station of 5,000 ha is in the mu-
nicipalities of Guapimirim and Cachoeiras de Macacd
(2226'-2232'S and 4250'-4256'W). Altitudes range
from 60 m to 1,350 m (Serra do Subaio) above sea level. The
vegetation there is typical submontane and montane forest.
We worked for seven days in the area, but no muriquis were
located. The people there informed us that they were very
difficult to see, having been, for too long, a favored target of
hunters. Silva (1987) reported that more than 10 muriquis
were killed in the Serra do Subaio in 1980.

Region ofMacae de Cima
Part of the 46,350 ha of forests that today make up the
Tres Picos State Park, this region (2221'-2228'S and
4227'-4235'W) is covered by typical montane evergreen
forest at altitudes ranging from 880 m to 1,720 m (Lima
and Guedes-Bruni, 1997a). It is one of the most important
areas of montane forest remaining in the state of Rio de
Janeiro. Botanically rich, the flora includes representatives
of 122 families, and 1,103 species of vascular plants have
been recorded there. Predominant are Lauraceae, Myrtace-
ae, Melastomataceae and Leguminosae (Lima and Guedes-
Bruni, 1997b). We spent 15 days in the area but no muriq-
uis were seen. Local inhabitants told us they were there, but
very rare. The primates we did see were the buffy-tufted-ear
marmoset (C .- aurita), horned capuchin monkey
(C. nigritus) and the brown howler monkey (A. guariba).
The forest was well preserved, and the rarity of the muri-
quis could only be due to hunting. Four hunter's hideouts





Neotropical Primates 13(Suppl.), December 2005

were found with shotgun traps (trabucos) and traps for me-
dium-sized animals.

Desengano State Park
In the municipalities of Santa Maria Madalena, Sao Fiddlis,
and Campos, this park of 22,400 ha protects the last rem-
nant of the Atlantic forest in the northern part of the state.
The vegetation there is dense evergreen submontane (up to
500 m) and montane (between 500 and 1,500 m) forest
and high altitude grasslands (above 1.600m).

We carried out four expeditions to the park. The first was
for 20 days in June and July of 1999, when we surveyed
the forests of Morumbeca (Matas da Morumbeca) cited by
Aguirre (1971). We found a group of 17 muriquis (15 adults
and 2 infants) on 12 July 1999 at 13:00 h, at a place
called "Boqueirao da Mata na Serra Grande" (2152'90"S,
4152'93"W), about three hours walking from Morum-
beca (base camp). Other locations in the park were visited
between November 2002 and March 2003. In January
2003, again at Morumbeca, our team found two muriquis
crossing a trail going up to the Pedra do Desengano, 200 m
away. It was not possible to be sure of the identity of the
muriquis as either B..' .;... .-.'... or B. arachnoides. Howler
monkeys (A. guariba) and capuchin monkeys (C. nigritus)
were also seen within the park boundaries. There are people
living, illegally, within the park. They have some livestock
and cultivate small garden plots, and hunt. According to
informants there, muriqui meat is much appreciated.

Cairufi Environmetal Protection Area (APA)
The APA Cairugi (33,800 ha) is in the far south of the mu-
nicipality of Paraty (2310'-2323'S and4430'-4451 'W).
The continental portion begins at the Rio Mateus Nunes
and ends at the state border with Sao Paulo, and the island
portion (63 islands) extends from the Ilha do Algodao in
Mambucaba (see Vaz, 1998) to the Ilha da Trindade in
Trindade. It adjoins the Serra da Bocaina National Park in
Sao Paulo. The relief is mountainous with altitudes rang-
ing from sea level to 1,320 m (Pico Cairugi). Marques
(1997) reported the following vegetation types there (in
order of importance): Dense evergreen forest; secondary
forest, rocky outcrops and rocky shorelines; mangroves and
resting (coastal scrub and forest on sand soil). There are
cultivated areas, beaches and urban areas such as the town
of Paraty itself and the Condominio Laranjeiras (a housing
estate).

The word 'cairuyg' translates in Tupi-Guarani to "cai" =
monkey and "rugu" = big, which makes us believe that
muriquis were common in the region at least in the past.
We spent 33 days in the area in August and September
1999, and later in February and December 2000. We vis-
ited the following locations: Toca do Ouro (adjoining the
Serra da Bocaina National Park), Pico do Cairugi (Vargem
Grande and the coastal area of the beach of Martin de Si,
Juatinga Ecological Reserve) and Saco do Mamangui. Only


one muriqui was seen; at the Toca do Ouro, identified as B.
arachnoides.

Protected by local legislation, the local people, called
caigaras, are fisher communities but also hunt, even though
local informants told us that there was little wildlife left.
With regard to habitat loss and degradation, the impact of
the caigara communities is not yet serious, but is increas-
ing markedly. Specimens of muriquis in the mammal col-
lection of the Museu Nacional of the Federal University
of Rio de Janeiro (UFRJ) were collected in Pedra Branca
(Paraty) in 1941 and 1943 and Mambucaba, Angra dos
Reis in 1942 (Vaz, 1998).

Itatiaia National Park
The Itatiaia National Park is in the southwest of the state of
Rio de Janeiro (2219'-2245'S and 4445'-4450'W), in
the municipalities of Resende and Itatiaia, extending into
southern Minas Gerais, in the municipalities ofAlagoa, Bo-
caina de Minas and Itamonte. With an area of 28,267 ha,
the park takes in the highest elevations of the Serra da Man-
tiqueira, and is characterized by mountains and rocky out-
crops at altitudes of 650 m to 2,787 m (Pico das Agulhas
Negras). According to the phytoecological classification of
Veloso et al. (1991), the vegetation of the Itatiaia National
Park includes: Dense evergreen montane forest at altitudes
ranging from 650 m to 1,500 m; high altitude evergreen
forest, above 1,500 m; mixed montane evergreen forest
with Araucaria angustifolia at altitudes around 1,200 m;
seasonal semideciduous montane forest along the leeward
slopes at 500 m; and high altitude grasslands in rocky and
precipitous regions above 1,600 m (IBDF, 1982).

We visited the park twice-in October 1999 and in De-
cember 2002. We did not see any muriquis on either occa-
sion. Camara (1995) and Marriog and Sant'Anna (2001)
however, have registered their presence there. We examined
three taxidermized muriquis on show in the museum of
the park; an adult male, adult female and infant collected
by Elio Gouveia in 1950 at a location called Maromba that
is within the park boundaries. All three had the vestigial
pollex, which would characterize it as the northern muriq-
ui, B. .'.... .-.'.. (Lemos de Sa and Glander, 1993). We
saw the black-fronted masked titi (Callicebus nigrifrons) and
the horned capuchin monkey (C nigritus) during our field
surveys there.

It would appear that there is little hunting in the area,
even though there are some private properties within the
park (Rocha et al., 2003). There is some adventure tour-
ism which could be affecting the use of the forest by the
muriquis, as was observed by Cunha (2005) in the Serra
dos Orgaos National Park.







Discussion

Distribution and abundance of muriquis in the state of Rio
de Janeiro
Montane forests at elevations above 500 m in Rio de Ja-
neiro and other regions of southeast Brazil are evidently
good habitat for the muriqui (Aguirre, 1971). The largest
areas of forest remaining in the state of Rio de Janeiro are
in these mountainous regions, and many are in protected
areas (Rocha et al., 2003). Of the six surveyed by the Pro-
jeto Muriqui-Rio, we were able to confirm muriquis in
three (Serra dos Orgaos National Park, APA Cairugi, and
Desengano State Park); observing a total of 55 individuals.
Although this is a small number, much lower than was es-
timated for the state by Aguirre (1971) in the 60s (between
650 and 840), it is patent that much more research and
field work are needed. Their long history of being hunted
means that muriquis are not just scarce but also extremely
wary and shy, and they now reside in areas of extremely
difficult access. Further work needs to be done in the areas
we have visited, as well in the four protected areas we have
yet to survey, all of which are reported to contain muriquis:
Tingui Biological Reserve (26,000 ha), APA Mangaratiba
(22,936 ha), Tres Picos State Park (46,350 ha), and the
Serra da Bocaina National Park (110,000 ha). The region
around Pedra Branca (Paraty) is also a priority for further
surveys, considering the historical (1941 and 1943) records
of muriquis occurring there.

In Rio de Janeiro, the muriquis are confined to montane
forests at high elevations, difficult to reach and difficult to
survey, which also means that we are undoubtedly underes-
timating their numbers. In the Serra dos Orgaos National
Park, for example, they were found at altitudes ranging
from 800 m to 1,500 m (Garcia, 2005). Muriquis may also
occur in naturally lower densities in the larger forest tracts,
as has been noted for the southern muriqui in Sao Paulo by
Strier (2000). In spite of these difficulties, it is vital that we
obtain better and more precise information on the number
and extent of muriquis remaining in the state if we are ever
to draw up a realistic conservation plan for the species.

Based on the absence of the vestigial pollex and the presence
of dark pigmentation in the bare skin of the face and geni-
tals of the muriquis that we observed in Serra dos Orgaos
National Park, and on the presence of the thumb and the
freckled pigmentation of the three stuffed specimens on
show in the museum in the Itatiaia National Park, it is evi-
dent that both species occur in the state-B. arachnoides
in the Serra do Orgaos and B. ':.. .-'.. in Itatiaia. The
southern muriqui (B. arachnoides) evidently occurs along
the Serra do Mar, from northern Parand, through Sao Paulo
into Rio de Janeiro, passing as such through the southern
(APA Cairugu and Serra da Bocaina National Park) and
central (Serra dos Orgaos National Park) regions and prob-
ably extending into the north of the state (Desengano State
Park). The northern muriqui (B. '\:.. .-'.. then would
be in the southwest (Itatiaia National Park), following the


Neotropical Primates 13(Suppl.), December 2005

Serra da Mantiqueira. These roughly delineated distribu-
tions require further research.

Threats to the muriqui in Rio de Janeiro
Although occurring in a number of protected areas, we
found that muriquis were under pressure from hunting,
habitat loss and degradation, and disturbance from human
activities of all sorts everywhere we went. In the Serra dos
Orgaos National Park, for example, both adventure tour-
ism (perhaps restricting the area that the muriquis will use)
and hunting were evidently serious enough to be prejudicial
to the small number of muriquis surviving there (Cunha,
2005). We found evidence of hunting throughout the park.
In the APA Cairugi, the Paraiso Ecological Station, and in
the region of Macad de Cima hunting is also the key factor,
both from the evidence we found and the reports of Silva
(1987) and Martuscelli (1994). Both hunting and deforest-
ation by squatters are threats in the Desengano State Park.
The Itatiaia National Park would seem to be comparatively
free of hunting, and habitat loss is probably the key issue
with the constant presence of people living in the park, of
tourists, the threat of fires, and the illegal exploitation of
plants such as palms for palm hearts (Rocha et al., 2003).

Muriquis are large, they travel in large groups, and are quite
noisy, which makes them easy prey to the patient hunter.
We were informed in the APA Cairugi and the Desengano
State Park that muriqui meat is considered a delicacy. As
they have a slow reproductive rate (one infant every three
years: Strier, 1993-1994) and possibly naturally low densi-
ties in the larger areas of forest (Strier, 2000), killing just a
few individuals each year can have serious consequences in
determining a gradual decline in numbers. Besides increas-
ing vigilance, it is important that environmental education
programs be put in place in the vicinity of these parks.

Future research
There are long-term programs in conservation and research
in most of the states where muriquis occur. Rio de Janeiro
is one, however, where activities of this sort are unfortu-
nately still incipient. We still lack basic information on
the numbers and location of the surviving populations of
muriquis, besides many other threatened species. In 2005,
Andrd A. Cunha and Jean P. Boubli launched the Projeto
Muriqui-Rio Fase II, with the specific objective of deter-
mining how many muriqui populations are remaining in
the state and their size. This project has received financial
support from Conservation International, The Interna-
tional Newcomers Club of Rio de Janeiro, the Zoological
Society of San Diego, the Serra dos Orgaos National Park
and the Brazilian Institute for the Environment (IBAMA),
and the Instituto Terra de Preservagao Ambiental. The Pro-
jeto Muriqui II will visit further sites and also collect fecal
samples of muriquis in order to begin genetic studies exam-
ining the genetic diversity and structure of the remaining
populations. Two sites will be selected to set up long-term
ecological, behavioral and demographic studies, including





Neotropical Primates 13(Suppl.), December 2005

phenological and floristic monitoring of the vegetation, to
examine the ecological diversity of the muriquis.

Acknowledgments

My sincere thanks to Admiral Ibsen de Gusmao Camara
for his encouragement, inspiration and help in setting up
the Projeto Muriqui-Rio. I am grateful to Russell A. Mit-
termeier and the Margot Marsh Biodiversity Foundation,
the Fundagao 0 Boticario de Protegao a Natureza, and
the John D. and Catherine T. MacArthur Foundation for
financial support. The Brazilian Institute for the Environ-
ment (Instituto Brasileiro do Meio Ambiente e dos Recursos
Naturais Renovdveis IBAMA) and the Forestry Institute
of Rio de Janeiro (Instituto Estadual de Florestas IEF-RJ)
kindly provided the permits to work in the protected areas
under their jurisdiction. Sr. Tatico, Ricardo, M. Rocha,
Guilherme and Jorginho were invaluable in their help in
setting up the expeditions to search for muriquis in Rio de
Janeiro, and I am especially grateful to Jean P. Boubli for his
participation in the trips to Maca6 de Cima and Desengano
State Park. My thanks also to the photographer Jos6 Caldas
for his participation in some of the trips and for allowing
me the use of his photos.

References

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Neotropical Primates 13(Suppl.), December 2005


SURVEY AND STATUS OF THE MURIQUIS (BRACHYTELESARACHNOIDES) IN THE SERRA
DOS ORGAOS NATIONAL PARK, RIO DE JANEIRO

Vania Luciane Alves Garcia

Secao de Mastozoologia, Departamento de Vertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de
Janeiro, Brazil, e-mail:


Abstract

The Serra dos Orgaos National Park protects 11,800 ha of Atlantic forest in the state of Rio de Janeiro (2230'S, 4306'W;
300 to 2,263 m above sea level). Vegetation types include montane dense evergreeen forest up to altitudes of 1,800 m;
cloud forest from 1,800 to 2,000 m; and high altitude grassland above 2,000 m. This paper reports on surveys carried out
in 10 localities in the park specifically to obtain a minimum estimate of the population of northern muriquis (Brachyteles
arachnoides). Muriquis were sighted 26 times at altitudes ranging from 800 to 1,500 m. It is possible that they belonged to
four groups in which case the minimum number of individuals recorded would be 56. If in fact the sightings were of just two
groups, the minimum number of individuals would be 32. Black-horned capuchin (Cebus nigritus) and brown howler mon-
keys (Alouatta guariba) were also recorded for the park. The buffy-tufted-ear marmoset (C .-'. aurita) was not seen.


Key Words primates, muriqui, Brachyteles, Serra dos Orgaos, Atlantic forest, Brazil


Introduction

There is now some quite substantial information on the
populations of the northern muriqui in Minas Gerais
(Brachyteles .' :.... .-'.. i in the states of Minas Gerais and
Espirito Santo, as well as on the occurrence of the southern
muriqui (B. arachnoides) in Sao Paulo (Mittermeier et al.,
1987; Paccagnella, 1991; Pinto et al., 1993; Martuscelli et
al., 1994; Strier and Fonseca, 1996/1997). The same cannot
be said of the state of Rio de Janeiro, where the remaining
populations have yet to be located and counted-it is still
unclear exactly which of the species occur there.

In his survey more than 30 years ago, Aguirre (1971)
found that they had disappeared from most of their range
in Rio de Janeiro, and estimated a total population of only
about 770. From 1999 to 2003, Garcia (2005) surveyed a
number of localities in the state (Projeto Muriqui Rio) in
order to identify their continued occurrence there and the
status of the populations. Hunting and forest loss continue
to be major threats. The "Projeto Muriqui" was created in
2002 in the Serra dos Orgaos National Park as a focus for
studies on the conservation of muriquis in Rio de Janeiro.
Here I report on the results of one of the projects of this
program; a study of the remnant population of muriquis in
the park itself.

Methods

Study area
The Serra dos Orgaos National Park, of 11,800 ha, was cre-
ated in 1939. It covers parts of the municipalities of Petr6p-
olis, Teres6polis, Mag6 and Guapimirin, in Rio de Janeiro


(2230'S, 4306'W) (Fig. 1). A number of rivers supplying
water to urban centers in the lowlands have their sources in
these mountains, including the rios Paquequer, Soberbo,
Jac6, Bananal, Bonfim and Santo Aleixo. The terrain is one
of steep slopes and rugged mountains, with elevations rang-
ing from 300 to 2,263 m (the Pico da Pedra do Sino). The
climate is tropical superhumid, with temperatures during
the year averaging 190C.

The park is largely forested, within the domain of the
Atlantic Forest (Rizzini, 1997): lower montane, mon-
tane and upper montane dense evergreeen forest (Floresta
Ombrofila Densa), following the classification ofVeloso et
al. (1991). Following the altitudinal gradient it is possible
to identify three phytophysiognomies in the park: montane
forest-the majority of the park, with very large trees and a
high canopy, at altitudes up to 1,800 m; cloud forest (Mata
Nebular) -with smaller trees, lower canopy, abundant in
epiphytes, from 1,800 a 2,000 m; and high altitude grass-
land (Campos de Altitude)-with shallow soils, bushy and
herbaceous plants, many of them of endemic, at altitudes
above 2,000 m. Although the forest would appear to be
primary-with immense trees, and rich in palms, lianas,
and epiphytes -the long history of exploitation of these
forests means that they are in fact secondary, but in late
stages of succession. Only some parts of the park maintain
their original forest cover.

Data collection
In a reconnaissance expedition in January 2002, we vis-
ited the park and neighboring areas to determine where
muriquis had been seen. Ten areas were selected. Field
work was from February to October 2002. To reach the





Neotropical Primates 13(Suppl.), December 2005


As'w 44'W 4YW 42'W 41W

Figure 1. Location of the Serra dos Orgaos National Park in the state of Rio de Janeiro.


locations where muriquis had been reported, it was neces-
sary to provide training in rock climbing techniques (Fig.
3). The field team included a coordinator in field research,
two assistants, three mountain climbers from Teres6polis,
two guides from Santo Aleixo (the village near the park),
and four porters.

The areas surveyed were some distance from the park head-
quarters and difficult to reach. We camped in each loca-
tion for up to 10 days. The porters were dispensed with
once camp had been set up. Locations and sightings were
mapped using a Geographic Positioning System, although
satellite reception was rather intermittent. We also mapped
our survey routes and made notes on sightings of other pri-
mates and large mammals and birds, as well as all signs
of hunting (including traps and hideouts) and encounters
with the hunters themselves and their dogs.

To locate the muriquis we would watch for them from van-
tage points, such as rocks or trees that afforded broad views
of a valley and the surrounding forest. All day watches were
set up at these lookouts while other team members would
walk the trails (Fig. 4). We used existing trails mostly, but
in some areas it was necessary to cut new ones. Radios
"Talk" were used to maintain contact between team mem-
bers and an HT radio to maintain contact with the park
headquarters.

We used "play-backs"-a recording of muriqui vocaliza-
tions to increase the chance of locating them. We did four
to six play-back sessions a day, each one lasting 15 minutes


Figure 2. View otf erra dos Urgaos National Park, showing some
of the rock. Peaks from left to right: Escalavrado, Dedo de Nossa
Senhora, Dedo de Deus and Cabega de Peixe. Photo by Jos6
Caldas.


Figure 3. An obstacle met when surveying the muriquis in the
Serra dos Orgaos National Park.


0 2 50 1 Kinl


1 Serra dos 6rgaos National Park





Neotropical Primates 13(Suppl.), December 2005


Figure 4. One of the of the observation points for muriquis in the
Serra dos Orgaos National Park.


(Fig. 5). For each muriqui sighting we noted the follow-
ing: date, time, number of individuals, age-category and
sex when possible, vegetation type, activity when first seen,
and the location. We accompanied each muriqui group for
as long as possible. We surveyed ten areas, totaling 86 days
of field work, averaging 65 hours per expedition. "Play-
back" recordings of their vocalizations were broadcast for a
total of six hours and 55 minutes.

Results

We saw muriquis 26 times, and found indications of hunt-
ing on 24 occasions (Table 1). The areas where we found
most signs of hunting were Santo Aleixo and Rio Bananal.
The majority of them were their hideouts and camps, but
we also found nets and various types of traps including
shotgun traps (armed), and wooden platforms, and even
came across the hunters' dogs and the hunters themselves.
A black-horned capuchin (Cebus nigritus) was in one of the
traps (it was photographed and released). Nearly all the
camps we found were evidently recent, with the remains of
food, a cooking fire, and cooking utensils-ready as such
to be used at any time. In most cases we were able plot the
location of these camps with the GPS.

Despite the considerable use of the "play-back" record-
ings, they resulted in replies from the muriquis only twice.
On the first occasion the team, watching from a lookout
had already seen a group, which was living in the area of


Table 1. Expeditions dates, their duration and hours in the field, time spent in playback sessions, number signs of hunters, sightings of
muriquis, and numbers of fecal sample obtained. Serra dos Orgaos National Park, Rio de Janeiro.
Expedition (months) No. of days Field work Time spent in Signs of Sightings Number of
2002 ________ __ (hours) 'playback'(mins.) hunting Sight feces collected
Rio Beija Flor 4 40 0 2 0 0
(February)
Dedo de Deus and Cabeqa de Peixe
(February- March)
Rio Paquequer or C6rrego Pedra Acu 7 25 0 1 2 1
(March)
Vale das Orquideas and Basin of the
Rio Paquequer or C6rrego Pedra Acu 8 77 230 0 1 0
(April)
Basons of the rios Jacuba and Beleira
and Pedra Itaculumi (Santo Aleixo) 11 66 95 4 0 0
(May)
Trilha das Torres da CERJ
(Santo Aleixo/Petr6polis) 10 56 0 2 0 0
(June)
Basin of the Rio Bananal 10 78 135 4 0 0
(July) 10 15 4 0 0
Basin of the Rio Soberbo
(Auut 10 82 105 1 12 3
(August)
High altitude grassland and Rio Jac6 10 75 45 2 0 0
Rio Santo Aleixo 11 114 45 7 10 1
Total 86 649 655 24 26 6
1Hunters' camps, traps, hunters and their dogs.







the springs of the Rio Paquequer. The muriquis had not
seen the observer, who decided to test the recording. The
muriquis were moving away, but when they heard the re-
cording the turned about and moved towards the calls.
On the second occasion, the observer had just completed
a playback session, but was leaving because it was becom-
ing foggy, at which moment an adult female appeared out
of the mist in the exact spot were the recording was being
played. It would seem that she had responded to the play-
back even though she did not herself vocalize.


Figure 5. Testing the "playback" equipment,
National Park, Rio de Janeiro.


Serra dos Orgaos


Neotropical Primates 13(Suppl.), December 2005

The muriquis we saw in the Serra dos Orgaos National Park
looked more like the southern muriqui (B. arachnoides)
than the northern (B. .'. -.'.. i Their faces were very
black. They were very difficult to observe. On seeing us
they would make alarm calls. One individual would show
intimidating behavior, calling, while the rest of the group
would slip away quietly. They were seen in four areas of
the park: in the forests adjacent to the Pedra do Dedo de
Deus and the Pedra da Cabega de Peixe (individuals were
seen, and photographed going up and down the latter,
which is entirely forested), and areas of the springs of the
rios Paquequer, Soberbo and Roncador (or Santo Aleixo)
(Table 2). When we saw them near the Dedo de Deus (in
March) they were eating fruits of a Myrcia (Myrtaceae) tree,
the seeds of which were consistently found in the feces we
collected in the area of the Rio Soberbo in August. It would
seem that the species fruits for prolonged periods or that
the mountainous terrain provides for different climates in
the various parts of the park that in staggered fruiting. The
muriquis of the Rio Soberbo were also seen eating fruits of
C j .'- .. viride (Mart. & Eichler), a tree of the Family
Sapotaceae. We found seeds of at least six other species in
their feces, but they could not be identified. The high alti-
tudes and humid conditions year round in many parts of
the park, we believe favor fruit production even in the dry
season, when they would be lacking in drier forests.

If the muriquis seen in each of the four areas are different
groups, we have a minimum count of 56 for the park. We
saw muriquis at altitudes ranging from 800 to 1,500 m.
One record, a photograph taken by a tourist of a muriqui
walking on the ground was at 2,000 m in the high alti-
tude grassland. This is the highest elevation recorded for
the species, which Aguirre (1971) believed should be be-
tween 1,800 and 2,000 m. The best estimates for group
composition came from observations of the Rio Soberbo
and Paquequer muriquis. Solitary females, females with in-
fants, juveniles of different sizes, and adults.

Two other primates were observed besides the muriq-
uis: the black-horned capuchin (Cebus nigritus) and the
brown howler monkey (Alouatta guariba) (Fig. 6). The
buffy-tufted-ear marmoset (C .-'. aurita) certainly


Table 2. Sightings of muriquis in the Serra dos Orgaos National Park, Rio de Janeiro.
Altitude Number of Age/sex 2 Activity when
(m) individuals composition' Forest type first seen
Forest adjacent to the AD, 1AM, 1AF,
mountain peaks of Dedo de 1.300 7 2JU MF Eating fruit
Deus and Cabeqa de Peixe
Rio Paquequer basin (C6rrego 1AM, 6AD, 1AF+, MF Traveling
Pedra Aqu) 1.500 17 9UN MF Traveling
Pedra Acu) 9UN
Rio Soberbo basin 1.250-1.493 20 2AF+1, 5JU, 12AD MF and HAF Eating fruit
Rio Roncador (Santo Aleixo) 800-1.200 12 10AD, 2JU MF Vocalizing
Total 56
'AM = adult male; AF+ 1 = adult female with infant; JU= juveniles; UN = sex and age unknown; AD = adults
2MF = montane rain forest; HAF = high altitude rain forest.





Neotropical Primates 13(Suppl.), December 2005

occurred in the region in the past (specimens in the Museu
Nacional of Rio de Janeiro), but it was never seen. An in-
troduced black-tufted-ear marmoset (C .-( penicillata)
was seen near the park headquarters. Muriquis were the
most frequently seen of the primates, even though they
were only found in four areas. Capuchins and howler mon-
keys were seen in most of the areas we visited, but only very
infrequently.


Table 3. Population density estimates for muriquis, Brachyteles.
For the Serra dos Orgaos National park (this study) the estimated
minimum number of muriquis was divided by the area of the
park (in bold).
Local Etado Area Densidade
(km2) (ind/km2)
Jacupiranga State Park SP 300.00 0.0067
Jurupara State Park SP 263.00 0.0190
Alto Ribera State Park SP 350.00 0.0343
Serra do Mar State Park SP 662.50 0.0377
Jureia State Park SP 200.00 0.0400
Rio Doce State Park MG 360.00 0.0583
Caparao National Park ES 260.00 0.0731
Ibitipoca State Park MG 14.88 0.1344
Fazenda Sao Sebastiao do Rio SP 10700 0.2056
SP 107.00 0.2056
Grande
Serra do Brigadeiro State Park MG 200.00 0.2500
Augusto Ruschi Biological Reserve ES 40.00 0.2750
Sao Francisco Xavier SP 40.00 0.3750
Parque Nacional da Serra dos R 118.00 0.474
Orgaos
Intervales State Park SP 380.00 0.6316
Carlos Botelho State Park SP 376.44 1.3282
Mata do Sossego Biological MG 8.00 2.6250
Station
Fazenda Barreiro Rico SP 32.59 2.9150
Caratinga Biological Station MG 8.60 10.4651
Fazenda C6rrego de Areia MG 0.60 13.3333
Fazenda Esmeralda MG 0.44 27.2727
Source: Strier & Fonseca, 1996/1997.




Cebus
nigfilus


Alouatta
guariba


Brachyteles

0 5 10 15 20 25 30
Frequency

Figure 6. Numbers of sightings for three primates in the Serra dos
Orgaos National Park, Rio de Janeiro.


Discussion

Dividing the estimated minimum number of muriquis (56)
by the area of the park gives a density of a little less than
0.5 muriquis per km2 (Table 3). Although not very differ-
ent from estimates of populations elsewhere, it would still
seem very low, and is certainly lower than any population
which would be considered viable in the long-term (Lande,
1988). It is quite possible that the overall density is low
because not all parts of the Serra dos Orgaos National Park
provide suitable habitat in terms of the abundance and dis-
persion of food resources. Equally it may be that in these
montane habitats home ranges are naturally larger for the
same reason. Prolonged field research would be required to
test this and, considering the difficulties of working in such
terrain, the chances of such studies being carried out would
seem to be slim.

While hunting is obviously taking its toll, the muriquis are
extremely shy and the terrain so difficult for any realistic es-
timate. The growth of the population at the Caratinga Bio-
logical Station in Minas Gerais, would, however, be reason
for hope that, with due protection and time, the popula-
tion would increase considerably (Strier, 2000). Under any
circumstances there are no doubts this is a most significant
population, both genetically and in terms of numbers.

We presume that the observations of muriquis in the four
areas were of different groups. Strier (1987) in her study of
B..':,... .-.'... i n the Caratinga Biological Station recorded
that muriquis can travel up to 3,400 in a single day, and
it is possible in this case that the Rio Soberbo, Dedo de
Deus and Rio Paquequer were of the same group or just
two groups, rather than three. We have no doubts that
the Santo Aleixo group at least was not confused with any
of the others because of the distance separating them. If
there were in fact only two groups, the minimum number
would be 32 (20 for Soberbo and 12 at Santo Aleixo). If
three groups, the number would perhaps be 49 (Soberbo
with 20, Paquequer with 17, and Santo Aleixo with 12).
Further studies, including the use of radio-collars perhaps,
would be needed to understand better the ranges of these
muriqui groups and provide more accurate counts.

Acknowledgments

I am most grateful to Roberto Vancini, biologist with the
staff of the national park. He it was who inspired me to
raise funds and set up the Projeto Muriqui. He helped
and advised throughout the project and also critiqued this
manuscript. I also thank Jovelino Muniz, former Director
of the Serra dos Orgaos National Park, for the opportunity
to coordinate this research, the first phase of the Projeto
Muriqui. Tereviva kindly and efficiently helped in acquir-
ing all the material and helped with the logistics. Thank
you to all the biologists of the team-Gilson, Norberto,
Marcio, Wilson, Marcelo, S&rgio, Elias, and Darlan for
their hard work, and the dangers they faced in searching for





Neotropical Primates 13(Suppl.), December 2005


the muriquis. Special thanks to the former Federal Deputy Veloso, H. P., Rangel-Filho, A. L. R. and Lima, J. C. A.
Luiz Ribeiro for his concern and dedication to environ- 1991. Classificafao da Vegetafao Brasileira Adaptada a Um
mental causes, and also to Jean P. Boubli, Karen B Strier Sistema Universal. Fundagio Instituto Brasileiro de Ge-
and Bernardo Souza (Director of the Serra dos Orgaos ografia e Estatistica (IBGE), Rio de Janeiro.
National Park) for reviewing this text. This study was sup-
ported by funds from the Federal Government through a
collaborative agreement between the Brazilian Institute for
the Environment (Instituto Brasileiro do Meio Ambiente e
dos Recursos Naturais Renovdveis IBAMA) and the non-
governmental organization Tereviva.

References

Aguirre, A. C. 1971. 0 mono Brachyteles arachnoides
(E. C. C...'.. Situafao atual da Espicie no Brasil. Acade-
mia Brasileira de Ciencias, Rio de Janeiro. 53pp.
Garcia, V. L. A. 2005. Status of the muriqui (Brachyteles)
populations remaining in the state of Rio de Janeiro,
Brazil: Projeto Muriqui-Rio. Neotrop. Primates 13(suppl.):
73-78.
Lande, R. 1988. Genetics and demography in biological
conservation. Science 241: 1455-1460.
Mittermeier, R. A., Valle, C. M. C., Alves, M. C., Santos,
I. B., Pinto, C. A. M., Strier, K. B., Young, A. L., Veado,
E. M., Constable, I. D., Paccagnella, S. G. and Lemos
de Sa, R. M. 1987. Current distribution of the muriqui
in the Atlantic Forest region of Eastern Brazil. Primate
Conserv. (8): 143-149.
Paccagnella, S. G. 1991. Censo da populagio de monos
(Brachyteles arachnoides) do Parque Estadual Carlos Bote-
lho, Estado de Sao Paulo. In: A Primatologia no Brasil- 3
A. B. Rylands and A. T. Bernardes (eds.), pp.225-233.
Fundagao Biodiversitas, Sociedade Brasileira de Primato-
logia, Belo Horizonte.
Pinto, L. P. S., Costa, C. M. R., Strier, K. B. and Fonse-
ca, G. A. B. 1993. Habitats, density, and group size of
primates in the Reserva Biol6gica Augusto Ruschi (Nova
Lombardia), Santa Tereza, Brasil. Folia Primatol. 61:
135-143.
Martuscelli, P., Petroni, L. M. and Olmos, E 1994. Four-
teen new localities for the muriqui (Brachyteles arach-
noides). Neotrop. Primates 2(2): 12-15.
Rizzini, C. T. 1997. Tratado de F'-. -.... F do Brasil: As-
pectos Ecoldgicos, Socioldgicos e Floristicos. 2nd edition.
Ambito Cultural, Sao Paulo.
Strier, K. B. 1987. Ranging behavior of woolly spider mon-
keys, or muriquis, Brachyteles arachnoides. Int. J. Primatol.
8(6): 575-591.
Strier, K. B. 1987. Ranging behavior of woolly spider mon-
keys. Int. J. Primatol. 8: 575-591.
Strier, K. B. 2000. Population viability and regional conser-
vation priorities for muriquis (Brachyteles arachnoides) in
Brazil's Atlantic Forest. Biotropica 32: 903-913.
Strier, K. B. and Fonseca, G. A. B. da. 1996/1997. The
endangered muriquis in Brazil's Atlantic forest. Primate
Conserv. (17): 131-137.





Neotropical Primates 13(Suppl.), December 2005 85

CONSERVATION GENETICS OF THE MURIQUI: PAST, PRESENT AND FUTURE

Valeria Fagundes

Departamento de Ciencias Biol6gicas, Centro de Ciencias Humanas e Naturais, Universidade Federal do Espirito Santo. Av.
Marechal Campos, 1468, Vit6ria 29.040-090, Espirito Santo, Brazil, e-mail:


Abstract

Our understanding of the genetics of the muriqui have increased in recent decades. In the mid 1980's the first data was
obtained from polymorphisms of allozymes of 10 individuals of B. .'-.... .-.'... (northern muriqui) from Minas Gerais, and
two individuals of B. arachnoides (southern muriqui) from Sao Paulo. All specimens were considered to be of a single species.
The DNA was extracted from blood samples, which required capture and anesthesia of animals. We can now extract mito-
chondrial DNA from feces samples. Analyzing more than 120 individuals of the northern muriqui from two populations,
we are now able make inferences about genetic variability, population distinctiveness as well as intra- and interpopulation
gene flow. DNA sampling through feces is reliable, efficient, and economic, and does not risk the physical integrity of the
animals, and furnishes enough DNA that is easily reproducible for PCR amplification. Using this method it is possible to
sample a greater number of individuals in nature than would be possible if live capture were necessary. A muriqui feces and
DNA bank has been set up, and currently has samples of 230 individuals from seven of the twelve known populations of
northern muriqui. The samples resulted from field studies, but more coordinated and systematic efforts among fieldwork-
ers at the different muriqui sites are needed to improve representation across populations and species. Future perspectives
include the use of new genetic markers (nuclear and mitochondrial DNA) to identify parents, offspring, and closely related
individuals in captive and wild populations; to define units for conservation and the gene flow between them; to quantify
genetic variability in the populations; to assess the rate at which genetic variation has been lost over time; to estimate the
degree of inbreeding in the population; and to understand better the genetic differentiation of the two species.


Key Words- conservation genetics, muriqui, Brachyteles, fecal DNA, genetic variability.


General Issues of Genetic Conservation

A major goal of conservation biology is to preserve genetic
diversity, based on the assumption that higher heterozygos-
ity (the measure of the within-population component of
genetic variation) increases the probability of a population's
survival in the event of ecological or evolutionary changes.
Under this concept, concerns about the conservation of
biodiversity represent concerns about the conservation
of genetic diversity.

For threatened species, hunting and reduction of habitat are
associated with a reduction of population size. In extreme
cases, a significant percentage of a population is killed or
otherwise prevented from reproducing (bottleneck); the
most frequent cause of loss of heterozygosity. When a large
percentage of a population is lost, only a subset of the
genes of the original gene pool will survive. Some alleles
will be disproportionately represented, while other alle-
les may be gone forever. If one survivor has a rare allele,
then that allele may come to be represented in the result-
ing population (a few generations later) in greater numbers
than was the case prior to the population crash (a founder
effect). In small populations, the effects of genetic drift on
loss of genetic variation (stochastic events that alter allele
frequencies among members of a population and change


the diversity of the group over time) are much greater than
they are in larger populations. Some examples of the effects
of habitat reduction on loss of genetic variation have been
reported for both the Florida panther (Roelke et al., 1993)
and the cheetah (O'Brien, 1994).

A critical parameter for the management and conservation
of natural populations, therefore, is the effective population
size, which affects the rate at which genetic diversity is lost
in the population by genetic drift (Franklin, 1980). The
longer the species experiences a bottleneck, the higher the
effects of genetic drift (Futuyma, 1992). Delays in promot-
ing a species' population recovery can be highly prejudi-
cial in terms of loss of genetic diversity, and measures that
can rapidly bring about an increase in population size are
paramount.

Moreover, due to reduction of population size, most of the
individuals will not mate randomly within the population,
and the effect of inbreeding is that the alleles are prone to
become homozygous and the hybrid heterozygous advan-
tage is lost. With inbreeding, the chance of unfavorable
recessive genes turning up in the offspring is greatly en-
hanced. Thus, the presence of recessive alleles in the popu-
lation may lead to inbreeding depression, which means im-
paired fitness with the reduction in evolutionary potential,







and ultimately an increase in the probability of a popula-
tion going extinct (Frankham et al., 2002).

The viability of species that survive short-term demograph-
ic and environmental threats may depend upon the genetic
variability and its spatial distribution prior to the popula-
tion crash. The spatial pattern of the population crash also
has important consequences for the resulting genetic vari-
ability (or lack of it). Thus, small and isolated populations
are at a higher risk of extinction than large and well-con-
nected populations (Frankham, 1995; Meffe and Carroll,
1997; Ebert et al., 2002; Frankham et al., 2002).

Over the short term, most endangered species are threat-
ened by extrinsic, environmental factors, but effective long-
term conservation planning must also incorporate genetic
factors. Conservation planning operates at many levels,
from whole ecosystems and communities to individual
organisms. At each of these levels, molecular genetic tech-
niques may provide appropriate tools to evaluate processes
and to develop management strategies. However, it is nec-
essary to understand how molecular analyses can address
questions about levels of threats and extinction.

First, threats must be identified clearly, and effective steps
taken to alleviate them (Caughley, 1994). Next, it is nec-
essary to identify priorities for conservation action-an
understanding of where measures are needed most urgently
to avoid the situation deteriorating rapidly and irrevocably.
In both cases, molecular genetic analyses can play an im-
portant role.

Management of genetic heterozygosity is the challenge
of conservation genetics. In captive populations, control-
ling inbreeding to maintain minimal population sizes and
adequate levels of heterozygosity is crucial (Queiroz et al.,
2000). In natural populations, measures must be taken not
only to guarantee the maintenance of the habitat, but also to
facilitate gene flow among individuals of local populations
in order to avoid inbreeding and loss of heterozygosity.

The general importance of genetic factors can be summa-
rized in two points. First, knowledge of genetic variation
allows an understanding of the current status and the his-
torical evolutionary processes that generated biodiversity
patterns. Second, future persistence of populations may
depend upon the preservation of important remnant com-
ponents of genetic diversity.

In the pre-molecular era, most of the studies involved phe-
notypic data amenable to observation (morphology, physi-
ology, behavior) to estimate kinship and phylogeny (Avise,
2004). However, rapid advances in the development of
molecular markers over the last two decades have facili-
tated gaining a better knowledge of the genetic structure
of natural populations. Molecular genetic approaches have
been used to identify parents, offspring, and closely related
individuals in captive and wild populations; to define units


Neotropical Primates 13(Suppl.), December 2005

for conservation, and the gene flow between such units;
to quantify genetic variability of historical populations; to
assess the rate at which genetic variation has been lost over
time in fragmented landscapes; to estimate the degree of
inbreeding in the population; to determine limits that dis-
tinguish a species, and so on. All of these areas are impor-
tant in the conservation genetics of endangered species.

Conservation Genetics of the Muriqui

Interspecific de.' 'eri.aon
The genus Brachyteles, the muriqui or mono-carvoeiro,
belongs to the Family Atelidae. In the past, only one spe-
cies was recognized, Brachyteles arachnoides, distributed
from southern Bahia to northern Parand, along the Bra-
zilian Atlantic rainforest. In 1971, Aguirre (1971) esti-
mated that the total number of individuals had been about
400,000 individuals.

Vieira (1944) it was who recognized two subspecies of
Brachyteles. Some morphological differences such as facial
skin pigmentation and the presence or absence of vestigial
thumbs suggested that this monotypic genus should be
separated into arachnoides E. Geoffroy, 1806 (in the states
of Rio de Janeiro, Sao Paulo and Parand along the Serra do
Mar) and i'.''- .-.'... Kuhl, 1820, occurring in southern
Bahia, Minas Gerais, and Espirito Santo south to the Serra
da Mantiqueira. Lemos de Sa et al. (1990, 1993), Fonseca
etal. (1991) and Lemos de Sa and Glander (1993) indicated
that Vieira's (1944) standing was valid, but that differen-
tiation is even more extreme and justifies the classification
of the two forms as separate species (Coimbra-Filho et al.,
1993; Groves, 2001), the northern muriqui, B. '- .
(Kuhl, 1820), and the southern muriqui, B. arachnoides
(E. Geoffroy, 1806). Whether the presence or absence of
vestigial thumbs is a good morphological marker to separate
the species remains questionable, however (S. L. Mendes,
pers. comm.).

The first question, therefore, about muriqui genetics in-
volves whether the southern specimens, B. arachnoides,
possess enough genetic diversification from northern speci-
mens, B. .' ... .-.'... to be designated as a separate spe-
cies under phylogenetic approaches, and whether, in an
a priori, non-discriminated analysis, specimens from the
south group together separately from the ones from north-
ern areas.

In general, mitochondrial DNA allows for analysis of phy-
logenetic relationships reflecting the history of maternal
lineages within a population, requiring only one-fourth
of the effective population size when compared to auto-
somal nuclear genes. The use of mtDNA is inappropriate
for detecting paternal gene flow between populations. On
the other hand, mtDNA is only a single genetic locus, lack-
ing recombination, which reduces its power to detect the
structure and the genetic history of the population at spa-
tial and temporal levels. DNA sequence data allow both a





Neotropical Primates 13(Suppl.), December 2005

phylogenetic and an allele-frequency approach to the anal-
ysis of population structure and patterns of population var-
iation. Because effective population size calculated under
mitochondrial loci in a given population is one-fourth of
nuclear loci, genetic drift is more powerful at mitochon-
drial loci; populations separated recently can show mito-
chondrial divergence unlike nuclear loci (Neigel and Avise,
1986). Thus, the mtDNA analyses involving samples from
several localities of northern and southern muriqui would
seem to be sufficient to address this question.

Genetic structure ofpopulations
The historical deforestation of the Brazilian Atlantic forest
since the 1500s has reduced it to small fragments with little
or no connection between them. This has resulted in few,
small and widely separated muriqui populations which
represent genetic bottlenecks, and has eliminated oppor-
tunities for gene flow through the migration of individuals
between these populations.

Currently, about 1,000 southern muriquis occur in rela-
tively large and well protected areas. The situation of the
northern muriquis is, however, more dramatic with fewer
than 900 individuals in 12 separate populations, a large
number restricted to unprotected forest fragments (Rylands
et al. 2003; Mendes et al., 2005a). Brachyteles .'.... .-.'...
is considered one of the world's 25 most endangered pri-
mates (Strier et al., 2006a).

The ecology, behavior, reproduction, and demography of a
population of northern muriquis have been investigated by
Karen B. Strier and her students since 1982 at the Carat-
inga Biological Station (EBC), also called the RPPN Feli-
ciano Miguel Abdala (EBC/RPPN-FMA), in Minas Gerais
(Strier, 1999). The population at the EBC has been grow-
ing steadily since long-term monitoring began, increas-
ing from about 50-70 individuals in the 1980's to about
226 individuals as of January 2005 (Strier et al., 2006b).
Since 2001, some new populations have been studied by
S&rgio Mendes in the municipality of Santa Maria de Jetibdi,
in the state of Espirito Santo (Mendes et al., 2005b). Since
2003, Luis G. Dias has also initiated studies of muriqui
populations in other areas of the state of Minas Gerais (Rio
Doce and Serra do Brigadeiro state parks, and the Mata do
Sossego private reserve).

In large populations with multiple groups, female muri-
quis leave their natal groups and move into others before
reaching reproductive maturity, reducing the risks of close
inbreeding (Printes and Strier, 1999; Strier and Ziegler,
2000). However, in smaller populations living in highly
fragmented and disconnected areas, dispersal is restricted,
and females with nowhere to go have been observed at
the periphery of their natal groups (S. L. Mendes, pers.
comm.). Research into the genetic variation and gene flow
among muriqui populations and the relationship of popu-
lation size to within-population genetic variability is criti-
cally needed for the formulation and implementation of a


management plan to ensure the long-term persistence of
remaining muriqui populations.

The first study involving muriqui genetics was conducted
by Pope (1998), based on polymorphisms of allozymes of
10 individuals of B..'. .... .-.'... from Fazenda Esmeralda,
Minas Gerais, and two individuals of B. arachnoides from
Fazenda Barreiro Rico, Sao Paulo. The DNA for these ge-
netic analyses was extracted from blood, with an invasive
method that depended on the capture of live specimens
(Lemos de Sa and Glander, 1993). At that time, Pope ana-
lyzed all individuals as the same species, B. arachnoides (the
possibility of two species was not generally recognized).
Pope observed a high level of genetic divergence using al-
lozyme investigations, despite the small size and isolation
of the populations. The variability observed was probably
large due to between-species rather than within-population
genetic diversity.

The first study using 126 individuals from two north-
ern muriqui populations (Estagao Biol6gica de Caratin-
ga- EBC, Minas Gerais, and Santa Maria do Jetib i- SMJ,
Espirito Santo) investigated the polymorphisms of restric-
tion fragments (PCR-RFLP) of 480 base pairs (bp) of a
hypervariable region of mtDNA or D-loop (Paes, 2005;
Fagundes et al., in press). DNA was obtained from feces
samples, a noninvasive method useful for endangered spe-
cies (Chaves et al., 2006). The overall level of genetic dif-
ferentiation between these muriqui populations was high.
The test of genetic differentiation (FsT), which character-
izes genetic differentiation among populations, indicated
that there was extensive genetic differentiation (FsT =
0.635, P-value = 0.000) between the EBC and SMJ popu-
lations (Fagundes et al., in press). Values of Nm [Nm =
(I/FsT-1)/4] indicated less than 1 migrant per generation
between SMJ and EBC, and related FsT data revealed an
absence of gene flow and high genetic distinction between
these two populations.

Also, Chaves (2005) studied the sequence of 280 bp from
the hypervariable internal segment of D-loop of 84 indi-
viduals from EBC and SMJ, and also observed high genetic
diversity among these populations (FT = 0.56). Despite the
distinction in mtDNA, the alleles did not cluster by geo-
graphic origin. Alleles from EBC and SMJ are interspersed
in both clades, which mean that these populations are not
completely distinct at this locus. Chaves (2005) also ob-
served that values of nucleotide diversity of B..'- ..
are considerably lower when compared to other endan-
gered species of mammals, including the gorilla (Garner
and Ryder, 1996), chimpanzee (Deinard and Kidd, 2000),
and the giant panda (Lu et al., 2001).

Our previous studies have shown that the loss and frag-
mentation of once contiguous habitat has caused the loss of
genetic variation in the muriqui, and that genetic variation
in the populations is among the lowest reported for any
species of primate. This substantial loss of genetic variation







has contributed to extensive genetic differentiation among
populations.

The next steps to measure genetic variability among pop-
ulations of northern muriquis will require field efforts to
sample new populations and individuals. Currently, our
collection of feces is from individuals of seven of the twelve
populations (Table 1). Some populations are still poorly
sampled, however, and not yet representative of the total
population. Just a few genetic samples for southern muri-
quis are available from blood, which makes it difficult to
conduct comparative analysis of genetic variability between
B. arachnoides and B. .': ... .-.'... New approaches to eval-
uate genetic variability, including nuclear loci, are needed
to better understand the consequences of fragmentation,
reduction of population size and genetic drift in muriquis,
and to assess the degree of genetic variation between the
northern and southern populations.

The genetic markers used in the last two decades have
changed, and there is an improved understanding of their
potential to answer the most important questions in con-
servation genetics. They include either mitochondrial
(mtDNA) or nuclear loci analyses, each with their advan-
tages and disadvantages (Avise 2004). Analyses of nuclear
DNA microsatellite loci have become an important ap-
proach for the conservation geneticist. This class of highly
variable repeated sequences, polymorphic and single locus
markers is routinely used to assess levels of genetic vari-
ability in small, endangered populations using non-inva-
sive samples, with important implications in conservation
biology. Because of their high mutation rates, microsatel-
lites can be excellent markers for studying genetically dep-
auperate populations, which show little or no variation at
allozyme loci or mitochondrial DNA. Moreover, because
of their short sequences, microsatellite loci can be ampli-



Table 1. Samples of feces collected from individuals of northern
muriqui populations.
Minimum Total of Percentage
Population population sampled of sampled
size individuals population
Espirito Santo
Santa Maria do 115 43 37.4
Jetiba
Capara6 National
Park
Minas Gerais
Caratinga Biological 226 130 57.5
Station
Serra do Brigadeiro 285 20 7.0
State Park
Rio Doce State Park 132 22 16.7
Serra do Ibitipoca 5 3 60.0
RPPN Mata do 42 10 23.8
Sossego


Neotropical Primates 13(Suppl.), December 2005

fied from degraded DNA, as often occurs when DNA is
obtained non-invasively from hair and scat samples.

Which rl.... 1. .;,.- and DNA segments are more appro-
priate to study is always subject to doubt. To answer this
question, it is necessary to look at the evolutionary proper-
ties of each class of DNA segment (mitochondrial or nucle-
ar, single or multiple copy, coding or non-coding sequence,
functional or non-functional) to evaluate the mutation rate
and forces that drive the evolutionary patch of each seg-
ment. In general, most molecular data have proved to sup-
port rather than contradict previous statements based on
other molecular markers. Nonetheless, the use of multiple
molecular markers allows for more accurate conclusions.

Genetic approaches to the study of reproductive and social
behavior
Developments in techniques of molecular genetics have
been widely used to address important issues in the biol-
ogy and behavioral ecology of mammal species (Woods
et al., 1999; Aitken et al., 2004). In particular, knowledge
of the current level of genetic variability and differentiation,
relatedness between individuals, extent of inbreeding, and
pedigree reconstructions are required to develop effective
strategies for the conservation of endangered populations.

Many of the demographic features of Brachyteles, such as
small and isolated populations, long inter-birth intervals,
slow maturation rates, and long and overlapping genera-
tions, make them vulnerable to the effects of genetic drift
and inbreeding, with the risks of lowering genetic variabil-
ity and viability (Strier, 2000; Strier et al., 2002). None-
theless, demographic data on the muriquis have not yet
revealed any evidence of deleterious signs of close inbreed-
ing. Reproductive rates have remained stable, and infant
mortality has been low in one group (Matao group) that
has been monitored since 1982 (Strier, 2000). Females
typically disperse from their natal groups prior to the onset
of puberty or sexual activity, thereby reducing the risks of
close inbreeding between siblings or father-daughter pairs
(Strier, 1996; Printes and Strier, 1999; Strier and Ziegler,
2000).

The mating patterns of northern muriquis at the EBC are
based on a system in which each female copulates with
several males during their peri-ovulatory periods (Strier,
1997). Although females generally mate with multiple
partners, copulations between mothers and their adult sons
are very rarely observed (Strier, 1997). Also, behavioral
observations have revealed a high tolerance of adult males
to all infants (Guimaraes and Strier, 2001). It is possible
that behavioral mechanisms for inbreeding avoidance have
contributed to the growth of the EBC muriqui popula-
tion, which has more than quadrupled in the past 24 years
(Strier et al., 2006b).

Because of the muriquis' promiscuous mating system, it is
impossible to determine the paternity of infants without





Neotropical Primates 13(Suppl.), December 2005

direct genetic data. Results from paternity studies can pro-
vide new insights into understanding muriqui mating be-
havior, and the relationship between adult male tolerance
toward infants and male-infant genetic relatedness.

Known as Short Tandem Repeats (STR) sequences, mic-
rosatellites have the potential to evaluate inter-individual
genetic variability. Microsatellite loci have been extensively
used to genotype samples of primates. Many of them, iso-
lated from the closely-related spider monkey (Ateles), can
also be used to genotype the northern muriqui (Di Fiore
and Fletcher, 2004). The use of heterologous primers is a
good strategy to initiate new investigations on endangered
species because the development of new primers of mic-
rosatellite DNA demands training, time and heavy finan-
cial investments. Heterologous primers were successful in
amplifying the DNA of black and brown bears (Lorenzini
et al., 2004). Also, tests of several human microsatellite loci
were positive and compatible in baboons (Morin et al.,
1998) and chimpanzees (Constable et al., 2001), and may
also be an option in muriqui studies.

Paternity and relatedness among members of northern
muriqui populations can be obtained from analyses of ge-
netic variability of STR sequence data. Analyses could be
conducted on infants and juveniles, their mothers and pos-
sible fathers. However, this approach is only possible in a
population such as that at the EBC, where data on paterni-
ty and genetic variation can be used to evaluate hypotheses
derived from long-term behavioral data.

Monitoring and Management of Populations

The Management Plan for Muriquis, proposed by Mendes
et al. (2005a), includes recommendations for monitor-
ing unknown populations, conducting long-term studies
of ecology and behavior, the reforestation of habitats in
order to facilitate dispersion of females, and reductions in
hunting and deforestation. Isolated groups and females in
muriqui populations would seem to be more frequently
observed in areas of highly fragmented forest. Transloca-
tion of reproductive individuals into potential receptor
groups is a difficult challenge, but it is necessary in order to
rescue the genetic variation represented by these individu-
als, which would otherwise die without leaving descend-
ants. Due to the relatively recent history of translocations
in muriqui (S. L. Mendes, pers. comm.), it is unknown
what effects they can have on the genetic structure of the
populations.

The problem of preserving the remaining wild popula-
tions is pertinent to concerns about the most appropriate
conservation and management units, such as Evolutionary
Significant Units (ESUs) and Management Units (MUs)
as defined by Waples (1991) and Moritz (1994). Distinct
MUs can be defined as populations connected by little or
no contemporary gene flow, but not separated historically
for very long periods of time (Waples, 1991).


The population viability of endangered species can be es-
timated based on demographic data (such as birth rates,
death rates, longevity, reproductive rates, effective popula-
tion size). Nonetheless, genetic studies of small populations
can provide fundamental evidence of how observed patterns
of mating and dispersion affect the loss of rare alleles within
and between groups. In addition, comparative genetic
studies can help to identify populations that are at such
high risk of extinction due to the loss of heterozygosity that
interventions (such as translocations) might be necessary.

The Muriqui Feces Bank

Most of the molecular genetic analyses of primates have
been restricted to DNA extracted from blood or tissue sam-
ples (Surridge et al., 2002), limiting the number of sam-
ples and risking the individuals due to anesthesia, capture
and handling. The quantity of material required for DNA
analyses may be infinitesimal using noninvasive methods,
which are essential to studies of endangered species. Hairs,
archeological or museum samples of pelts and bones, or
feces from wild subjects, for example, can be obtained non-
invasively. The first successful effort in isolating human
shed epithelial cells mixed with feces was performed by ly-
engar et al. (1991), and since then, studies in conservation
genetics using DNA from faecal samples have been carried
out on many threatened species.

The non-invasive technique of obtaining DNA from feces
to investigate the genetic variability of northern muriquis
has been applied in the past few years. DNA sampling
through feces is a reliable, efficient, and economic method,
which does not risk the physical integrity of the animals,
and furnishes enough DNA that is easily reproducible for
PCR amplification of fragments up to 800 bp in length
(Chaves et al., 2006). Also, it is a way of sampling a greater
number of individuals in nature than would be possible if
live captures to obtain blood were necessary.

At the same time, intensive fieldwork is needed to be able
to obtain reliable fecal samples from individuals in nature.
This may require long-term investment to habituate wild
animals to human presence. An extensive study involving
monitoring populations is the limiting factor in enabling
the collection of feces from individually-known animals.

Currently, the feces bank comprises samples of 230 indi-
viduals from seven out of twelve populations of northern
muriqui, all the result of extensive field studies (Table 1).
The bank represents still a minor percentage of the north-
ern populations, and a more coordinated and systematic
effort among fieldworkers at the different muriqui sites
is needed to achieve better representation across popula-
tions and species. Although the present studies are not as
complete as would be desirable, they represent a landmark
in the conservation genetics of free-living populations
of muriqui, since the lack of completeness of the data is







a situation that confronts all population geneticists and be-
havioral ecologists studying endangered species.

Acknowledgments

I thank the Brazilian Institute for the Environment (In-
stituto Brasileiro do Meio Ambiente e dos Recursos Naturais
Renovdveis- IBAMA) for the collecting license (363/2001),
and S. L. Mendes, P. B. Chaves, M. E Paes, K. B. Strier,
J. P. Boubli, C. B. Possamai, L. G. Dias, and the fieldwork
teams for making this work possible; L. P. Costa, K. B.
Strier and S. L. Mendes kindly reviewed this manuscript.
The Brazil Science Research Council (Conselho Nacional
do Desenvolvimento Cientifico e Tecnoldgico -CNPq), the
Ministry of the Environment (MMA-PROBIO), Critical
Ecosystem Partnership Fund (CEPF), and the Brazilian
Higher Education Authority (Coordenafao de Aperfeifoa-
mento de Pessoal de Nivel Superior- CAPES) provided fi-
nancial support.

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Neotropical Primates 13(Suppl.), December 2005


MANAGEMENT OF MURIQUIS (BRACHYTELES, PRIMATES) IN CAPTIVITY

Alcides Pissinatti

Centro de Primatologia do Rio de Janeiro (CPRJ/FEEMA), Caixa Postal 23011, Rua FonsecaTeles 1221, Sao Cristovao,
Rio de Janeiro, Brazil, e-mail:
Centro Universitirio Plinio Leite (UNIPLI), Niter6i, Rio de Janeiro, Brazil
Fundagao Educacional Serra dos Orgaos (FESO), Teres6polis, Rio de Janeiro, Brazil


Abstract

Muriquis are the largest of the Neotropical primates. Two forms are recognized today-Brachyteles arachnoides (E. Geoffroy,
1806), the southern muriqui with a black face, and Brachyteles .'-.... .-.'... (Kuhl, 1820), the northern muriqui with face
and genitalia mottled pink and black. They occur in eastern Brazil from the south of the state of Bahia to northern Parand.
The destruction, degradation and fragmentation of the Atlantic forest, along with hunting, are the reasons for their severely
threatened status today. In this article, I briefly describe the history of conservation efforts and research on muriquis. Cap-
tive breeding, although still incipient as an effective conservation measure, has been successful at the Rio de Janeiro Primate
Center (CPRJ/FEEMA) and the Curitiba Zoological Park, Parand. I discuss particularly aspects of breeding success, cage
design, colony formation, feeding and nutrition, diseases and the prevention and treatment of illnesses.


Key Words- primates, muriqui, Brachyteles, Atelidae, captive breeding, Atlantic forest


Introduction

Muriquis are the largest of the Neotropical primates. They
occur in southeastern Brazil, with recent discoveries of a
population in the state of Parand in the south (Koehler
et al., 2002, 2005), and reports of their existence in the
state of Bahia, to the far north. Their name comes from
the word "Myraqui," of the Tupi language. Its approximate
meaning is "people that swing as they come and go" and it
refers particularly to the large, pale brown monkeys that in-
habit forests along Brazil's Atlantic coast, initially assigned
the scientific name of Ateles i.' .-.'... by Wied-Neuwied
(1958).

Two forms are recognized today-Brachyteles arachnoides
(E. Geoffroy, 1806), the southern muriqui with a black
face, and Brachyteles .' .... .-'.. (Kuhl, 1820), the north-
ern muriqui with face and genitalia mottled pink and
black. The first author to consider the two forms distinct
was Vieira (1944), although he subsequently referred to
Brachyteles as a single species (Vieira, 1955). More recent
studies by Lemos de Sa and Glander (1993) confirmed
Vieira's initial suggestion, which had also been considered
byTorres deAssumpcao (1983) and Coimbra-Filho (1990,
1992a, 1992b).

Coimbra-Filho and Magnanini (1968) and Coimbra-Filho
(1972) noted the increasing scarcity of muriquis. How-
ever, only in 1982 was there international recognition of
the plight of Brachyteles, during a symposium on the con-
servation of primates in tropical forests held in Houston,
Texas, USA (Mittermeier et al., 1983). The most detailed


evaluation of the population and habitat status of Brach-
yteles was conducted by Aguirre (1971), but studies on this
taxon resumed only in the 1980s, with work by Fonseca
et al. (1983), Mittermeier et al. (1987), Nishimura et al.
(1988), Oliver and Santos (1991) and Strier (1992), whose
long-term research, begun in 1983, focused on the north-
ern form of Brachyteles, at the Fazenda Montes Claros, Car-
atinga, in Minas Gerais. Torres de Assumpcao (1983) and
Milton (1984) carried out some early studies of the south-
ern muriqui at the Fazenda Barreiro Rico, Sao Paulo, but
a long-term field research program was established (in the
Carlos Botelho State Park) only in the mid 1990s (Talebi
and Soares, 2005).

In the early 1980s, Russell A. Mittermeier, Chair of the
IUCN/Species Survival Commission (SSC) Primate
Specialist Group (PSG), and then Director of Primate
Programs at the World Wildlife Fund-US, began work-
ing in close collaboration with researchers at the Rio de
Janeiro Primate Center (Centro de Primatologia do Rio de
Janeiro- CPRJ/FEEMA), the Zoology Department of the
Federal University of Minas Gerais (UFMG), the Brazilian
Forestry Institute (Instituto Brasileiro de Desenvolvimento
Florestal- IBDF), and a non-governmental organization
(NGO), the Brazilian Foundation for Nature Conserva-
tion (Fundafdo Brasileira para Conservafdo da Nature-
za-FBCN) in Rio de Janeiro, to identify the most im-
portant federal and state reserves protecting remnants of
the Atlantic forest and its rich endemic fauna (Mittermeier
et al., 1982). The WWF-US project included three areas of
investigation. One concerned the nonhuman primates and







other large mammals, another the avifauna, and the third
the vegetation and flora.

The Endemic Primates of the Atlantic Forest

The status of the primate species in the region was studied
in great detail, with the aim of assessing their populations
and habitats. In the first phase, emphasis was given to the
most threatened-the muriquis (Brachyteles), and the
lion tamarins (Leontopithecus rosalia, L. chrysomelas, and
L. chrysopygus) (L. caissara was only discovered in 1990).
Hunting and the widespread destruction and degradation
of their forests are the principal causes of threat.

Twenty-four species and subspecies of nonhuman pri-
mates occur in the Atlantic forest. Twenty of them are
endemic, and 17 are found in the southeast-the states
of Sao Paulo, Rio de Janeiro, Espirito Santo, the eastern
portion of Minas Gerais and the southern part of the state
of Bahia, below the Rio de Contas. We consider this area
critical because it is where most of the remaining forests
still exist, and because it is where the Pleistocene forest ref-
ugia are thought to have been concentrated (Kinzey, 1982;
Rylands et al., 1996). Of the 17 species and subspecies of
nonhuman primates in southeastern Brasil, 14 are endem-
ic and only encountered in this region. As indicated by the
field investigations conducted by the Primate Program or-
ganized by WWF-US/CPRJ-FEEMA, at least 13 of these
forms are seriously endangered and two are vulnerable.
Some of the endangered primates were even considered on
the verge of extinction.

Muriquis (Brachyteles) are one of the most endangered non-
human primates in southeastern Brazil, and are also con-
sidered to be amongst the most threatened primates in the
world (Strier et al., 2006). Altogether, the total population
of B. .'.i... .-.'... is estimated at 864 individuals, and for
B. arachnoides the estimate is 1300 individuals (Melo and
Dias, 2005) which, for both species, live precariously in
few remaining forests, mostly degraded and isolated.

The original habitat of B. arachnoides and B. .'... .-.'...
is primary forest, or late successional and mature forest to
be more precise. Few forests remain that provide adequate
habitat for the muriquis. They are always a target for hunt-
ers that further reduces their populations, even in state and
federal protected areas. Improving the management and
policing of these reserves and parks, would be a very posi-
tive measure for their long-term protection.

Unlike the three species of Leontopithecus that benefit from
highly organized and effective captive breeding programs,
there are very few muriquis in captivity. There are small
colonies in the Centro de Primatologia do Rio de Janeiro
(CPRJ/FEEMA) and the Parque Zool6gico de Curitiba,
where they have been bred successfully.


Neotropical Primates 13(Suppl.), December 2005

The Captive Breeding Program

The existence of a Primate Center in the region where
Brachyteles occurs made it possible to establish an ex situ
breeding project to support an integration of field and cap-
tive management, following the example established and
functioning for Leontopithecus. Despite the critical status
of the two species, only a few individuals were maintained
in public or private institutions in the past, and without
any pretensions to a structured breeding program. It fell
to the Centro de Primatologia the historic task of repro-
ducing this rare species in captivity (Coimbra-Filho et
al., 1993). Animals kept by a Swiss Animal dealer, Marco
Schwarz, were transferred to the Parque Zool6gico de Cu-
ritiba, which has also had success with their reproduction.
The Fundagao Parque Zool6gico de Sao Paulo, Orquidario
de Santos, Parque Zool6gico Quinzinho Barros, Museu de
Biologia Mello Leitao (Ruschi, 1964) have all maintained
this primate, but without establishing a breeding nucleus.
Perhaps, as Crandall (1964) and Aguirre (1971) thought,
and even today for many others, the maintenance and re-
production of these primates ex situ represents a difficult
and uncertain challenge.

Conditions in captivity
Captive management is one of the alternatives for the pres-
ervation of species threatened with extinction. In these
man-made environments, it is necessary to utilize specific
knowledge to develop plans for the areas and people, as
well as the animals involved. These plans must take into
consideration the principals of functionality, hygiene, and
security. Enclosures must be sufficiently large, and contain
high quality space suitable for the species. Other specific
considerations that must be taken into account in the con-
struction of enclosures include:

* Protection against predators
* Exposure to the sun's rays, preferably in the morning
* Avoidance of large fluctuations in temperature and
humidity
* Access to shade
* Minimization of contact with feces, urine, and food
remains
* Sheltered areas, as necessary.

In addition to the preparation of areas for the temporary
isolation of individuals when needed, there must also be:

* Storage areas for both non-perishable and perishable
foods (controlled refrigeration)
* Storage areas for equipment and materials used in the
colony
* Storage for any hazardous materials and food wastes
* Medical-veterinary supplies and storage
* An area to maintain and store data
* A hygienic area for the workers and other people
involved in the management of the colony





Neotropical Primates 13(Suppl.), December 2005

* An area for washing and disinfecting equipment,
cages, etc.

Colony formation
Ex situ reproduction should begin with a founding popu-
lation that is of high quality in every aspect. This unfor-
tunately was not the case with the colony at the CPRJ-
FEEMA, as shown by Coimbra-Filho et al. (1993), and in
Table 1. Nonetheless, we have had notable breeding success
in a period of only five years. Ideally, captive breeding ini-
tiatives would have a colony of healthy animals of the ap-
propriate sexes and ages, and the behavior of which has not
been influenced by humans and, most especially, negative
social experiences. These factors, along with dietary man-
agement and sanitary medicine, could result in successful


reproduction. However, the Centro de Primatologia has
received confiscated animals many of which were in terri-
ble condition on their arrival (Coimbra-Filho et al., 1993).
Some even died soon after arriving (Table 1), while others
presented health risks to the rest of the colony. Some of
the individuals that developed an aversion to the food they
were presented ultimately recovered over time (CP 891, CP
924, CP 2049, CP 2097). Others died quickly (CP 2047 e
CP 2050) (Table 1), despite every effort and care.

Feeding and nutrition
Special care in the choice of food and in the preparation
of the diets for these monkeys is necessary. Knowing the
fondness that muriquis have for Garapa (Apuleia leiocarpa)
and for Jacarandi-branco (T' .-, .7.. '. elegans) leaves, we


Table 1. Breeding and Management of captive muriquis, Brachyteles, at the Centro de Primatologia do Rio de Janeiro (CPRJ-FEEMA).
Local Date of arrival Date of
Species Sex Origin number (A) or birth (B) Locale Father Mother death Tatoo Experience Cause of death
Number (A) or birth (B) _death
B. lypoxanthus F W 850 A 11 Sep 87 CPRJ WB WB 25 Jun 90 A 1 NOX Multiple lesions;
peritonitis
associated with
Strongyloides
B. hypoxanthus F W 891 A 12 Jan 88 CPRJ WB WB 11 Oct 96 A 2 IE 2(2) B Serious internal
2(2) hemorrhage
B. hypoxanthus F W 924 A 18 Jul 88 CPRJ WB WB 25 Jul 97 A 3 IE 2(2) B Enteritis and
3(3) anorexia
B. arachnoides M W 1012 A 24 May 89 CPRJ WB WB Transfer to A 4 IE 4(4) B Hepatitis B
Rio Zoo 1(1)
(12 Mar 99)
B. arachnoides M W 1091 A 5 Jan 90 CPRJ WB WB A 5 B 4(4)
Hybrid F C 1245 B 10 Sep 91 CPRJ 1091 MS 924 FS 12 Sep 91 NOX Birth difficulties;
ruptured lung vessel
Hybrid F C 1286 B 30 Oct 91 CPRJ 1091 MS 891 FS Chip IE 1(1)
2558
Hybrid F C 1335 B 3 Jun 92 CPRJ 1091 MS 924 FS 4 Jun 98 IE 2(2) Festering abscess
of abdominal wall;
peritonitis
B. arachnoides M W 1407 A 21 May 93 CPRJ WB WB 4 Dec 96 NOX Hepatitis B
Hybrid C 1430 B 12 Oct 93 CPRJ 1091 MS 924 FS 12 Oct 93 NOX Dead at birth
Hybrid M C 1475 B 25 Apr 94 CPRJ 1091 MS 891 FS CHIP IE 3(3)
9539
Hybrid M C 1488 B 24 Jun 94 CPRJ 1091 MS 924 FS Transfer to 1488 IE 2(2) Hemorrhagic
Rio Zoo enteritis
(12 Mar 99)
B. arachnoides F W 1528 A 20 Dec 94 CPRJ WB WB 13 Jul 95 NOX Anorexia, general
infection
Hybrid M C 1671 B 8 Jun 96 CPRJ 1012 MS 924 FS 11 Oct 98 IE 1(1) Enteritis
Hybrid M C 1689 B 7 Sep 96 CPRJ 1012 MS 891 FS 25 Sep 96 NOX Exhaustion due to
mother's illness
B. hypoxanthus F W 2047 A 22 Jan 02 CPRJ WB WB 21 Jun 02 NOX Anorexia, enteritis
B. arachnoides F W 2049 A 6 Feb.02 CPRJ WB WB NOX
B. arachnoides M W 2050 A 14 Mar 02 CPRJ WB WB 22 Mar 02 NOX Serious intestinal
lesions and
Strongyloides
B. hypoxanthus F W 2097 A 13 Nov 02 CPRJ WB WB NOX

Legend: WB Wild born, W Wild, C Captivity, NOX None, IE L Infant experience, B Breeder







planted them nearby. This was enormously beneficial for
the recovery of these animals when brought to us in poor
health (Coimbra-Filho et al., 1993). Those that were res-
cued were generally reluctant to accept artificial food, or
even wild foods that were not part of their accustomed
diet. New foods must be introduced carefully, with vari-
ety, to break the monotony of the diet and to stimulate
their digestive tracts. Milton (1984), Strier (1991), and
Moraes (1992) made important observations on the diet
of Brachyteles in the wild that indicate appropriate recipes
in captivity.

In general, primates with strongly folivorous diets are more
difficult to maintain in captivity, mainly because of the dif-
ficulty of obtaining a diversity of appropriate foods to offer
them. Owing to the enviable location of the CPRJ-FEE-
MA, we were able to overcome these difficulties, a factor
certainly contributing to our success in breeding them.
Animals that had been kept as pets had, in general, been
accustomed to very bizarre diets (the case of the individu-
als CP 1528 and CP 2047, for example), which made the
process of adapting them to a diet more typical of their
natural needs more difficult. To illustrate the complications
of adjusting their feeding regime, we relate the story of one
individual (CP 1528) that had been maintained on entirely
inadequate foods.

To stimulate this individual to eat a new diet, she was
housed in an enclosure that was adjacent to that of the
resident muriqui group. There, she could observe, vocalize
and interact with the other muriquis, and become famil-
iar with their diets. Over time, with little or nothing to
eat, we decided to release her with the others, where she
was well-received. Under these conditions, she ate few of
the new food items, and in very small quantities, which
probably lowered her physical resistance. She contracted a
respiratory illness, and later had gastrointestinal problems.
Although experiencing a long period of improvement,
during which she received various medications, she eventu-
ally died.

The acceptance of food can be improved by adopting an
appropriate feeding strategy. The muriquis fight over veg-
etation if we offer it to them in small quantities, but when
offered as a large branch with numerous leaves, the muri-
quis feed together peacefully, as has been observed in the
wild. They remain peaceful while feeding and vocalizing, as
if they were satisfied with the food. Offering natural vegeta-
tion instead of supermarket foods is a more adequate diet
for these primates in captivity.

Breeding- evolution of the colony
The breeding colony at the Centro de Primatologia do
Rio de Janeiro originated with two females (CP 891 and
CP 924), both B. ..;.. . and two males (CP 1012 and
CP 1091), both B. arachnoides. The two males arrived very
young, but were in better condition than the females. The
contributions of male CP 1091 and of female CP 924 were


Neotropical Primates 13(Suppl.), December 2005

Table 2. Contribution of males (Brachyteles arachnoides) and fe-
males (Brachyteles ', I in the reproduction of muriquis
in captivity at the CPRJ/FEEMA.
Males Females Birth
B. arachnoides B. hypoxanthus Offspring Sex conditions
1091 x 924 1245 F D
1335 F T
1430 ? D
1488 M D
891 1286 F T
1475 M T
1012 x 924 1671 M T
891 1689 M D

Legend: D = Difficult birth; surgery necessary, T = Full-term (normal)


greater than those of male CP 1012 and female CP 891.
Births were problematic in 50% of the cases, as shown in
Table 2, emphasizing the precarious history of these fe-
males as "pets," which had resulted in developmental prob-
lems with their pelvic bones and subsequent complications
during parturition (Table 2). Under these conditions, there
are always concerns with the female and the offspring. The
possibility of success is uncertain.

Prevention and treatment of illnesses
Various studies provide detailed coverage of pathologies
associated with primates, with those by Ruch (1959), Ap-
pleby et al. (1963), Fiennes (1967, 1972), Martin (1986),
and Brack (1987) being of particular relevance. Preventive
medicine is fundamental for the good health of the colony.
It is also necessary to protect researchers from illness and
death due to direct or indirect contact with pathogens
transmitted by primates (Whitney Jr., 1976; Brack, 1987;
Dalgard, 1991; Adams etal., 1995; Butler etal., 1995).

Many illnesses can attack primates in the wild and in cap-
tivity, the latter exacerbated through direct contact with
humans. When different species are put together, there
is also the possibility that one will pass serious diseases to
the others. For example, Herpesvirus tamarinus is latent
in Saimiri, but fatal in Aotus and Saguinus (Holmes et al.,
1964; Melendez et al., 1966; Hunt et al., 1973) as well as
in other species. Conversely, Herpesvirus hominis is latent
in humans, but fatal for Aotus and Hylobates (Smith et al.,
1969).

Very little has been written about the pathologies of muri-
quis. Works by Artigas (1935), Travassos (1943), Stuart
et al. (1993), and Pissinatti et al. (1997) remain the best
sources on their parasites. There has been a prevalence of
intestinal problems associated with the deaths of muriquis
in captivity, where the presence of Strongyloides sp. is
marked, despite the sanitary medical controls employed
(Pissinatti et al., 1997). Strongyloides has been the cause of
deaths among the individuals received and maintained at
the Center (Table 1).





Neotropical Primates 13(Suppl.), December 2005

The conservation status of the muriqui continues to be criti-
cal, despite the many studies conducted to date. It was only
18 years after the first intensive field studies on muriquis
that the first "Population and Habitat Viability Assessment
Workshop for the Endangered Muriqui. Brachyteles arach-
noides" was held, and where some recommendations for the
conservation of the species were established (Rylands et al.,
1998). From this meeting until present, ongoing studies
have continued at Caratinga and surrounding areas, as well
as in the state of Sao Paulo, and at the Centro de Primato-
logia, where efforts to extend the captive breeding project
have resulted in the approval of three enclosures (similar to
the one already built) as part of the compensatory meas-
ures resulting from the Programa de Despoluifdo da Baia de
Guanabara (PDBG). Construction of two more enclosures
has been approved as part of the project of the surrounding
the Paraiso State Ecological Station. All of the approved
resources for these enclosures are embargoed, however, due
to unrelated administrative and political issues.

Recently, the Brazilian Institute for the Environment (Ins-
tituto Brasileiro do Meio Ambiente e dos Recursos Naturais
Renovdveis-IBAMA) and the research group working
at the Serra dos Orgaos National Park initiated a census
of the muriqui population. Two workshops were organ-
ized by this "Programa Muriqui", through a partnership
of IBAMA/TEREVIVA. They culminated in the creation
of the International Committee for the Conservation and
Management of the Muriqui/Woolly Spider Monkey
(B. arachnoides and B. .'.... .-.'... (Edict 1.369/02 of
10 October 2002- IBAMA)-an international commit-
tee of the government specifically to discuss the two species
and provide advice and coordinated direction for research,
conservation and captive management measures on their
behalf (Oliveira et al., 2005). We believe that the best and
most important actions on behalf of this extraordinary pri-
mate can be executed now that all of the necessary legal
instruments for implementing them exist.

Acknowledgments

The Wildlife Preservation Trust International (WPTI)
provided funding for the construction of the enclosure for
muriquis. The Zoological Society of Philadelphia, Conser-
vation International (CI), the Jersey Wildlife Preservation
Trust (JWPT), the American Zoological and Aquarium
Association (AZA), the Greater Los Angeles Zoo Associa-
tion, IBAMA-DF and IBAMA-BH, Zoology Department
of the Federal University of Minas Gerais (UFMG), Parque
Ecol6gico Turistico Alto Ribeira (PETAR), Orquidirio de
Santos, Federal University of Vigosa, the Rio de Janeiro
State Research Support Foundation (Fundafdo de Amparo
d Pesquisa do Estado do Rio de Janeiro FAPERJ) (Proc.
E-26/171.573/00), and the Ministerio Ptblico Federal pro-
vided fundamental help during the muriqui project. We
appreciate the support of Braz Cosenza, Lucio Leoni, Rosa
Lemos de Sa, Milton Thiago de Mello, Russell A. Mit-
termeier, Andy Baker, Anthony B. Rylands, Adelmar E


Coimbra-Filho and Sonia Maria Eduardo de Franga. Our
thanks to Karen B. Strier for her kindness in translating
this paper.

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