CRANIAL VARIABILITY IN AMAZONIAN MARMOSETS A Dissertation by JOHN MARSHALL ...

277 Pages·2009·5.27 MB·English

CRANIAL VARIABILITY IN AMAZONIAN MARMOSETS

A Dissertation
by
JOHN MARSHALL AGUIAR

Submitted to the Office of Graduate Studies of
Texas A&M University
in partial fulfillment of the requirements for the degree of
DOCTOR OF PHILOSOPHY

December 2009

Major Subject: Wildlife and Fisheries Sciences
CRANIAL VARIABILITY IN AMAZONIAN MARMOSETS

A Dissertation
by
JOHN MARSHALL AGUIAR

Submitted to the Office of Graduate Studies of
Texas A&M University
in partial fulfillment of the requirements for the degree of
DOCTOR OF PHILOSOPHY

Approved by:
Chair of Committee, Thomas E. Lacher, Jr.
Committee Members, John Bickham
Duane A. Schlitter
James B. Woolley
Head of Department, Thomas E. Lacher, Jr.

December 2009

Major Subject: Wildife and Fisheries Sciences
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ABSTRACT

Cranial Variability in Amazonian Marmosets. (December 2009)
John Marshall Aguiar, B.A.; B.A., University of Richmond;
M.A., Old Dominion University
Chair of Advisory Committee: Dr. Thomas E. Lacher, Jr.

The family Callitrichidae encompasses the marmosets and tamarins, the smallest
of the anthropoid primates and one of the most species-rich of platyrrhine families.
Seven new species of Amazonian marmosets (Callithrix, Callitrichidae) have been
discovered in recent years, as well as the exceptional dwarf marmoset Callibella humilis.
Most of these species were described on the basis of their pelage and presumed
separation by major rivers. I performed analyses of craniometric variables by taxa and
by river basins, in order to determine if there are significant cranial distinctions between
taxa separated by rivers.
I analyzed quantitative cranial and mandibular characters of Callibella humilis to
determine if it could be distinguished from other callitrichids. I found that Callibella is
clearly distinct from all other genera of marmosets and tamarins, in particular in the
morphology of the lower jaw. I also analyzed representative species of Amazonian
Callithrix and found support for the theory of separation by river-barriers. In my
analyses the Amazonian marmosets were divided into three separate species groups,
with the easternmost species (Callithrix argentata and C. leucippe) strongly distinct and
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separated from the others by the broad Rio Tapajós. Two additional species, C.
chrysoleuca and C. saterei, formed a discrete group in the central Amazon, and the
westernmost species – C. melanura, C. nigriceps and the Rondônia marmoset – formed a
third distinct group. These results from cranial morphology align with recent genetic
studies indicating that the Amazonian marmosets are strongly divided by the Rio
Tapajós, and offer additional support to the theory of river-barriers.
Although these species are typically considered to be of low conservation
priority, many of them are found in areas experiencing accelerated deforestation. An
initial analysis of protected-area coverage for the Amazonian marmosets demonstrates
that while some species may be found in a number of protected areas, others are virtually
uncovered, and the lack of comprehensive information on their distributions may
preclude an effective conservation strategy. The dwarf marmoset Callibella is known
from an exceptionally restricted range, with almost no protected areas, and this unique
species should be a conservation priority.
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ACKNOWLEDGEMENTS

A great many lives have affected mine during the course of this research, like a
river of stars swirling through the galaxy – each with its own unique tug and pull of
gravity, all combining their effects to shape the course of my very long and eccentric
orbit. As with the galactic disc, some stars have shone more brightly, and others have
departed on separate vectors, but each has influenced me in some strong or subtle way.
Brightest among the luminous host is my advisor, Dr. Tom Lacher, who has
provided steady guidance, sound advice, and vital perspective, as well as an occasional
dose of motivation. He has supported me at all times, in every aspect of this endeavor –
and as Stephen Maturin might say, I fear he has burdened me with a debt I can never
fully repay. I have also been glad to know his wife Susana, one of my very favorite
Brazilians, who (along with her husband) has always encouraged me on my long road
towards learning Portuguese.
Another triad of bright stars are my committee members, Dr. John Bickham, Dr.
Duane Schlitter and Dr. Jim Woolley, who have been superb in their willingness to help
with matters great and small.
The logistics of my travel and research could not have been navigated without
support from the staff of the Department of Wildlife and Fisheries Sciences, in particular
Vicki Buckbee, Dawn Miles and Diann Radke. I owe special thanks to Janice Crenshaw
for helping me through my first semesters, and for her efforts in helping me locate and
pursue scholarship opportunities. Tariq Ayyub provided excellent computer support
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during my final, intense visits to the department, and Shirley Konecny deserves special
mention for her kindness and mother-birding. Thanks are also due to Dr. Jane Packard,
whose encouragement of my science writing is much appreciated.
Few can appreciate the intensity, stress and challenge of the graduate experience
as deeply as those who have only lately survived it, and so thanks are due to Elizabeth
Kennedy, for counsel and support in difficult times, and friendship in the better; and also
to Michael Corson, for his patient and unfailing encouragement, and for whom going
above and beyond is a signature style. And, thanks to Tom Dolan, fellow wanderer on a
parallel course.
I have been fortunate to have an advisor who supported my research travel to the
fullest extent, and fortunate that this travel has taken me through many countries, chief
among them Brazil. On my first trip to Brazil I was privileged to meet Dr. Adelmar
Coimbra-Filho, who has devoted his life to the conservation of the lion tamarins, and
what fragments yet remain of their ancient forest home. On that first trip I also met
Ilmar Bastos Santos, whose enthusiastic support, both personal and professional, was
invaluable for that and subsequent journeys.
Thanks are also due to Dr. Leonardo Sena, for his open and generous assistance
during my travels in and around Belém. I owe special gratitude to Vicki Haines
(Vitôria), who was a lifesaver during my first visit to the Brazilian Amazon, and to
Delfinay Barbosa (Dedão) and his brother Ruy, who kindly took time out of their own
lives to guide me in search of a monkey none of us had ever seen.
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I am especially grateful to Marc van Roosmalen for making the type skull of
Callibella humilis available to examine while I was in Brazil, as well as for the dinners
and conversation at his home. Thanks are also due to José de Sousa e Silva Júnior and
Suely Aguiar of the Museu Paraense Emílio Goeldi in Belém; João Alves de Oliveira of
the Museu Nacional in Rio de Janeiro; Mario de Vivo of the Museu de Zoologia da
Universidade de São Paulo; and the staff of the Instituto Nacional de Pesquisas
Amazônicas in Manaus, for access to their respective collections in Brazil. I also
appreciate the opportunity to examine specimens under the care of Linda Gordon and
Richard Thorington, Jr. at the United States National Museum of Natural History in
Washington, D.C.; Robert Randall at the American Museum of Natural History in New
York; Maria Rutzmoser at the Harvard Museum of Comparative Zoology in Cambridge,
Massachusetts; and Bruce Patterson at the Field Museum in Chicago. Additional thanks
are also due to Olavi Grönwall of the Naturhistoriska Riksmuseet in Oslo, Sweden;
Manfred Ade of the Humboldt Museum für Naturkunde in Berlin, Germany; the staff of
the Museum National de Histoire Naturelle in Paris, France; and most especially Chris
Smeenk of the Rijksmuseum van Natuurlijk Historie in Leiden, the Netherlands.
I am also grateful to Colin Groves and Michael Willig for constructive comments
on the details of marmoset morphology and statistical analysis. In addition, thanks are
due to Daniel Juhn and Kellee Koenig of Conservation International, who helped me to
locate and manipulate the satellite image which became Figure 12. I would like to
thank Susan Ford, Lesa Davis, and Leila Porter, organizers of the Marmoset and
Callimico Symposium at the 2005 meeting of the American Association of Physical
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Anthropology, for inviting myself and Dr. Lacher to participate in the symposium.
Additional thanks are due to Susan Ford for her kind advice and support.
Deep thanks are due to Krista Adamek, who spent countless hours working with
shapefiles to create the maps, data and supporting materials for Chapters I and V. She
did much of this while under course and project deadlines of her own; but whatever the
request, she was willing, capable and enthusiastic, and without her the maps most likely
could not have been done. Thanks also to Rich Miller, for a vital and timely save.
Finally, several exceptional colleagues at Conservation International deserve a
special mention. Kim Meek helped in many ways, and she taught me a great deal about
editing and graphic design in a professional environment. Karyn Tabor helped
immensely at several key, stressful junctures, and more than once spent hours of her own
time solving technical problems for me. And Edward Lohnes, a good pal and stand-up
bloke, cheerfully and willingly helped in countless ways.
And a special thanks must go to Stephen Nash, Scientific Illustrator for
Conservation International, who has been a kind and generous colleague, and whose
artwork is found on so many of the following pages. This dissertation would be far less
colorful – and the marmosets themselves only distant, abstract names – were it not for
his ready permission to use so many of his illustrations. I feel privileged to be able to
include a few of them here, and dream of a day when I can show him a new species to
capture with pencil and brush.

And, above and beyond it all, is Mom. And the cats.
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TABLE OF CONTENTS

Page
ABSTRACT .............................................................................................................. iii
ACKNOWLEDGEMENTS ...................................................................................... v
TABLE OF CONTENTS .......................................................................................... ix
LIST OF FIGURES ................................................................................................... xi
LIST OF TABLES .................................................................................................... xiii
CHAPTER
I INTRODUCTION ................................................................................ 1

Primate Diversity ............................................................................ 1
Overview of Defining Callitrichid Features ................................... 8
Overview of Callitrichid Genera .................................................... 12

II TAXONOMY OF THE AMAZONIAN MARMOSETS .................... 42
Introduction .................................................................................... 42
The Genus Callithrix ...................................................................... 43
Callithrix argentata ........................................................................ 51
Callithrix chrysoleuca .................................................................... 54
Callithrix emiliae ............................................................................ 57
Callithrix humeralifer .................................................................... 59
Callithrix intermedia ...................................................................... 61
Callithrix leucippe .......................................................................... 63
Recent Discoveries ......................................................................... 65
Callimico ........................................................................................ 68

III CRANIAL MORPHOLOGY OF THE DWARF MARMOSET
CALLIBELLA IN THE CONTEXT OF CALLITRICHID
VARIABILITY .................................................................................... 76

Introduction .................................................................................... 76
Methods .......................................................................................... 84
Results ............................................................................................ 90
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CHAPTER Page
Discussion ......................................................................................... 98
IV RIVER-BARRIERS AND CRANIAL MORPHOLOGY IN
AMAZONIAN MARMOSETS ........................................................... 115

Introduction .................................................................................... 115
Methods .......................................................................................... 140
Results ............................................................................................ 146
Discussion ...................................................................................... 159
V CONCLUSION: CONSERVATION OF CALLITRICHIDS IN THE
BRAZILIAN AMAZON ...................................................................... 187

REFERENCES .......................................................................................................... 215
APPENDIX A ........................................................................................................... 236
APPENDIX B ........................................................................................................... 261
VITA ......................................................................................................................... 264