Edited by
Devra G. Kleiman and Anthony B. Rylands
Smithsonian Institution Press, 2002
FROM THE DUST JACKET
Without the extraordinary efforts of the editors and authors of this book,
three of the four lion tamarin species (golden, golden-headed, black-faced,
and black) would most likely be extinct. The contributors' hard work set
international standards and became the model for the preservation of other
endangered species. There is, of course, still much to be done, and this
comprehensive assessment of research findings and conservation efforts
leads the way.
The first section of the book covers the history and framework of research
and conservation for the four species, stressing the importance of both
group and individual efforts. Part Two examines the principal studies that
have played important roles in contributing to the management of the
species in captivity and the wild; the authors maintain that there is no
substitute for long-term data and good science when developing recovery and
conservation programs. Part Three focuses on direct interventions to
conserve wild populations and their habitats as guided by scientific and
educational principles.
Kleiman and Rylands close the book by noting the remarkable accomplishments
of lion tamarin conservation as they look hopefully toward future
directions and challenges.
About the Editors
Devra G. Kleiman is a research associate at the Smithsonian National
Zoological Park and coeditor of Wild Mammals in Captivity: Principles and
Techniques (I997).
Anthony B. Rylands is senior director for conservation biology at the
Center for Applied Biodiversity Science, Conservation International in
Washington, D.C., and editor of Marmosets and Tamarins: Systematics,
Behaviour, and Ecology (I993).
TABLE OF CONTENTS
Contributors x
Foreword xv
RUSSELL A. MITTERMEIER
Introduction and Acknowledgments xix
Acronyms xxiv
PART ONE: THE HISTORY AND STATUS OF LION TAMARINS
l . A History of Lion Tamarin Research and Conservation 3
ANTHONY B. RYLANDS, JEREMY J. C. MALLINSON, DEVRA G. KLEIMAN, ADELMAR F.
COIMBRA-FILHO, RUSSELL A. MITTERMEIER, IBSEN DE GUSMAO CAMARA, CLiUD10 B.
VALLADARES-PADUA, AND MARIA IOLITA BAMPI
2. Distribution and Status of Lion Tamarins 42
ANTHONY B. RYLANDS, MARIA CECILIA M. KIERULFF, AND LUIZ PAULO DE SOUZA PINTO
3. The Role of Nongovernmental Organizations and the International
Committee for the Conservation and Management of Leontopithecus in Lion
Tamarin Conservation 71
DENISE MARCAL RAMBALDI, DEVRA G. KLEIMAN, JEREMY J. C. MALLINSON, LOU ANN
DIETZ, AND SUZANA M. PADUA
4. History, Management, and Conservation Role of the Captive Lion Tamarin
Populations 95
JONATHAN D. BALLOU, DEVRA G. KLEIMAN, JEREMY J. C. MALLINSON, ANTHONY B.
RYLANDS, CLAUDIO B. VALLADARES-PADUA, AND KRISTIN LEUS
PART TWO: THE BIOLOGY OF LION TAMARINS
5. Genetics and Evolution of Lion Tamarins 117
HECTOR N. SEUANEZ, ANTHONY Dl FIORE, MIGUEL ANGELO M. MOREIRA, CARLOS
ALBERTO DA S. ALMEIDA, AND FLAVIO C. CANAVEZ
6. Lion Tamarin Reproductive Biology 133
JEFFREY A. FRENCH, KRISTEL DE VLEESCHOUWER, KAREN BALES,
AND MICHAEL HEISTERMANN
7. Behavioral Ecology of Lion Tamarins 157
MARIA CECILIA M. KIERULFF, BECKY E. RABOY, PAULA PROCOPIO DE OLIVEIRA,
KIMRAN MILLER, FERNANDO C. PASSOS, AND FABIANA PRADO
8. Mating System and Group Dynamics in Lion Tamarins 188
ANDREW J. BAKER, KAREN BALES, AND JAMES M. DIETZ
9. Infant Care in Lion Tamarins 213
SUZETTE D. TARDIF, CRISTINA V. SANTOS, ANDREW J. BAKER, LINDA VAN ELSACKER,
ANNA T. C. FEISTNER, DEVRA G. KLEIMAN, CARLOS R. RUIZ-MIRANDA, ANTONIO
CHRISTIAN DE A. MOURA, FERNANDO C. PASSOS, ELUNED C. PRICE, LISA G.
RAPAPORT, AND KRISTEL DE VLEESCHOUWER
10. Conspicuousness and Complexity: Themes in Lion Tamarin Communication 233
CARLOS R. RUIZ-MIRANDA AND DEVRA G. KLEIMAN
l1. Diseases of Lion Tamarins 255
ALCIDES PISSINATTI, RICHARD J. MONTALI, AND FAICAL SIMON
PART THREE: CONSERVATION AND MANAGEMENT OF LION TAMARINS IN THE WILD
12. Reintroduction and Translocation as Conservation Tools for Golden
Lion Tamarins 271
MARIA CECILIA M. KIERULFF, PAULA PROCOPIO DE OLIVEIRA,
BENJAMIN B. BECK, AND ANDREIA MARTINS
13. The Effects of Prerelease Environments and Postrelease Management on
Survivorship in Reintroduced Golden Lion Tamarins 283
BENJAMIN B. BECK, MARIA INKS CASTRO, TARA S. STOINSKI, AND JONATHAN D. BALLOU
14. Metapopulation Management for the Conservation of Black Lion
Tamarins 301
CLAUDIO B. VALLADARES-PADUA, JONATHAN D. BALLOU, CRISTIANA SADDY MARTINS,
AND LAURY CULLEN, JR.
15. In Situ Conservation Education and the Lion Tamarins 315
SUZANA M. PADUA, LOU ANN DIETZ, DENISE MARCAL RAMBALDI, MARIA DAS GRACAS DE
SOUZA, AND GABRIEL RODRIGUES DOS SANTOS
16. Lion Tamarin Biology and Conservation: A Synthesis and Challenges for
the Future 336
DEVRA G. KLEIMAN AND ANTHONY B. RYLANDS
References 345
Index 407
FORWARD
The first field observations of lion tamarins were made by the amazing
German naturalist Prince Maximilian zu Wied, who traveled through the
Atlantic Forest region of Brazil in the early nineteenth century. At that
time he described the golden lion tamarin and golden-headed lion tamarin as
common, but unfortunately their numbers in the wild declined dramatically
in the second half of the twentieth century. With the rapid economic growth
of Brazil beginning in the 1960s, most marked in the Atlantic Forest
region, there has been large-scale conversion of forest to cattle pasture,
agricultural land, and plantation forestry, and the lion tamarins have been
squeezed into smaller and smaller forest patches.
The first to call attention to this in Brazil was Adelmar F. Coimbra-Filho,
the pioneer of Brazilian primatology and one of the great leaders of
primatology for the entire neotropical region. With his colleague Alceo
Magnanini, he carried out fieldwork on the golden lion tamarin in the 1960s
and wrote of its plight in the latter half of that decade. In 1969 and
1970, he rediscovered the black, or golden-rumped, lion tamarin in the
Morro do Diabo State Reserve in Sao Paulo, which had not been seen in 65
years. Although his discoveries were published in the latter part of 1970,
they received little international attention since they were in Portuguese.
In 1970, I had just finished my undergraduate work at Dartmouth College and
had spent 3 months working on the mantled howler monkey on Barro Colorado
Island in Panama. Having decided to work on Neotropical primates for my
Ph.D., I met with Barbara Harrisson, founder, and then chair, of the IUCN's
Species Survival Commission Primate Specialist Group. Barbara encouraged me
to go to Brazil and showed me Coimbra's papers on the lion tamarins.
Although I could not yet read Portuguese, I struggled through them with my
Spanish and wound up fascinated with how little was known about these
wonderful little creatures.
About 6 months later, in duly 1971, I appeared on Coimbra's doorstep in Rio
de Janeiro, speaking the rudimentary Portuguese that I had learned over the
past few weeks traveling by boat and bus from the Brazilian Amazon down to
Rio. We struck up an immediate friendship that has lasted for three decades
and has been one of the most productive of my career. Our discussions of
primate conservation laid the groundwork for a series of activities over
the next decade, including publication of his early lion tamarin work in
English and the need to carry out primate surveys in the Atlantic Forest
and Amazonia.
On the international end, there was growing concern about the declining
number of captive golden lion tamarins in the United States and Europe
following articles published by John Perry (Smithsonian National Zoological
Park [SNZP], Washington, D.C.) and Clyde Hill (San Diego Zoo). This led to
the historic conference, in February 1972, entitled "Saving the Lion
Marmoset," which was organized by the late Don Bridgwater, then of the
Minnesota Zoo, Bill Conway of the New York Zoological Society (now the
Wildlife Conservation Society), and John Perry. The meeting was held in a
backroom behind the cafeteria at the SNZP and laid the groundwork for
almost everything else that followed. As a result of this meeting, Devra
Kleiman assumed coordination of the captive golden lion tamarin population,
which proved amazingly successful, increasing the numbers from about 70 to
a controlled 500.
Taking advantage of the international interest in the conference and with
some seed money from the World Wildlife Fund (WWF), in 1973, Coimbra and
Magnanini, were successful in establishing a captive breeding facility: the
Lion Tamarin Biological Bank at the edge of Tijuca National Park in Rio de
Janeiro. There, Coimbra began the first colony of black lion tamarins, with
six individuals from the Morro do Diabo State Reserve, and the following
year, he and Magnanini were also successful in establishing the Poco das
Antas Biological Reserve in the lowlands of Rio de Janeiro. International
interest was further generated by a second callitrichid conference
organized by Devra Kleiman in 1975 (Kleiman, 1978). A third meeting was
hosted by Hartmut Rothe, Jurgen Wolters, and John Hearn in 1977 in
Gottingen, Germany (Rothe et al. 1978). "The Marmoset Workshop" added an
important European dimension, giving the lion tamarins even more status as
flagship species for the Atlantic Forest. As a result of these meetings,
Coimbra was again able to leverage on-the-ground conservation action, this
time resulting in the creation of the Una Biological Reserve for the
golden-headed lion tamarin in 1980.
In 1973 and 1974, the first major primate survey of Brazilian Amazonia and
a multiyear survey, entitled "Conservation of Eastern Brazilian Primates"
(funded by WWF-U.S.), which Coimbra and I had discussed when we first met,
became a reality. It had many subcomponents, including the groundbreaking
study of the golden-headed lion tamarin by Anthony Rylands in 1980, the
initiation of the long-term efforts of Claudio and Suzana Padua on the
black lion tamarin in the mid-1980s, and the first survey of the golden
lion tamarin since Coimbra's early research-a 1980 study by Ken Green. The
WWF program also helped to lay the groundwork for the SNZP-based field
program on the golden lion tamarin (I was able to introduce Devra Kleiman
to her first wild golden lion tamarin in the POCO das Antas Biological
Reserve in 1982), as well as the field surveys of Ilmar Santos, Cristina
Alves, Luiz Paulo Pinto, and Cecilia Kierulff. Perhaps most importantly,
this program was instrumental in placing the Atlantic Forest high on the
agenda of major international conservation organizations-to the point that
it is now recognized as one of the top five biodiversity "Hotspots" on
Earth (Mittermeier et al. 1999a, l999b).
Another watershed event was the establishment in 1981 of the first
Management Committee for the Golden Lion Tamarin, chaired by Devra Kleiman
and initially intended for the management of the captive population.
Committees followed for the other species: a golden-headed lion tamarin
committee, chaired by Coimbra and Jeremy Mallinson, director emeritus of
the Durrell Wildlife Conservation Trust (then the Jersey Wildlife
Preservation Trust), and one for black lion tamarins, chaired by Faical
Simon of the Sao Paulo Zoo and Devra Kleiman. The Instituto Brasileiro do
Meio Ambiente e dos Recursos Naturais Renovaveis (IBAMA-Brazilian Institute
of the Environment and Renewable Natural Resources) officially recognized
the committees in 1990, which became models of international collaboration
on behalf of endangered species. Special recognition for making this happen
must go to Maria lolita Bampi, general coordinator for fauna, Directorate
of Wildlife and Fisheries of IBAMA, who has long been the government's
representative on these key structures. Then, in 1990, came one of the
biggest surprises in primatology in the last quarter century: a "newcomer"
to the lion tamarin world. The black-faced lion tamarin was discovered by
two Brazilian researchers, Maria Lucia Lorini and Vanessa Persson, on the
island of Superagui in the state of Parana. This exciting new find amazed
all of us, reminding us how little we know of the world's biodiversity.
All in all, I think it fair to say that the international effort of the
past 30 years on behalf of the lion tamarins of Brazil represents one of
the great success stories in the global conservation movement. Together
with the muriquis (Brachyteles spp.), they have long been the flagship
species for this critically important "Hotspot," and without the lion
tamarins it is doubtful that this region would have received the attention
that it has. Like the giant panda in China, the orangutan and the Sumatran
rhino in Indonesia, and the lemurs in Madagascar, the lion tamarins have
been the international ambassadors for their forest home. Although we
cannot afford to be complacent, I am very optimistic about the future of
the lion tamarins and the Atlantic Forest as a whole. The lion tamarin
effort has set high international standards and has been a model for the
development of similar efforts around the world. By summarizing all the
good work that has taken place, the editors, Devra Kleiman and Anthony
Rylands, and all the authors in this book have made a great contribution to
biodiversity conservation and have really helped us in the great challenges
that we face over the next couple of decades. Without their dedication,
their commitment, and their many sacrifices, the lion tamarins would
probably be close to extinction today. Instead, they represent one of our
greatest reasons for hope in the saving of the earth's biodiversity.
Finally, I am very pleased that this book has been dedicated to one of the
world's greatest ecoheroes, Dr. Adelmar F. Coimbra-Filho. Without Coimbra,
none of what is recounted in the pages that follow would have been
possible. He has been a pioneer, a leader, a visionary, and a great
spokesman for conservation for nearly half a century and is deserving of
our greatest respect and admiration. I am proud to call him one of my
closest friends and am honored that he saw fit to involve me in this noble
effort so long ago.
-RUSSELL A. MITTERMEIER
PRESIDENT, CONSERVATION INTERNATIONAL
CHAIRMAN, IUCN/SSC PRIMATE SPECIALIST GROUP
CONTRIBUTORS
Carlos Alberto da S. Almeida
Secao de Genetica
Instituto Nacional de Cancer
Praca da Cruz Vermelha 23
20230-130 Rio de Janeiro
Rio de Janeiro, Brazil
Andrew J. Baker
Philadelphia Zoological Garden
3400 West Girard Avenue
Philadelphia, PA 19104, USA
Karen Bales
Department of Psychiatry
University of Illinois at Chicago
1601 W Taylor Street, Room 436
Chicago, IL 60612, USA
Jonathan D. Ballou
Department of Conservation Biology
National Zoological Park
Smithsonian Institution
Washington, DC 20008, USA
Maria lolita Bampi
Departamento de Vida Silvestre
Diretoria de Ecossistemas
Instituto Brasileiro do Meio Ambiente e
dos Recursos Naturais Renovaveis
(IBAMA)
SAIN Avenida 14 Norte
Edificio Sede
70800 Brasilia, DF, Brazil
Benjamin B. Beck
National Zoological Park
Smithsonian Institution
Washington, DC 20008, USA
Ibsen de Gusmao Camara
Avenida das Americas 2300-C40
Barra da Tijuca
22640-101 Rio de Janeiro
Rio de Janeiro, Brazil
Flavio C. Canavez
Secao de Genetica
Instituto Nacional de Cancer
Praca da Cruz Vermelha 23
20230-130 Rio de Janeiro
Rio de Janeiro, Brazil
Maria Ines Castro
Conservation International
1919 M Street, NW
Washington, DC 20036, USA
Adelmar E Coimbra-Filho
Rua Artur Araripe 60/901
Gavea
22450-020 Rio de Janeiro
Rio de Janeiro, Brazil
Laury Cullen, Jr.
Instituto de Pesquisas Ecologicas (IPE)
Caixa Postal 47
12960-000 Nazare Paulista
Sao Paulo, Brazil
Kristel De Vleeschouwer
Center for Research and Conservation
Royal Zoological Society of Antwerp
Koningin Astridplein 26
B-2018 Antwerp, Belgium
James M. Dietz
Department of Zoology
University of Maryland
College Park, MD 20742, USA
Lou Ann Dietz
World Wildlife Fund
1250 24th Street NW, Room 5047
Washington, DC 20037-1132, USA
Anthony Di Fiore Department of Anthropology and New
York Consortium in Evolutionary
Primatology (NYCEP)
New York University
25 Waverly Place
New York, NY 10003, USA
Anna T. C. Feistner
Durrell Wildlife Conservation Trust
Les Augres Manor
Trinity
JerseyJE3 5BP
Channel Islands, British Isles
Jeffrey A. French
Department of Psychology
University of Nebraska at Omaha
Omaha, NE 68182-0274, USA
Michael Heistermann
Department of Reproductive Biology
German Primate Center
Kellnerweg 4
D-37077 Gottingen, Germany
Maria Cecilia M. Kierulff
Conservation International do Brasil
Rua Major Homem Del Rey 147
Cidade Nova
45650-000 Ilheus
Bahia, Brazil
Devra G. Kleiman
Department of Conservation Biology
National Zoological Park
Smithsonian Institution
Washington, DC 20008, USA
Kristin Leus
Center for Research and Conservation
Royal Zoological Society of Antwerp
Koningin Astridplein 26
B-2018 Antwerp, Belgium
Jeremy J. C. Mallinson
Durrell Wildlife Conservation Trust
Les Augres Manor
Trinity
JerseyJE3 5BP
Channel Islands, British Isles
Andreia Martins
Associacao Mico-Leao-Dourado
Caixa Postal 109.968
28.860-000 Casimiro de Abreu
Rio de Janeiro, Brazil
Cristiana Saddy Martins
Instituto de Pesquisas Ecologicas (IPE)
Caixa Postal 47
12960-000 Nazare Paulista
Sao Paulo, Brazil
Kimran Miller
Department of Biology
University of Maryland
College Park, MD 20742, USA
Russell A. Mittermeier
Conservation International
1919 M Street, NW
Washington, DC 20036, USA
Richard J. Montali
National Zoological Park
Smithsonian Institution
Washington, DC 20008, USA
Miguel Angelo M. Moreira
Secao de Genetica
Instituto Nacional de Cancer
Praca da Cruz Vermelha 23
20230-130 Rio de Janeiro
Rio de Janeiro, Brazil
Antonio Christian de A. Moura
Departarnento de Sistematica e Ecologia-
CCEN
Universidade Federal de Paraiba
58.059-9OOJdo Pessoa
Paraiba, Brazil
Suzana M. Padua
Instituto de Pesquisas Ecologicas (IPE)
Caixa Postal 47
12960-000 Nazare Paulista
Sao Paulo, Brazil
Fernando C. Passos
Departamento Zoologia
Universidad Federal do Parana
Caixa Postal 19020
81531-990 Curitiba
Parana, Brazil
Luiz Paulo de Souza Pinto
Conservation International do Brasil
Av. Getulio Vargas, 1300-7 andar
30112-021 Belo Horizonte
Minas Gerais, Brazil
Alcides Pissinatti
Centro de Primatologia do Rio de Janeiro
(CPRJ)
Fundacao Estadual de Engenharia do
Meio Ambiente (FEEMA)
Rua Fonseca Teles 121/1624
Sao Crist6vao
20940-200 Rio de Janeiro
Rio de Janeiro, Brazil
Fabiana Prado
Instituto de Pesquisas Ecol6gicas (IPE)
Caixa Postal 47
12960-000 Nazare Paulista
Sao Paulo, Brazil
Eluned C. Price
Durrell Wildlife Conservation Trust
Les Augres Manor
Trinity
Jersey JE3 5BP
Channel Islands, British Isles
Paula Proc6pio de Oliveira
Programa de Translocacao
Associacio Mico-Leao-Dourado
Caixa Postal 109.995
28.860-000 Casimiro de Abreu
Rio de Janeiro, Brazil
Becky E. Raboy
Department of Biology
University of Maryland
College Park, MD 20742, USA
Denise Marcal Rambaldi
Associacao Mico-Leao-Dourado
Caixa Postal 109.968
28.860-970 Casimiro de Abreu
Rio de Janeiro, Brazil
Lisa G. Rapaport
Department of Anthropology
University of New Mexico
Albuquerque, NM 87131, USA
Carlos R. Ruiz-Miranda
Lab. de Ciencias Ambientais
Centro de Biociencias
e Biotecnologia
Universidade Estadual Norte
Fluminense
Avenida Alberto Lamego 2000
28015-620 Campos dos Goytacazes
Rio de Janeiro, Brazil
Anthony B. Rylands
Center for Applied Biodiversity Science
Conservation International
1919 M Street, NW
Washington, DC 20036, USA
Cristina V. Santos
Departamento de Psicologia
Experimental
Instituto de Psicologia
Universidade de Sao Paulo
Avenida Professor Mello Moraes 1721
05508-900 Sao Paulo
Sao Paulo, Brazil
Gabriel Rodrigues dos Santos
Instituto de Estudos S6cio-Ambientais
do Sul da Bahia
Rua Major Homem Del Rey 147
45650-000 Ilheus
Bahia, Brazil
Hector N Seuanez
Secao de Genetica
Instituto Nacional de Cancer
Praca da Cruz Vermelha 23
20230-130 Rio de Janeiro
Rio de Janeiro, Brazil
Faical Simon
Fundacao Parque Zool6gico de Sao Paulo
Av. Miguel Stefano 4241
Agua Funda
04301-905 Sao Paulo
Sao Paulo, Brazil
Maria das Gracas de Souza
Instituto de Pesquisas Ecol6gicas (IPE)
Caixa Postal 47
12960-000 Nazare Paulista
Sao Paulo, Brazil
Tara S. Stoinski
TECHLab
Zoo Atlanta
800 Cherokee Avenue
Atlanta, GA 30315, USA
Suzette D. Tardif
Southwest Regional Primate Research
Center
PO. Box 760549
San Antonio, TX 78245-0549, USA
Claudio B. Valladares-Padua
Instituto de Pesquisas Ecol6gicas (IPE)
Caixa Postal 47
12960-000 Nazare Paulista
Sao Paulo, Brazil
Linda Van Elsacker
Centre for Research and Conservation
Royal Zoological Society of Antwerp
Koningin Astridplein 26
B-2018 Antwerp, Belgium
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