The Smallest Anthropoids Developments in Primatology: Progress and Prospects

Series Editor: Russell Tuttle Department of Anthropology The University of Chicago, IL, USA

For other titles published in this series, go to www.springer.com/series/5852 Susan M. Ford ● Leila M. Porter ● Lesa C. Davis Editors

The Smallest Anthropoids

The Marmoset/Callimico Radiation BookID 125266_ChapID FM_Proof# 1 - 26/08/2009 BookID 125266_ChapID FM_Proof# 1 - 26/08/2009

Editors Susan M. Ford Leila M. Porter Southern Illinois University Northern Illinois University Carbondale, IL DeKalb, IL USA USA [email protected] [email protected]

Lesa C. Davis Northeastern Illinois University Chicago, IL USA [email protected]

ISBN 978-1-4419-0292-4 e-ISBN 978-1-4419-0293-1 DOI 10.1007/978-1-4419-0293-1 Springer New York Dordrecht Heidelberg London

Library of Congress Control Number: 2009927722

© Springer Science+Business Media, LLC 2009 All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer Science+Business Media, LLC, 233 Spring Street, New York, NY 10013, USA), except for brief excerpts in connection with reviews or scholarly analysis. Use in connection with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights.

Cover Illustration: Top: by Wallisen Tadashi Hattori; Bottom: by Leila M. Porter

Printed on acid-free paper

Springer is part of Springer Science+Business Media (www.springer.com) Preface

The marmosets and callimicos are diminutive monkeys from the Amazon basin and Atlantic Coastal Forest of South America. The marmosets are the smallest anthropoid primates in the world, ranging in size from approximately 100 to 350 g (Hershkovitz 1977; Soini 1988; Ford and Davis 1992; Araújo et al. 2000); callimi- cos are not much bigger, at around 350–540 g (Ford and Davis 1992; Encarnación and Heymann 1998; Garber and Leigh 2001). Overwhelming genetic evidence, from both nuclear and mitochondrial DNA, now indicates that these taxa represent a unified clade within the callitrichid radiation of New World monkeys, a finding that was unthinkable to all but a few geneticists a decade ago (see review in Cortés- Ortiz, this volume Chap. 2). With increasing evidence that the earliest anthropoids were themselves small bodied (under the 0.8–1 kg threshold that marks all other living anthropoids; see Ross and Kay 2004), the ecology, behavior, reproductive stresses, and anatomical adaptations of the marmosets and callimicos provide the best living models with which to assess the types of adaptations that may have characterized early anthropoids. When Anthony Rylands’ Marmosets and Tamarins: Systematics, Behaviour and Ecology was published in 1993, contributions focused almost entirely on tamarins due to the scarcity of data on marmoset behavior and the almost total lack of knowl- edge about the enigmatic callimicos. Fortunately, this has changed (see Fig. 1). In the last 15 years, there has been an explosion of new information on the South American marmosets and callimicos. In 1977, in his seminal work, Philip Hershkovitz recog- nized only four species of marmosets: Cebuella pygmaea (the pygmy marmoset), Callithrix jacchus (the tufted-ear or common marmoset), Callithrix argentata (the bare-ear marmoset), and Callithrix humeralifer (the tassel-ear marmoset). Since then, many other species have been accepted, and the Amazonian non-pygmy marmosets have been raised to generic level, Mico (Rylands et al. 2000). An entirely new mono- typic genus, Callibella humilis, was first discovered in 1998 (van Roosmalen et al. 1998) and raised to genus level in 2003 (van Roosmalen and van Roosmalen 2003). This is the first new genus of a New World monkey discovered since Callimico 100 years ago (Thomas 1904), and it remains enigmatic and poorly known (see, in particular, Aguiar and Lacher Jr Chap. 18, and Ford and Davis Chap. 21). Six other new species have been identified: Mico nigriceps (Ferrari and Lopes 1992), M. mauesi (Mittermeier et al. 1992), M. marcai (Alperin 1993), M. saterei (Silva Jr and

v vi Preface

Fig. 1 Illustrations of the diminutive anthropoids of the marmoset-callimico radiation. Drawings by Stephen Nash, Conservation International Preface vii

Fig. 1 (continued) viii Preface

Fig. 1 (continued) Preface ix

Fig. 1 (continued) x Preface

Noronha 1998), M. acariensis (van Roosmalen et al. 2000), and M. manicorensis (van Roosmalen et al. 2000). Ten others have been raised to full species status, including Callithrix aurita, C. flaviceps, C. geoffroyi, C. kuhlii, C. penicillata, Mico chrysoleucus, M. emiliae, M. intermedius, M. leucippe, M. melanurus, with at least one other pend- ing: Mico cf. emiliae [Rondônia]. Therefore, this radiation of diminutive monkeys is currently recognized as comprising 4 genera and 22 species of marmosets plus one of callimicos. The taxonomic status, distribution, and descriptions for each of these is reviewed by Rylands et al. (Chap. 2), and the differences between them are discussed in a number of chapters, particularly in the Phylogeny and Anatomy sections of the volume. We have also dramatically improved our understanding of their anatomy, loco- motion, diet, ecology, and social behavior, much of which has been quite surprising. We now know that members of this radiation may form monogamous, polyandrous, and occasionally polygynandrous groups; Cebuella vertically clings but does not often leap; Callibella may not twin all of time; Callimico eats fungi, and may have twinned in the distant past; and the group displays measurable craniodental and postcranial differences related to the unique ways they exploit their respective habi- tats. In addition, many of these species are at risk or are highly endangered (see, in particular, de la Torre et al. Chap. 22 and Ferrari Chap. 23). This volume is an outgrowth of a lunch conversation between the three co-editors and Paul Garber during the 2003 Annual Meeting of the American Association of Physical Anthropologists in Tempe, Arizona, when we realized that there was considerable new information available with which to reassess the complexities of callimico and marmoset behavior and anatomy. In 2005, the co- editors chaired a symposium at the Annual Meeting of the American Association of Physical Anthropologists in Milwaukee, Wisconsin (Advances in Marmoset and Goeldi’s Monkey (Callimico) Research: Anatomy, Behavioral Ecology, Phylogeny, and Conservation). Expanded versions of the presentations from that symposium form the core of this volume, with the addition of a number of other important contributions. This volume presents the work of primary researchers from three continents, and it explores these diminutive primates from several different perspectives. In Section I, phylogeny of the group is examined through genetics, morphology, distribution, and vocalization. Behavior and ecology are examined both in the wild and in captiv- ity, in their reproductive, social, and cognitive dimensions (Section II) as well as rang- ing and locomotion (Section III). These include studies on four of the five genera (Callimico, Callithrix, Mico, and Cebuella; there are still no in depth studies on Callibella, although new information on ecology is included in Aguiar and Lacher Jr, Chap. 18). The functional and phylogenetic anatomy of all five genera is dis- cussed in Section IV, including chapters on cranial anatomy, postcranial anatomy, and jaw mechanics and musculature associated with the marmosets’ distinctive diet of exudativory. The volume closes with consideration of conservation issues and concerns (Section V). For consistency throughout the volume, we have adopted certain taxonomic con- ventions (largely following Rylands et al. 2000; Rylands et al. Chap. 2). Although Preface xi not all authors fully agree with the classificatory choices made here, all have agreed to use the following names in their chapters: all marmosets, tamarins, and callimi- cos are in the family Callitrichidae; no subfamily names are used; and any refer- ence to the twinning callitrichids (excluding callimicos) is to the “marmosets and tamarins.” The common name used for Callimico is callimicos, although they are often referred to as Goeldi’s monkeys elsewhere. The first time any platyrrhine is mentioned in a chapter, both the scientific and common names are given; after that, individual author(s) may adopt either scientific or common terminology. Much of the work on these smallest anthropoids has been published in languages other than English or in sources that can be difficult to acquire. It is our hope that by bringing the work of these authors together in one place and one language, with abstracts in both Spanish and Portuguese, this volume will provide readily acces- sible information on the evolution, behavior, adaptations, and conservation needs of the marmosets and callimicos both for people interested in these wonderful monkeys for themselves, and for those who discover that knowledge of the diminu- tive marmosets and callimicos aids their understanding of other organisms and the diverse ecosystems in which marmosets and callimicos live.

Acknowledgments The editors are particularly indebted to several individuals for advice, cri- tique, and assistance, without which this volume could not have been completed. These include Dr. Anthony Rylands for leading a spirited and inspiring discussion after the original symposium; Drs. Paul Garber and Anthony Rylands (plus two anonymous reviewers) for suggesting some additional contributors and generally much-welcomed advice; Dr. Dan Gebo for critique of some chapters; the authors themselves, some of whom read and provided input on other chapters; Dr. Liliana Cortés-Ortiz and Mr. José Romulo Sanchez for translating most of the abstracts into Spanish; and Drs. Maria B.C. de Sousa and Gabriel Marroig, and Ms. Ana Carolina Castro for translating most into Portuguese. Several graduate students provided editorial assistance, includ- ing Rose Hores, Chihiro Shibata, Karen Wolf, and for the index: Elliott Forsythe and Aimee Hosemann. Conservation International and Dr. Russell Mittermeier underwrote the marvelous color plates by Stephen Nash, to whom we are particularly indebted. Drs. Jennifer Rehg and Tab Rasmussen provided the hospitality of their cottage for one memorable weekend of work. LCD is grateful for the organizational talents of Avril Murray and Felicia Elliott in the early stages of the book, and for the enduring gift of JM’s support. SMF especially thanks her husband, Al Allen, for assistance with many illustrations and Al, David and Emily for their patience, love, and good humor (mostly) throughout the production of the book. Carbondale, IL Susan M. Ford DeKalb, IL Leila M. Porter Chicago, IL Lesa C. Davis

References

Aguiar JM, Lacher TE Jr (this volume) Cranial morphology of the dwarf marmoset Callibella in the context of callitrichid variability. In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids: The marmoset/callimico radiation. Springer Press, New York, pp 355–380 xii Preface

Alperin R (1993) Callithrix argentata (Linnaeus, 1771): Considerações taxonômicas e descrição de subespécie nova. Bol Mus Para Emílio Goeldi, Sér Zool. 9(2):317–328 Araújo A, Arruda MF, Alencar AI, Albuquerque F, Nascimento MC, Yamamoto ME (2000) Body weight of wild and captive common marmosets (Callithrix jacchus). Int J Primatol 21:317–324 Cortés-Ortiz L (this volume) Molecular phylogenetics of the Callitrichidae with an emphasis on the marmosets and Callimico. In: Ford SM, Porter LM, Davis LC (eds) The smallest anthro- poids: The marmoset/callimico radiation. Springer Press, New York, pp 3–24 de la Torre S, Yepez P, Snowdon C (this volume) Conservation status of pygmy marmosets in Ecuadorian Amazon. In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids: The marmoset/callimico radiation. Springer Press, New York, pp 451–464 Ferrari SF (this volume) Marmosets and callimicos: conservation status and concerns. In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids: The marmoset/callimico radiation. Springer Press, New York, pp 465–476 Ferrari SF, Lopes MA (1992) A new species of marmoset, genus Callithrix Erxleben 1777 (Callitrichidae, Primates) from western Brazilian Amazonia. Goeldi Zool (12):1–3 Ford SM, Davis LC (1992) Systematics and body size: Implications for feeding adaptations in New World monkeys. Am J Phys Anthropol 88:415–468 Garber PA, Leigh SR (2001) Patterns of positional behavior in mixed-species troops of Callimico goeldii, Saguinus labiatus, and Saguinus fuscicollis in northwestern Brazil. Am J Primatol 54:17–31 Hershkovitz P (1977) Living New World Monkeys (Platyrrhini) with an Introduction to Primates, vol 1. Chicago University Press, Chicago Mittermeier RA, Schwarz M, Ayres JM (1992) A new species of marmoset, genus Callithrix Erxleben 1777 (Callitrichidae, Primates), from the Rio Maués region, state of Amazonas, Central Brazilian Amazonia. Goeldi Zool (14):1–17 Ross CF, Kay RF (eds) (2004) Anthropoid origins: New visions. Kluwer Academic/Plenum Publishing, New York Rylands AB, (1993) Marmosets and Tamarins: Systematics, Behaviour and Ecology. Rylands AB (ed) Oxford University Press, Oxford Rylands AB, Mittermeier RA, Coimbra-Filho AF (this volume) The systematics and distribu- tion of the marmosets (Callithrix, Callibella, Cebuella, and Mico) and Callimico (Callimico) (Callitrichidae, Primates). In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids: The marmoset/callimico radiation. Springer Press, New York, pp 25–61 Rylands AB, Schneider H, Langguth A, Mittermeier RA, Groves CP, Rodríguez-Luna E (2000) An assessment of the diversity of New World primates. Neotrop Primates 8(2):61–93 Silva Jr JS, Noronha M de A (1998) On a new species of bare-eared marmoset, genus Callithrix Erxleben, 1777, from central Amazonia, Brazil (Primates: Callitrichidae). Goeldi Zool (21):1–28 Soini P (1988) The pygmy marmosets, genus Cebuella. In: Mittermeier RA, Rylands AB, Coimbra-Filho AF, da Fonseca, GA (eds) Ecology and behavior of neotropical primates, vol 2. World Wildlife Fund, Washington DC, pp 79–129 Thomas O (1904) New Callithrix, Midas, Felis, Rhipidomys, and Proechimys from Brazil and Ecuador. Ann Mag Nat Hist 14(7):188–196 Van Roosmalen MGM, Van Roosmalen T (2003) The description of a new marmoset genus, Callibella (Callitrichinae, Primates), including its molecular phylogenetic status. Neotrop Primates 11(1):1–10 Van Roosmalen MGM, Van Roosmalen T, Mittermeier RA, Fonseca GAB da (1998) A new and distinctive species of marmoset (Callitrichidae, Primates) from the lower Rio Aripuanã, state of Amazonas, central Brazilian Amazonia. Goeldi Zool (22):1–27 Van Roosmalen MGM, Van Roosmalen T, Mittermeier RA, Rylands AB (2000) Two new species of marmoset, genus Callithrix Erxleben, 1777 (Callitrichidae, Primates), from the Tapajós/ Madeira interfluvium, south central Amazonia, Brazil. Neotrop Primates 8(1):2–18 Contents

Section I Phylogeny

1 Molecular Phylogenetics of the Callitrichidae with an Emphasis on the Marmosets and Callimico ...... 3 Liliana Cortés-Ortiz

2 The Systematics and Distributions of the Marmosets (Callithrix, Callibella, Cebuella, and Mico) and Callimico (Callimico) (Callitrichidae, Primates) ...... 25 Anthony B. Rylands, Adelmar F. Coimbra-Filho, and Russell A. Mittermeier

3 The Vocal Identity of the Callithrix Species (Primates, Callitrichidae) ...... 63 Sérgio Lucena Mendes, Jacques Marie Edme Vielliard, and Paulo De Marco Jr.

Section II Reproductive, Social, and Cognitive Behavior

4 Social Behavior of Callimicos: Mating Strategies and Infant Care ...... 87 Leila M. Porter and Paul A. Garber

5 Genetic Structure Within and Among Populations of the Common Marmoset, Callithrix jacchus: Implications for Cooperative Breeding ...... 103 Christopher G. Faulkes, M.F. Arruda, and M.A.O. Monteiro da Cruz

xiii xiv Contents

6 Mating Systems and Female–Female Competition in the Common Marmoset, Callithrix jacchus ...... 119 Maria Emilia Yamamoto, Maria de Fátima Arruda, Anuska Irene Alencar, Maria Bernardete Cordeiro de Sousa, and Arrilton Araújo

7 Balancing Cooperation and Competition in Callitrichid Primates: Examining the Relative Risk of Infanticide Across Species ...... 135 Leslie Digby and Wendy Saltzman

8 Social Hierarchy and Dispersal in Free-Ranging Buffy-Headed Marmosets (Callithrix flaviceps) ...... 155 Stephen F. Ferrari

9 Emigration as a Reproductive Strategy of the Common Marmoset (Callithrix jacchus) ...... 167 Maria Bernardete Cordeiro de Sousa, Ana Claudia Sales da Rocha Albuquerque, Maria Emilia Yamamoto, Arrilton Araújo, and Maria de Fátima Arruda

10 Social and Physical Cognition in Marmosets and Tamarins ...... 183 Ludwig Huber and Bernhard Voelkl

Section III Ranging Behavior and Locomotion

11 Limited Dispersal and Genetic Structure of Silvery Marmosets (Mico argentatus) in the Fragmented Landscape of Central Amazonia ...... 205 Evonnildo Gonçalves, Stephen F. Ferrari, Paulo E.G. Coutinho, Elytânia Menezes, Artur Silva, and Maria Paula C. Schneider

12 Habitat Use and Ranging Behavior of the Silvery Marmoset (Mico argentatus) at Caxiuanã National Forest (Eastern Brazilian Amazonia) ...... 221 Cecilia Veracini

13 Ranging Patterns of Callimico goeldii (callimico) in a Mixed Species Group ...... 241 Jennifer A. Rehg

14 A Comparative Study of the Kinematics of Trunk-to-Trunk Leaping in Callimico goeldii, Callithrix jacchus, and Cebuella pygmaea ...... 259 Paul A. Garber, Ana Sallenave, Gregory E. Blomquist, and Gustl Anzenberger