New World Monkeys: The Evolutionary Odyssey

New World Monkeys

NEW WORLD MONKEYS

The Evolutionary Odyssey

Alfred L. Rosenberger

PRINCETON UNIVERSITY PRESS

PRINCETON AND OXFORD

Copyright © 2020 by Princeton University Press

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Published by Princeton University Press

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ISBN: 978-0-691-14364-4

ISBN (e-book): 978-0-691-18951-2

Version 1.0

British Library Cataloging-in-Publication Data is available

Editorial: Alison Kalett and Abigail Johnson

Production Editorial: Ellen Foos

Figures 1.1, 2.1, 2.6, 2.11, and 4.4 are copyright 2013 Stephen D. Nash / IUCN SSC Primate Specialist Group

Jacket image courtesy of Luciano Candisani / Instagram: @lucianocandisani

This book is dedicated to Rivka Rosenberger,

my SuzieQ ,

my muse,

twice my wife,

forever the love of my life.

CONTENTS

List of Illustrationsxi

Prefacexv

CHAPTER 1.What Is a New World Monkey?1

What is a monkey?3

What is a platyrrhine?8

Platyrrhines and catarrhines12

Platyrrhine taxonomy15

20 million years of evolution: 16 genera of extant playrrhine primates18

CHAPTER 2.Diverse Lifestyles22

Predatory frugivores: Family Cebidae26

Fruit huskers and seed eaters: Family Pitheciidae50

Prehensile-tailed frugivore-folivores: Family Atelidae66

CHAPTER 3.What’s In a Name?79

A new fossil gets a title82

Names can reflect evolutionary hypotheses86

Changing ideas can result in name changes89

CHAPTER 4.Evolutionary Models91

How do diverse genera coexist in one patch of forest?: the Ecophylogenetic Hypothesis95

DNA and anatomy: molecules and morphology100

Cebines and callitrichines share a unique common ancestor102

Chasing monkeys: synthesizing behavior, ecology, and morphology105

The platyrrhine Tree of Life109

CHAPTER 5.How to Eat like a Monkey113

Different teeth for different foods115

What do they eat?119

Secondary food preferences121

Surviving preferred-food scarcity124

Gouging tree bark to eat the tree gum126

Incisors are key to fruit eating129

Who are the leaf eaters?134

CHAPTER 6.Arboreal Acrobats139

Locomotor types: clingers, climbers, leapers, and more144

Feet and hands tell the story of platyrrhine evolution148

Hanging, clambering, and locomoting with a prehensile tail151

Platyrrhines are the only primates that evolved grasping tails154

Tails for balancing, embracing, and coiling for social bonding158

CHAPTER 7.Many Kinds of Platyrrhine Brains161

Studying brain size and shape163

Brain-to-body-size relationships168

The monkey stole my keys: intelligence and dexterity are tightly correlated170

Fingertips, precision grips, and tool use172

The sensorimotor strip in the brain controls tail use174

Evolution of the brain in platyrrhines is shaped by phylogeny, ecology, and social behavior176

CHAPTER 8.The Varieties and Means of Social Organization178

A day in the life of a platyrrhine181

Communicating through visual displays186

Tail-twining in Titi and Owl Monkeys as tactile communication190

Vocalizing with roars and duets191

Sending scent signals196

The odoriferous callitrichines200

Foraging parties203

Capuchin gestural language204

An evolutionary model of platyrrhine sociality207

CHAPTER 9.20 Million Years: Every Fossil Tells a Story212

Linking a fossil with a living monkey: the Long-Lineage Hypothesis220

The La Venta fossils look like modern monkeys224

Fossil evidence for longevity with little change231

A 12–14-million-year-old Owl Monkey fossil233

Fossils that tell us where they once lived, what they ate, and more237

The mystery of fossils found on Caribbean islands250

Fossils prior to 20 million years ago: more questions than answers258

CHAPTER 10.South America Was Once an Island: How Did Platyrrhine Ancestors Get There?263

The Americas Scenario267

The Transatlantic Scenario274

Calculating the likelihood of the Transatlantic Scenario278

CHAPTER 11.After 20 Million Years of Existence, New World Monkeys Face Extinction282

Not only species, but entire evolutionary streams are in peril283

The Atlantic Forest, a biodiversity hotspot, is being decimated285

Conservation efforts: Golden Lion Tamarin Project and Muriqui Project of Caratinga287

All that is being lost can never be recovered293

Acknowledgments295

Glossary of Terms297

Recommended Reading301

References303

Index317

ILLUSTRATIONS

Plates

PLATE 1.Cebus nigritus, Black Capuchin Monkey

PLATE 2.Saimiri sciureus, Common Squirrel Monkey

PLATE 3.Callimico goeldii, Goeldi’s Monkey

PLATE 4.Saguinus imperator, Emperor Tamarin

PLATE 5.Leontopithecus rosalia, Golden Lion Marmoset

PLATE 6.Callithrix flaviceps, Buffy-headed Marmoset

PLATE 7.Cebuella pygmaea, Pygmy Marmoset

PLATE 8.Pithecia pithecia, White-faced Saki

PLATE 9.Chiropotes chiropotes, Red-backed Bearded Saki

PLATE 10.Cacajao calvus, Red Uacari

PLATE 11.Callicebus torquatus, Collared Titi Monkey

PLATE 12.Aotus azarae, Southern Owl Monkey

PLATE 13.Ateles chamek, Black-faced Spider Monkey

PLATE 14.Brachyteles arachnoides, Muriqui

PLATE 15.Lagothrix lagothricha, Woolly Monkey

PLATE 16.Alouatta seniculus, Red Howler Monkey

Figures

FIG. 1.1. Cladogram of the major groups of living primates

FIG. 1.2. Map of South America and its major ecological zones

FIG. 1.3. Skull and face of a capuchin and a rhesus monkey

FIG. 2.1. Cladistic relationships and classification of living cebid genera

FIG. 2.2. Average body weights of the 16 living platyrrhine genera

FIG. 2.3. Skeleton of Cebus, the Capuchin Monkey

FIG. 2.4. Skull of Saimiri, the Squirrel Monkey

FIG. 2.5. Skull of Callithrix, the Marmoset

FIG. 2.6. Cladistic relationships and classification of living pitheciid genera

FIG. 2.7. Incisors and canines of a saki, bearded saki, and uacari compared with a spider monkey

FIG. 2.8. Skull of Cacajao, the Uacari

FIG. 2.9. Skull of Callicebus, the Titi Monkey

FIG. 2.10. Skull of Aotus, the Owl Monkey

FIG. 2.11. Cladistic relationships and classification of living atelid genera

FIG. 2.12. Skeleton of Ateles, the Spider Monkey

FIG. 2.13. Cranium of Brachyteles, the Muriqui

FIG. 2.14. Skull of Alouatta, the Howler Monkey

FIG. 3.1. Fossiliferous bluffs at Killik Aike Norte, Argentina, and the fossil Killikaike blakei

FIG. 3.2. Crania of two male Cebus species compared

FIG. 4.1. Gradistic model of platyrrhine evolution and classification

FIG. 4.2. Schematic overlays of molar sets of the 16 living genera of platyrrhines

FIG. 4.3. Three sets of platyrrhine dentitions showing progressive reduction in size and shape of molars

FIG. 4.4. Morphology-based cladogram of the living platyrrhine genera and families

FIG. 5.1. Sketches of four platyrrhine upper and lower molar sets

FIG. 5.2. Key cranial and dental features associated with dietary specializations

FIG. 5.3. Scanning electron micrograph of vertical cross sections of lower central incisors

FIG. 5.4. Three-dimensional models of three upper and lower molars of a howler monkey

FIG. 6.1. Structure of a tropical rainforest, with three-layer arboreal composition

FIG. 6.2. Varied feet and hands of platyrrhine primates and the Tree Shrew

FIG. 6.3. Length proportions of feet and hands in selected platyrrhines

FIG. 6.4. Right hand and wrist skeletons of a marmoset, capuchin, and muriqui

FIG. 6.5. Plot of tail length against body size in platyrrhines

FIG. 6.6. Schematic model of sitting postures of a haunch-sitting platyrrhine and a rump-sitting catarrhine

FIG. 7.1. Relationship between body mass and cranial capacity in living platyrrhines and other primates

FIG. 7.2. Left-side views of the brains of five platyrrhines

FIG. 7.3. Lateral views of the brains of a prehensile- and semiprehensile-tailed monkey

FIG. 8.1 Monthly time schedule for waking up and bedding down in Goeldi’s Monkey and Saddle-back and Red-bellied Tamarins

FIG. 8.2. Comparative anatomy of head, neck, and shoulders of two monkeys

FIG. 8.3. Some facial expressions of Tufted Capuchin

FIG. 9.1. Increase over time in number of unique, named genera of fossil platyrrhines

FIG. 9.2. Geographic distribution of platyrrhine fossils in South America and the Caribbean

FIG. 9.3. Molecular cladogram and timeline for evolution of clades and genera

FIG. 9.4. Type specimen of Dolichocebus gaimanensis, a relatively complete edentulous cranium

FIG. 9.5. Right side of lower jaw of Neosaimiri fieldsi, and the type mandible of Laventiana annectens, now known as genus Dolichocebus

FIG. 9.6. Type specimen of Tremacebus harringtoni, an edentulous cranium, compared with a titi monkey and squirrel monkey

FIG. 9.7. Left and right halves of the crania of an owl monkey and the fossil Tremacebus harringtoni

FIG. 9.8. Side views of the mandibles of a living owl monkey and fossil Aotus dindensis, and reconstructed mandible of Homunculus patagonicus

FIG. 9.9. Oblique view of the Dolichocebus cranium

FIG. 9.10. Reconstructed partial face of Homunculus patagonicus and the mandible designated as a new type specimen

FIG. 9.11. Three-dimensional models of endocasts and crania of the fossils Cartelles coimbrafilhoi and Caipora bambuiorum compared with two living platyrrhines

FIG. 9.12. Type specimen of Soriacebus ameghinorum, right side of a mandible with teeth

FIG. 9.13. Cranium and mandible of Antillothrix bernensis

FIG. 9.14. Scuba diver Oleg Schevchuk brings a monkey skull to the surface from a submerged cave

FIG. 10.1. Polar-projection of the northern megacontinent of Laurasia during the early Eocene showing the disposition of landmasses

FIG. 11.1. Drs. Devra Kleiman, Benjamin Beck, and Karen Strier

Tables

TABLE 2.1. Summary of critical adaptations and behaviors

TABLE 2.2. Comparative measures of living platyrrhine body proportions

TABLE 4.1. Revised classification of New World monkeys

TABLE 6.1. Principal modes of locomotion among New World monkeys

TABLE 7.1. Comparison of brain sizes among living platyrrhines

TABLE 8.1. Summary of social organization, mating systems, and dispersal patterns

TABLE 8.2. Daily activities of three species of callitrichines

TABLE 9.1. Paleontological record of New World monkeys

TABLE 10.1. Americas Scenario and Transatlantic Scenario compared

TABLE 10.2. Transatlantic Scenario in sequential steps

PREFACE

Today, New World monkeys may be the most intensely studied group of primates. When I first became intrigued by the question of platyrrhine evolution as a college student in the 1970s, few people were interested in New World monkey fossils, morphology, ecology, or behavior. The focus then was on apes, Old World monkeys, and lemurs. It was my great good fortune that primatology grew rapidly as a discipline at the same time that I matured to become a professional primatologist, working in the lab, in the field, and in the museum. The methods of study developed, new technologies were introduced, and the scope of research interests broadened, thus transforming our knowledge of platyrrhine evolution. This made possible the modern study of what Charles Darwin described as descent with modification, meaning how a lineage or a taxonomic group of organisms becomes altered over generational time while adjusting to the circumstances of an ever-changing environment. We call this phylogeny and adaptation. That’s what this book is about.

Other key evolutionary concepts that form the basis of our understanding of the harmonious coexistence of the long-lived New World monkeys and their diversification, each group in its ecological niche, will become clear in the story of their odyssey.

My interest in platyrrhines and primatology had many beginnings. Words and names and a charismatic professor, Warren Kinzey, drew me in when I was a sophomore at City College of New York. The words that attracted me were the invented, Latinized taxonomic names of these animals written in italics to offset them from everyday vocabulary. They were often exotic compound terms—Para | pithecus, Australo | pithecus, Calli | cebus—which when deciphered, might reveal an author’s hypothesis about where a particular fossil or modern primate fit into the scheme of evolution, a geographic place of origin, or what physical trait set one species apart from others. Professor Kinzey, whom I soon knew as Warren, though I was half his age, tossed these names about in lectures as he explained ideas, challenging his students to learn in what seemed like speaking in code. He prodded us to think visually as he used old-fashioned chalk to annotate an anatomical image on the blackboard, sometimes drawing with both hands simultaneously. The scientists, his contemporaries, about whom he talked in lectures, he called by first or nicknames, and he mentioned their academic affiliations to humanize them even more: Cliff was Clifford Jolly at NYU; Sherry was Sherwood Washburn at Berkeley. Warren used surnames to note the pantheon of greats cited in our textbook, the only advanced book on primate evolution at the time, The Antecedents of Man by Sir Wilfrid E. Le Gros Clark, which remains a classic. I could see that becoming a physical anthropologist would allow me to combine my attraction to a small branch of science for which I seemed to have an aptitude, with my desire to write.

As a first-year graduate student at the City University of New York (CUNY) Graduate Center, my first real taste of professional-level study occurred in a primate anatomy course, one of only two offered in the entire country, during the weekly evening appointments I had with a dead gelada baboon in a high-rise office building on 42nd Street, off Broadway, in midtown Manhattan in the heart of New York City. I dissected it in the physical anthropology lab. It was an invaluable learning experience, to open the animal up, isolate the individual muscles, follow their ribbonlike paths to see how the muscles spanned the joints, and learn the routes of coursing nerves and blood vessels.

My years at CUNY consolidated my interests in form, function, behavior, theory and practice, and New World monkeys. During two summers I did fieldwork in the Peruvian Amazon, chasing monkeys as it was called, learning what monkey life was like and how little we knew about them. I learned how important it was to study morphology and behavior together in order to reveal how these primates evolved. The results of this work in the field were published in several coauthored articles, and this was my initiation into the world of professional scientists.

Meanwhile, my sanctum became the study collections of skeletonized and preserved primates in the American Museum of Natural History in New York. There, evolutionary puzzles and anatomical questions could be probed by studying skulls, teeth, limbs, and pelts. I was encouraged by my mentors to do problem-based research, to express my opinions and publish them when I had something original to say.

At that time at the Museum, graduate students could freely roam the stacks of one of the world’s best research libraries. There I spent hours, days, months, poring over reprint collections that had once belonged to, and bore the signatures of, the intellectual giants in the field. They included the Museum’s curator of vertebrate paleontology, comparative anatomy and ichthyology—three departments all at once—William King Gregory, who was the finest primate evolutionist of the first half of the 20th century. I was even able to peruse Linnaeus’s 1758 edition of Systema Naturae, written in Latin, which became the starting point of modern taxonomy.

In the stacks, everything seemed there for the touching and reading; rare books, defunct foreign journals, mimeographed and photocopied personal logs, dog-eared separates gifted to Museum scientists by far-flung colleagues, the collected writings of the famous and the forgotten systematic biologists and paleontologists whose works were collected into individual boxes and books bound for convenience. In the stacks, I could turn the pages of rare, oversized, leather-bound volumes dating back 200 years and more, with hand-colored illustrations describing wild primates never before seen by Europeans and with gorgeous lithographs depicting the minute anatomical details of newly discovered skulls and tiny fossil teeth. Examples of this brilliant artistry from the naturalist Blainville, published between 1839 and 1864, are presented in chapter 2. The library was the resource vault behind the taxonomic names I found so intriguing. Therein lay the historical evidence that primates have long claimed the imaginations not only of scholars, but also of adventurers, explorers, artists, amateurs, expatriates, courtiers, monarchs and Jesuit priests, writing in English, French, Spanish, Italian, German, Dutch, Latin, and more. It was a group whose ranks I was eager to join and whose legacy I would be privileged to carry onward.

In the 1970s the American Museum was a hotbed of the cladistic revolution, a newly refined method of reconstructing phylogeny, taxonomic genealogies, that spread from Europe. It was a truly tumultuous period in evolutionary biology, with a public, often hostile battle of ideas and egos among scholars forcing a rethinking of a fundamental scientific approach, and a rewriting of the evidence for primate evolution. What was being replaced was the rather loose way scientists had approached drawing the genealogy of organisms, the Tree of Life, from fossils and living species ever since Darwin’s On the Origin of Species in 1859 convincingly argued that all of life was interconnected by a web of ancestry and descent.

At that time, two core members of the evolutionary primatology faculty at CUNY were carrying out a thorough review of primate evolution. They were my graduate school mentors who published prolifically for decades. Eric Delson went on to cofound, and is, as of this writing, the head of the New York Consortium of Evolutionary Primatology (NYCEP), and Frederic Szalay is now retired after having had a tremendous impact on the field. While they were frequently on opposite sides of the cladistics debate, there was between them a mutual respect and appreciation for each other’s opinions and expertise. They spent several years jointly writing Evolutionary History of the Primates, an indispensible resource which immediately became a classic when published in 1979.

As they cowrote their magnum opus I became involved as an avid listener, occasional sounding board, and also an enthusiastic contributor. It became clear that there was a topical gap in their coverage. While Eric and Fred commanded an unparalleled knowledge of the evolution of Old World anthropoid primates, and of Madagascar’s lemurs and the early primates, it was not so for New World monkeys. Little was known then about platyrrhine evolutionary history. At that time I was writing my doctoral thesis, Phylogeny, Evolution and Classification of New World Monkeys (Platyrrhini, Primates), and I was given the opportunity to present some new ideas about their phylogeny, how they should be extensively reclassified, how their adaptive diversity unfolded, and how long-lineages played an important role in platyrrhine evolutionary history. I was privileged to be heard and trusted as Eric and Fred filled in what was missing from the platyrrhine chapter of their book, based on the research for which I earned a PhD in the same year. For that, I will always be grateful to them.

I went on to publish papers and edited volumes with Eric, Fred, and 100 other collaborators—men, women, professionals, peers, and students. My inner circle of colleagues with whom I have continued to work is narrow, but our combined network is broad, spanning five continents and fields as diverse as geology, ethology, conservation, behavioral ecology, software engineering, 3-D computer graphics, scuba diving, and more. This is the nature of scientific research and discovery. It is only because of the work of this dedicated network of professionals, and many others, that the story of the New World monkeys’ odyssey can be told.

Fifty years ago, when I began to study primatology, the world was a different place and I could never have imagined that the rainforest would be disappearing and the primates living there would be facing extinction. I am grateful for the opportunity to study these magnificent animals, to learn from them, and to write this book. As a small token to aid in the efforts to save the platyrrhines and other primates, I feel it is only right to donate a portion of the proceeds of the sale of this book to primate conservation efforts.

CHAPTER 1

WHAT IS A NEW WORLD MONKEY?

This book is about the evolutionary odyssey of New World monkeys, the South and Middle American platyrrhines, though it is mostly about their evolution in South America where most of platyrrhine history was played out. Their odyssey appears to have begun 45–50 million years ago when an ancestral population of monkeys arrived in South America to found one of the most diverse and colorful adaptive radiations produced by the Order Primates. A robust view of what platyrrhines have become and how can be gleaned from the living animals today and the fossil record, which, though still limited, documents the major features of New World monkey evolution during roughly the last 25 to 35 or 40 million years of their existence, although the record is exceedingly sparse for periods older than 20 million years. Unlike other major primate groups, the history of New World monkeys is one in which the separate lines of descent leading to many of the 16 extant genera recognized herein can be traced back in time for millions of years by fossils and by molecules. This long-lineage pattern is what gives the structure of platyrrhine evolution its distinctive shape, and it is a centerpiece of this book. It also serves as a poignant point of reflection in thinking about the platyrrhines’ future. Fourteen of the 16 living genera include species that are now classified, according to the International Union for Conservation of Nature (IUCN), as Critically Endangered or Vulnerable.

There is an abundant record of fossil South American mammals that dates back nearly to the beginning of the Age of Mammals, about 66 million years ago. However, the oldest New World monkeys we know of date back only 36–40 million years. Given that South America was an island continent for most of the last 66 million years, as the world’s living mammals began to flourish and before Isthmus of Panama emerged to firmly connect North and South America 3 million years ago, the questions arise: Where did their ancestors come from, and how did they get there? Whether primates originally came from Africa by rafting across the Atlantic Ocean on a floating mat of vegetation, or mostly overland from North America, two scenarios detailed in chapter 10, they arrived as pioneers in a landscape where monkeys had never existed before.

The ways in which these animals evolved and thrived on the isolated continent, always in the trees, is a history of radical change and enduring stasis, novel adaptive solutions and predictable transformations. It is a story of giants, dwarfs, brainy predaceous tool users, dim vegetarians, fungus feeders, and bark-gnawing gum eaters. It is an account of cautious quadrupeds, acrobatic arm-and-tail swingers, quiet nocturnal denizens, and roaring diurnal howlers. Their mating strategies include codominant monogamists, and alpha males and alpha females living in large social groups. In some species females use scent to control the breeding success of their daughters; in another, males queue up on big branches waiting their turn to copulate with one female. By inhabiting a range of niches so varied in ecological and anatomical solutions to feeding and locomotion, or in social arrangements for group living, mating, and rearing offspring, platyrrhines have produced one of the most diverse adaptive radiations among the primates.

How did this happen? The present is key to understanding the past. There are two intertwined models describing how platyrrhine evolution has unfolded, the Long-Lineage Hypothesis and the Ecophylogenetic Hypothesis. What this means is that the many kinds of monkeys we see today have been around for millions of years and that some have existed for at least 20 million years with little change in their ecological situation, to the extent that their adaptations are documented in the fossil record. Furthermore, at another level, genetically related subgroups of New World monkeys, clusters of genera linked by their shared phylogenetic histories, have found success in various ecological niches defined by the particular sets of characteristics inherited from their remote common ancestors. Today, more than a dozen extant platyrrhine species belonging to all the six major subgroups can be found packed into a single rainforest locality, forming a harmonious monkey community. The fossil record suggests that this phylogenetic and ecological framework may have been in place for the entirety of the modern platyrrhines’ long-lived existence, setting the stage for the evolution of more refined divisions of niches by the procession of the living genera and species.

As further discussed below, I use the term lineage to mean a genus-level line of descent, an evolutionary stream carried in DNA that is embodied in a species, or a collection of intimately related species, and is manifested as a distinct ecological lifestyle. When examining an entire radiation such as the platyrrhines, the taxonomic level of genus, not species, is the most appropriate perspective. Genera exemplify and define the combinations of anatomical and behavioral characteristics that are of particular ecological relevance, and that separate all the significant lines of descent that compose an adaptive array.

FIG. 1.1. Cladogram of the major groups of living primates mapped with the distribution of external nose shapes. Primate images courtesy of Stephen Nash.

What is a monkey?

We regularly call platyrrhines monkeys, but the word monkey has no scientific significance. There are two groups of primates commonly called monkeys, the New World monkeys and the Old World monkeys. However, they are not grouped together in formal taxonomic language because they lack the evolutionary connection that is the main reason animals are classified jointly in particular groups: a genetic, or phylogenetic, relationship. The two groups we call monkeys are less closely related than the use of the word monkey suggests. In fact, the primates we call Old World monkeys, such as olive baboons and the rhesus macaques, are more closely related to apes than they are to New World monkeys (fig. 1.1). New World monkeys are a separate group entirely, an offshoot of the primate family tree that appeared about 25 million years before the earliest appearance of today’s Old World monkeys and apes documented in the fossil record. The sameness implied by the word monkey is an anachronism that may date back to the 14th century, according to the Oxford English Dictionary, an old-fashioned word based on an equally old, pre-evolutionary idea about the natural world. It was meant to distinguish these animals from apes and the other nonhuman primates, the lemurs, lorises, galagos, and tarsiers of Africa and Asia. They are all very different from monkeys and apes in many ways, including the structure of their skulls, their dentition and skeletons, sensory systems, and behavior, reflecting separate evolutionary histories.

Taxonomic groups that are formally recognized and named as units in classifications, such as species, genus, family, and order, are called taxa, the plural form of the word taxon. The term taxonomy, which means arrangement, is derived from the words taxon and taxa. The groups mentioned thus far—primates, platyrrhines and New World monkeys, Old World monkeys, apes, tarsiers, lemurs, lorises and galagos—are all taxa that have formal names in classifications as well as these common names. But monkey is not a taxon and has not been thought of in that way since Darwin introduced us to evolution and phylogeny, and reinforced the notion that classification should be based on relatedness, which previously was only a vague idea. The word is applied to two different groups of taxa that are actually not each other’s closest relatives.

Some labels for primate groups are like nicknames and have no scientific standing. Sometimes they are holdovers from the pre-Darwinian period when natural history was not a secular enterprise and scholars used such terms to express their ideas about how far a group was stationed along an imagined trajectory, a ladder of ascent, reflecting the Scale of Nature or the Great Chain of Being that emanated from Creation. Humans were considered the pinnacle of creation and all other animals were said to occupy standings below that high point, as lower grades or stages in the procession of life. The early naturalists arranged their classifications accordingly and their informal language sometimes expressed those views. Thus the term monkey referred to the group of primates grouped with the apes as higher primates and gradistically situated between apes and the lower primates, the tarsiers, lemurs, lorises, and galagos. The latter were called prosimians, meaning near monkeys and apes. Eventually, Darwin made it quite clear that the two great groups of monkeys were distinct: Old World monkeys are the closest living relatives of apes and New World monkeys are a separate line of evolution within the monophyletic group—the unique descendants of a common ancestor—we call Anthropoidea, informally anthropoids, the taxonomic equivalent of higher primates, composed of New World monkeys, Old World monkeys, apes, and humans.

Even in the Darwinian era grade-thinking persevered throughout biology, and particularly when it came to discussing nonhuman primates as human relatives. Darwin’s most effective scientific ally, Thomas Henry Huxley, wrote of primate diversity and evolution in 1863, in Man’s Place in Nature, four years after On the Origin of Species was published. He said, Perhaps no order of mammals presents us with so extraordinary a series of gradations as this—leading us insensibly from the crown and summit of the animal creation down to creatures, from which there is but a step, as it seems, to the lowest, smallest, and least intelligent of the placental Mammalia. In the next 100 years the gradistic mindset faded from research practice but it still endures in our everyday language as a convenience, hence the word monkey. As a way of viewing the world, however, gradistics failed with the onset of a methodological revolution known as cladistics that occurred in the 1960s, which sought to organize and classify groups according to their placement on the appropriate branch, or clade, of the phylogenetic Tree of Life, as will be fully discussed later. That failure had important consequences in spurring a wholesale re-thinking of platyrrhine evolution.

The geographic modifier in the name New World monkey is also an anachronism. Since the Age of Discovery, in the 15th century, European writers have referred to the Western Hemisphere as the New World, ostensibly discovered by Columbus, in contrast to the Old World, comprising Eurasia and Africa. Similarly, platyrrhines are also often called Neotropical primates, meaning primates of the New World tropics. In an ecological sense, that term may conjure up a misunderstanding about the habitats where platyrrhines live, and what the relevant environments of South America in particular look like. It delimits the wide swath of South and Central America straddling the equator, the tropical zone, where the climate is moist, warm or hot all year round and supports dense, evergreen, jungle vegetation. But that landscape is not all continuous rainforest, and platyrrhines are not strictly jungle dwellers.

South America is a vast continent that is two-and-a-half times the size of the Amazonian rainforest, where most platyrrhines are found. Another vitally important tropical and subtropical region, the Atlantic Forest of southeastern Brazil, supports a smaller, unique ensemble of monkeys including several endemic forms, meaning they are found nowhere else in the world (fig. 1.2). Most of them are presently endangered as a result of the wholesale decimation of the Atlantic Forest that occurred during the last 500 years which, as discussed in chapter 11, has reduced their habitat to disconnected, relict forest fragments about one-tenth the size it was when European colonists first arrived in Brazil half a millennium ago.

FIG. 1.2. Map of South America and its major ecological zones.

The full geographic range encompassed by monkeys in South America extends from the northern edge rimming the Caribbean Sea and the Atlantic and Pacific Oceans, to northern Argentina in the distant south. The habitats mapped out in this enormous expanse are predominantly evergreen rainforests, semideciduous forests where trees lose their leaves seasonally, and open-country savannas, grasslands, and shrublands. Primates can be found in all these areas, though the greatest concentration of species and the most densely packed communities of platyrrhine species occur in the rainforests. In drier, more sparsely vegetated zones, only a few generalist species of monkeys, or those with a special set of adaptations to procure food from a limited, local supply, manage to get by. There they are often found in narrow strips of forest situated alongside water courses. Of all things, New World monkeys need trees no matter where they live.

Why is this so? Comparing the vegetation map of South America with the distribution maps of the living species highlights an intensely interesting question about platyrrhine evolution: Why are there no terrestrial species? In Africa, another enormous continent with a similarly varied distribution of habitats, Old World monkeys have evolved an impressive array of terrestrial and arboterrestrial species, living in forests and even extending into bone-dry, near-desert areas. In contrast, while platyrrhines are obviously an exclusively arboreal radiation, there is nothing about the design of their bodies or their dietary needs that makes it impossible for a New World monkey to habitually visit the ground and benefit from it. Actually, some species do so occasionally in order to cross large gaps in the forest or obtain drinking water in drier places when the forest does not provide them with enough because watery fruits are in short supply.

Juvenile monkeys sometimes play on the ground. Clever capuchin monkeys living in swampy areas have even learned to collect clams on the ground when the tide recedes. Yet, no living platyrrhines have evolved terrestrial adaptations or a terrestrial lifestyle. Given their long evolutionary history, however, and knowing that South American forests have waxed and waned over the entire continent, it may be that the fossil record will at some point turn up a ground-dwelling New World monkey. In fact, there is already a hint of this in the few remains of an extinct Caribbean platyrrhine, Paralouatta, to be discussed in a later chapter. With all that biologically built-in ecological flexibility and a vast area of the continent as potentially exploitable habitat, under the forest canopy and beyond, the absence of living terrestrial platyrrhines seems quite the mystery.

What is a platyrrhine?

The technical name for New World monkeys is Platyrrhini; platyrrhines, colloquially. It means flat- or wide-nosed. The name was given to them in 1812 by the French naturalist Étienne Geoffroy Saint-Hilaire, who was then sorting and cataloging specimens of mammals held in the collections of the Muséum National d’Histoire Naturelle in Paris. He found that the shape of the nose turned out to be a useful way to identify several groups of primates. In platyrrhines the nostrils are widely spaced and laterally facing, separated by a broad fleshy strip between the openings (fig. 1.1). In some, such as the Saki Monkey, the expression of this characteristic is rather extreme. A contrasting pattern occurs among Old World monkeys and apes, which have nostrils that are closely spaced and separated by a thin band of flesh. They are classified as Catarrhini; catarrhines, informally, meaning downwardly facing nose.

These distinctions, like many others used in identifying and classifying primates, are exhibited consistently among platyrrhines, but not universally. To see an exception, one has only to look at the gorilla-like face and nose of the largest living platyrrhine, the Muriqui, with its adjacent nostrils. The usefulness of employing these names, terms stemming from the same Greek root word for nose, rhine, is that they are physically descriptive and they bind together a naturally paired, phylogenetic set of primates. Platyrrhines and catarrhines are the two branches of the extant anthropoid primates, the taxonomic group consisting of New and Old World monkeys, apes, and humans that arose monophyletically from an exclusive common ancestor.

Because the nose is made of flesh, which under nearly all circumstances does not fossilize, paleontology is limited in what it can tell us about the evolution of the platyrrhine nose, and the contrasting catarrhine pattern as well; but is there is a way to reconstruct their morphological histories by examining the living animals? If so, what would the nose have looked like in the last common ancestor of anthropoids? Would its shape have been platyrrhine, catarrhine, or something else? In other words, what nose shape is the primitive form in anthropoids?

In fact, we have good reason to infer that in the first anthropoids the nose was platyrrhine-like. To arrive at that interpretation, we use information on the comparative soft anatomy of extant animals in order to envision the past, as a hypothesis, with an assist from fossil evidence. This method, called character analysis, involves examining the similarities and differences of inherited traits—or presumably inherited, since links between genes and anatomy are still difficult to establish—in closely related forms, with the aim of tracing the sequence in which the details of those features evolved. The approach applies to any observable trait and it is important for understanding how and why evolutionary changes happened functionally, although it does not always lead to adaptive insight because we often do not know the benefit of one pattern or another even when they are linked historically.

In the case of noses, character analysis entails invoking the primate cladogram, a simplified family tree, as a map that guides us toward the common morphological denominators shared between the animals in question and their nearest relatives: platyrrhine and catarrhine noses are compared with the nose of the tarsiers of Southeast Asia (fig. 1.1). Tarsiers are small, giant-eyed, nocturnal predators, and they have an external nose that is a close match for a platyrrhine’s even though most of the animal’s other features look almost nothing like a platyrrhine or any anthropoid. Since its broad, laterally facing nostrils and pug nose conform to the New World monkey pattern, we can infer that the ancestral anthropoids also shared that morphology, perhaps comparable to a pygmy marmoset’s.

The scientific logic behind this conclusion is that it is the most parsimonious, or efficient, explanation of the taxonomic distribution of nose shape among the three groups. Reasoning this way implies that New World monkeys inherited a tarsier-like pattern with little change from the original condition, and that catarrhines later evolved the newer, derived shape. An alternative inference would hypothesize that the catarrhine shape was ancestral in anthropoids. But that means we would have to explain why the same wide-nosed morphology evolved twice in this one monophyletic group, once in the line leading to tarsiers and a second time in the ancestors of New World monkeys. Minimizing such parallelisms, which means minimizing the number of hypothesized evolutionary changes required to satisfy existing morphological and taxonomic conditions when there is no reason to think otherwise, is basic to the protocol of the character analysis strategy. That’s what is meant by parsimony, and explanatory efficiency. Regarding the evolution of the two nasal shape patterns in this exercise, we still have no sound explanations concerning functional significance, but we do have possible explanations for some of the more oddly shaped, superwide external noses found in a few living platyrrhines, such as the Saki Monkey, as we shall see below.

Focusing on the nose to identify a primate or other mammal, and formalizing it descriptively in the structure of a taxonomic name, is a common practice in mammalogy. The rhinoceros, formally the genus Rhinoceros, meaning horn-nosed in Greek, is a familiar example. Among catarrhine primates, there is the Proboscis Monkey, Nasalis, meaning of or pertaining to the nose in Latin, a genus in which females have a striking, projecting nose and males have an extremely large, pendulous nose.

It may seem odd or even trivial that scientists continue to sort major, higher taxonomic groups of primates such as the platyrrhines and catarrhines by the shapes of their noses because of a tradition dating back to the early 1800s, particularly if we have few ideas about any adaptive significance or benefit to the different morphologies. True, nose shape once served as nothing more than a convenient descriptor and identifier for early naturalists who had limited knowledge of the deeper anatomy, or the actual lives, of the animals whose remains they studied. But as understanding of anatomy and behavior accumulated, this approach began to yield important clues about primate evolution.

The Order Primates is divided into two major extant groups (fig. 1.1), called Strepsirhini (strepsirhines) and Haplorhini (haplorhines). The extant strepsirhines include lemurs, lorises, and galagos. They have wet noses with slitlike, comma-shaped nostrils: strepsirhine, from the Greek streph, means twisted nose, a reference to the shape of the nostril’s opening. The haplorhines are tarsiers, New World monkeys, and Old World monkeys, apes, and humans. They have dry noses with rounded nostrils. Hapl, also Greek, means simple, an illusion to the rounded nares.

We now understand that these names represent profoundly different biological systems. They are only parts of a larger anatomical complex that is functionally and behaviorally important in regulating communication and even how these animals tend to perceive the world, how the two groups gather fundamental information about their surroundings. While all primates are highly competent visual animals, the strepsirhine primates, which are mostly nocturnal and live in low-light conditions, favor olfaction over vision as sensory input. Their acute sense of smell is tied to the structure of their noses. Haplorhine primates, who are mostly diurnal, favor visual input over olfactory information. Consequently, they are less dependent on the anatomy of the nose, and the snout has evolved in another direction.

The outward, easily seen differences in nostril shape, traits that are still without a good adaptive interpretation, are accompanied by other, functionally significant features. A slit or rounded nostril is one piece of a more important whole, the nose itself. Strepsirhines have a bulbous external nose, much like a dog’s, covered in a perpetually moist, textured skin. Situated at the very tip of the bony snout, the nose extends as a broad flap directly into the mouth, and splits the hairless upper lip in the middle. As a result, the mouth is not ringed by muscle, and no lemur, loris, or galago is able to control the contour of their lips to shape the mouth to produce facial expressions—no smiling, grimacing, or pouting.

The textured surface of the wet nose is designed to collect molecules of scent from the air they breathe and shunt them down a strip of skin toward a chemosensory organ, the vomeronasal, or Jacobson’s organ, situated in the mouth