NORTHWESTERN UNIVERSITY Morphology of the Hindlimb and Correlations to Locomotor Tendencies in Platyrrhines a DISSERTATION SUBMI

Home , Department of Loreto, Micodon, Patasola (mammal), Philip Hershkovitz, Prehensility, Suspensory behavior

NORTHWESTERN UNIVERSITY

Morphology of the Hindlimb and Correlations to Locomotor Tendencies in Platyrrhines

A DISSERTATION

SUBMITTED TO THE GRADUATE SCHOOL IN PARTIAL FULFILLMENT OF THE REQUIREMENTS

For the degree

DOCTOR OF PHILOSOPHY

Field of Driskill Graduate Program in the Life Sciences

Michael Scott Mutehart

EVANSTON, ILLINOIS

September 2018 2

Abstract

Platyrrhines are an enigmatic and intriguing radiation of New World monkeys that currently inhabit the western hemisphere from Argentina to Mexico. Platyrrhini, a taxonomic parvorder within Primates, is their formal taxonomic designation, as they represent the sister group of the

Catarrhini or all of the Old World monkeys and apes. These platyrrhine monkeys are diverse in terms of body size, their ecology, and in their movement patterns. From the smallest anthropoid,

Cebuella pygmaea, to the large bodied Brachyteles, platyrrhines inhabit the Amazon rain forest basins, the Atlantic coastal forests of Brazil, and the Central American rain forests. Their locomotor abilities range from arboreal quadrupedalism, to climbing and leaping preferences, to forelimb suspensory behaviors. It is the intention of this study to identify anatomical correlates in the hind limb of these New World monkeys relative to their respective movement patterns.

Forty-five species of platyrrhines, representing hundreds of individual specimens, were measured and analyzed to determine if morphology of the hip and pelvis, thigh and proximal femur, and/or knee, could be mapped to their known locomotor behavior. The features examined were chosen on the basis of previous studies conducted on platyrrhine primates or other mammals where hindlimb anatomy had been correlated with positional behavior. Behavioral studies that included quantified and qualitative descriptions were examined. Statistical analyses, including regressions and the analysis of variance were employed to determine if correlations between morphology and movements could be specified. 4

Results from this study indicated that morphological adaptations for leaping are more generalized within platyrrhines than in “prosimian” primates. Dorsal ischial projection was found to be a good indicator of (vertical) leaping in pithecids for example, but not among callitrichids nor among platyrrhines as a whole. There are elements of the platyrrhine postcranium that are linked to climbing including a wide pubis, robust intertrochanteric crest and posteriorly placed lesser trochanter. The New World brachiators have increased their joint excursion range at the hip and evidence two features of the knee, a wide patellar groove and gracile medial condylar lip, that help to distinguish them morphologically from the other groups.

Overall, this study demonstrates that the hindlimb morphology of the platyrrhines examined here are more generalized in nature and they are not as strongly indicative of the distinctive movement patterns as has been noted previously in “prosimian” primates or for the brachiating apes. Callitrichids, in particular (excluding Cebuella, the pygmy marmoset), although exhibiting differences in frequency and style of locomotor behaviors, actually do not vary very much morphologically in their hindlimb anatomy. While several monkeys, including Cebuella and

Ateles species, stand out as being genuinely unique morphologically and do not fit the expectations of the movement hypotheses developed in this study. In the end, this project has identified features of the hindlimb that are indicative of certain locomotor behaviors, while also illustrating platyrrhine locomotor behavior in terms of a rather generalized hindlimb morphology.

Acknowledgements

This work would not have been possible without the help and support of many individuals and institutions. I am grateful to the Driskill Graduate Program in the Life Sciences for their support throughout my graduate career. I am especially indebted to the program committee members and

Dr. Steve Anderson for their unending guidance and patience throughout my time in the program. Special thanks to the Field Museum in Chicago, the National Museum (Smithsonian) and the American Museum in New York for giving me access to their collections. I would like to extend specific thanks to Dr. Martha Tappen for allowing me access to the Neil Tappen primate collection housed at the Department of Anthropology at the Univeristy of Minnesota.

This journey began many years ago when I was an undergraduate at Northern Illinois University.

I would like to extend my gratitude to my undergraduate professors who made me believe that a career in primate studies was possible. Thanks to Dr. Leila Porter for showing me that primate behavior and ecological studies should be on the same level as morphology and for fostering in me a desire to learn as much as possible about the platyrrhines.

I would not have survived graduate school without the help and inspiration of my colleague and lab partner, Dr. Denitsa Savakova. Thank you for all the fun times, interesting conversations and unique experiences that made the graduate school years bearable. I am grateful for our friendship.

I would not have been able to make this study work without the help, insight, perspective, and guidance of my dissertation committee. Dr. Dan Gebo provided years of inspiration and I am 6 forever grateful for your guidance during my undergraduate years. Dr. Larry Cochard, thank you for your unique perspective to research and teaching. Dr. Brian Shea, thanks for all the advice and help from day one. I will forever remember our conversations, which, I believe have covered every topic imaginable.

I am forever indebted to my thesis advisor, Dr. Marian Dagosto. Marian, you have provided me with years of friendship, immeasurable support, mentorship, and shared with me your vast knowledge and intellect. Thank you for all of your support and for guiding me through this turbulent process. Your example of a quiet and mature demeanor and years of scholarship has not gone unnoticed.

My family has been by my side throughout this process and I am grateful for all of their support.

My parents have been helpful in so many ways and I will always cherish their love. My wife and daughter were brought into this through no fault of their own, and have always been completely devoted to helping me through to the the finish line. Thank you.

Lastly, I would like to thank the many dozens of researchers who have come before me who spent their time and money studying primates in the wild, obtaining behavioral and body weight data. That research and data is invaluable and this study would be impossible without it.

Dedication To my daughter, Eva Bear When you were born, I had a ‘legitimate’ reason to buy everything monkey! To my wife, Brandy Even in the difficult times, you made me believe in myself! You both have my unending and complete love.

Table of Contents

Abstract ...... 3 Acknowledgements ...... 5 Dedication ...... 7 Table of Contents ...... 8 List of Tables and Figures ...... 13 Chapter 1 ...... 22 Introduction ...... 22 Objectives...... 24 Significance ...... 24 Positional and Locomotor Behavior ...... 26 Previous work...... 26 Definitions of Locomotor Behavior ...... 30 Morphological Studies ...... 34 The Hip ...... 34 The Knee ...... 36 Studies Incorporating Morphology and Behavior ...... 36 Hypotheses ...... 39 Leaping: ...... 39 Quadrupeds: ...... 41 Climbing: ...... 42 New-World Brachiation: ...... 43 Platyrrhine Phylogeny ...... 44 How to Interpret the ‘Function’ in Functional Anatomy? ...... 48 Chapter 2 ...... 49 Materials and Methods ...... 49 9

Introduction ...... 49 Taxa ...... 50 Issues affecting the inclusion of taxa (species) ...... 50 Issues affecting the inclusion of individual specimens ...... 51 Data Collection and Analysis ...... 56 Data Collection ...... 56 Specimen Measurements ...... 60 Measurement Error ...... 61 Morphology ...... 62 Specimen collection ...... 62 Features examined ...... 64 Linear Measurements ...... 65 Non-Quantitative Features ...... 68 Presence Robustness of the Intertrochanteric Line ...... 69 Lateral Margin of the Patellar Groove ...... 71 Orientation of the Femoral Condyles ...... 73 Femoral Head Height Compared to Greater Trochanter Height ...... 74 Presence/Robustness of Intertrochanteric Crest ...... 76 Depth of the Trochanteric Fossa ...... 78 Position of the Lesser Trochanter ...... 80 Medial Margin of the Patellar Groove ...... 82 Femoral Condyle Symmetry ...... 84 Body Size ...... 86 Statistical Analyses Used in this Study ...... 92 Chapter 3 ...... 94 Results ...... 94 Introduction ...... 94 Leaping Hypotheses ...... 99 Hypothesis 1a ...... 99 Dorsal Projection of the Ischium ...... 99 10

Distal Projection of the Ischium ...... 104 Hypothesis 1b...... 109 Presence/Robustness of Intertrochanteric Line ...... 109 Ilium Width ...... 111 Femoral Neck Length ...... 115 Femoral Neck Thickness ...... 118 Femoral Neck Angle ...... 121 Posterior Articular Surface of the Femoral Head ...... 125 Greater Trochanter Width ...... 128 Hypothesis 1c ...... 133 Femoral Condyle Symmetry ...... 133 Patella Groove Width ...... 137 Lateral Margin of the Patellar Groove ...... 140 Orientation of the Femoral Condyles ...... 142 Quadrupedal Hypotheses ...... 145 Hypothesis 2a ...... 145 Ischium Length ...... 145 Hypothesis 2b...... 149 Femoral Neck Length ...... 150 Femoral Neck Angle ...... 150 Posterior Articular Surface ...... 150 Greater Trochanter Width ...... 151 Hypothesis 2c ...... 152 Patellar Groove Width ...... 152 Femoral Condyle Symmetry ...... 152 Femoral Condyle Orientation...... 153 Climbing Hypotheses ...... 154 Hypothesis 3a ...... 154 Pubic Ramus Width ...... 154 Ilium Width ...... 155 11

Hypothesis 3b...... 156 Femoral Head Height Compared to Greater Trochanter Height ...... 156 Anterior Femoral Head Articular Surface ...... 158 Posterior Articular Surface of the Femoral Head ...... 160 Presence/Robustness of Intertrochanteric Line ...... 160 Presence/Robustness of Intertrochanteric Crest ...... 161 Depth of the Trochanteric Fossa ...... 163 Position of the Lesser Trochanter ...... 165 Hypothesis 3c ...... 167 Medial Femoral Condyle Length ...... 167 Suspensory Hypotheses ...... 169 Hypothesis 4a ...... 169 Ischium Length ...... 169 Acetabulum Width ...... 169 Acetabulum Height ...... 171 Hypothesis 4b...... 173 Femoral Head Height ...... 173 Femoral Head Width ...... 174 Posterior Articular Surface of the Femoral Head ...... 176 Anterior Articular Surface of the Femoral Head ...... 177 Femoral Head Height Compared to the Height of the Greater Trochanter ...... 177 Position of the Lesser Trochanter ...... 178 Hypothesis 4c ...... 179 Ratio of Femoral Head Size to Femoral Neck Size ...... 180 Ratio of Acetabulum Width to Femoral Head Size ...... 183 Hypothesis 4d...... 185 Medial Condyle Length ...... 185 Lateral Condyle Length ...... 186 Intercondylar Width ...... 187 Patellar Groove Width ...... 189 12

Medial Margin of the Patellar Groove ...... 189 Lateral Margin of the Patellar Groove ...... 191 Chapter 4 ...... 193 Discussion ...... 193 Introduction ...... 193 Summary of the Hypotheses ...... 194 Leaping ...... 194 Climbing ...... 198 Suspensory Behavior ...... 200 Quadrupeds ...... 202 Taxa that ‘Stand Out’ ...... 207 Factors that Influence the Results ...... 213 Interspecific Scaling of Variables ...... 213 Muscle Rugosity and Osteological Markings ...... 214 Bodyweight Data ...... 216 Body Size, Ecology and Locomotion ...... 218 Locomotor and Behavioral Data ...... 220 Locomotor Categories and the Pitfalls of ‘Lumping’ Behavioral Modes ...... 222 Sample Size ...... 224 Species Data ...... 225 Missing Data ...... 226 Future Studies ...... 227 Locomotor Behavior in Fossil Platyrrhines ...... 231 Conclusion ...... 234 References ...... 236 Appendix 1 ...... 278 Appendix 2 ...... 305

List of Tables and Figures

Table 1.1 - Locomotor Studies of Platyrrhine Primates ...... 30

Table 1.2 - Hindlimb Features and Locomotor Categories ...... 39

Table 2.1 - Extant Platyrrhine Genera ...... 50 14

Table 2.2 - Platyrrhine Species Obtained for this Study ...... 55

Figure 2.1 - Photographic Set-up ...... 58

Table 2.3 - Measurement Error Percentage by Feature ...... 62

Table 2.4 - Features Examined in this Study ...... 67

Figure 2.2 - Pelvis Measurements ...... 67

Figure 2.3 - Pelvis Measurements Cont...... 67

Figure 2.4 - Femoral Measurements ...... 68

Table 2.5 - Non-Quantitative Features ...... 69

Figure 2.5 - Alouatta caraya - Prominent intertrochanteric line (1) ...... 70

Figure 2.6 - Saimiri boliviensis - Absence of intertrochanteric line (4) ...... 71

Figure 2.7 - Cacajao calvus - Rounded lateral patellar lip (1) ...... 72

Figure 2.8 - Ateles fusciceps robustus - Sharp/pronounced lateral patellar lip(3) ...... 73

Figure 2.9 - Callimico goeldii - Posteriorly oriented femoral condyles (red arrow), distally oriented condyles (blue arrow) and distally and posteriorly oriented condyles (green arrows) ...... 74

Figure 2.10 - Callimico goeldii - Femoral head above greater trochanter (2) ...... 75

Figure 2.11 - Chiropotes satanas - Femoral head equal to greater trochanter height (1) ...... 76

Figure 2.12 - Ateles fusciceps robustus - distinctly visible crest (1)...... 77

Figure 2.13 - Callithrix jacchus jacchus - barely visible crest (3) ...... 78

Figure 2.14 - Callimico goeldii - shallow trochanteric fossa (3) ...... 79 15

Figure 2.15 - Ateles geoffroyi - Deep trochanteric fossa (1) ...... 80

Figure 2.16 - Cebuella pygmaea - Medial/midline placed lesser trochanter (1) ...... 81

Figure 2.17 - Alouatta caraya - Posterior placement of lesser trochanter (3) ...... 82

Figure 2.18 - Alouatta caraya - Robust medial condyle lip (3) ...... 83

Figure 2.19- Leontopithecus rosalia - Rounded medial condyle lip (1) ...... 84

Table 2.6 - Species, Origin and Sexes of Specimens Obtained for this Study ...... 85

Table 2.7 - Published Platyrrhine Bodyweight Data ...... 90

Table 2.8 - Specimens with Associated Bodyweight ...... 92

Table 3.1a – Basic stats for platyrrhine-wide regressions discussed in this chapter. Non-significance is indicated in red. Confidence intervals that cover .333 are in bold...... 96

Table 3.1b – Basic stats for callitrichid regressions discussed in this chapter. Non-significance is indicated in red. Confidence intervals that cover .333 are in bold...... 97

Table 3.1c – Basic stats for pithecid (individual specimens) regressions discussed in this chapter. Non- significance is indicated in red. Confidence intervals that cover .333 are in bold...... 98

Figure 3.1 – Platyrrhine Wide - Regression of species means dorsal projection of the ischium vs. body mass...... 101

Table 3.2 - ANCOVA Dorsal Projection ...... 102

Figure 3.2 - ANCOVA - Dorsal Projection: Black = leapers, Red = Quadrupeds, Blue = Climbers, Green =

Brachiators ...... 102 16

Figure 3.3 – Callitrichid Only - Regression of species means dorsal projection of the ischium vs. body mass...... 103

Figure 3.4 - Within Pithecids - Regression of individual specimens dorsal projection of the ischium vs.

LCL ...... 104

Figure 3.5 - Platyrrhine Wide - Regression of species means distal projection of the ischium vs. body mass ...... 106

Figure 3.6 - Callitrichid Only - Regression of species means distal projection of the ischium vs. body mass.

...... 107

Figure 3.7 - Regression of individual specimens distal projection of the ischium vs. LCL ...... 108

Table 3.3 – Summary – Hypothesis 1a ...... 108

Table 3.4 - Analysis of Variance - Test for equal means - intertrochanteric line ...... 109

Table 3.5 - Tukey's Pairwise Comparison - intertrochanteric line ...... 110

Table 3.6 – Percentages by Measurement Category ...... 110

Figure 3.8 - Least Squares Means Histogram - intertrochanteric line ...... 111

Figure 3.9 – Platyrrhine Wide - Regression of species means ilium width vs. body mass ...... 113

Figure 3.10 – Callitrichid Only - Regression of species means ilium width vs. body mass ...... 113

Figure 3.5 - Within Pithecids - Regression of individual specimens ilium width vs. LCL ...... 114

Figure 3.12 - Platyrrhine Wide - Regression of species means femoral neck length vs. body mass ...... 116

Figure 3.6 - Callitrichid Only - Regression of species means femoral neck length vs. body mass ...... 117 17

Figure 3.14 - Within Pithecids - Regression of individual specimens vs. LCL ...... 118

Figure 3.15 - Platyrrhine Wide - Regression of species means femoral neck thickness vs. body mass ... 119

Figure 3.16 - Callitrichid only - Regression of species means femoral neck thickness vs. body mass ...... 121

Figure 3.17 - Within Pithecids - Regression of individual specimens femoral neck thickness vs. LCL ...... 121

Figure 3.18 - Platyrrhine Wide Femoral Neck Angle in Degrees ...... 122

Figure 3.19 - Callitrichid Only - Femoral Neck Angle in Degrees ...... 123

Table 3.7 - Analysis of Variance - Test for equal means femoral neck angle ...... 124

Table 3.8 - Tukey's Pairwise Comparison femoral neck angle ...... 124

Figure 3.20 - Least Squares Means Histogram - Femoral Neck Angle ...... 125

Figure 3.21 - Platyrrhine Wide - Regression of species means post. articular surface vs. body mass ..... 126

Figure 3.22 – Callitrichid Only - Regression of species means post. articular surface vs. body mass ...... 127

Figure 3.23 - Within Pithecids - Regression of individual specimens post. articular surface vs. LCL ...... 128

Figure 3.24 - Platyrrhine Wide - Regression of species means greater trochanter width vs. body mass 130

Figure 3.25 - Callitrichid Only - Regression of species means greater trochanter width vs. body mass .. 131

Figure 3.26 - Within Pithecids - Regression of individual specimens greater trochanter width vs. LCL ... 132

Table 3.9 – Summary – Hypothesis 1b ...... 133

Figure 3.27 - Platyrrhine Wide femoral condyle symmetry ...... 134

Figure 3.28 - Callitrichid Only - femoral condyle symmetry ...... 135

Table 3.10 - Analysis of Variance - Test for equal means femoral condyle symmetry ...... 135 18

Table 3.11 - Tukey's Pairwise Comparison - Femoral Condyle Symmetry ...... 136

Figure 3.29 - Least Squares Means Histogram - femoral condyle symmetry ...... 137

Figure 3.30 - Platyrrhine Wide - Regression of species means patellar groove width vs. body mass ...... 139

Figure 3.31 - Callitrichid Only - Regression of species means patellar groove width vs. body mass ...... 139

Figure 3.32 - Within Pithecids - Regression of individual specimens patellar groove width vs. LCL ...... 140

Table 3.12 - Analysis of variance - test for equal means – lateral patellar lip ...... 141

Table 3.13 - Tukey's Pairwise comparison - lateral patellar lip ...... 141

Figure 3.33 - Least squares means histogram - Lateral patellar lip ...... 142

Table 3.14 - Analysis of variance - test for equal means - condyle orientation ...... 143

Table 3.15 - Tukey's Pairwise comparison - condyle orientation ...... 143

Figure 3.34 - Least squares means histogram - Femoral condyle orientation ...... 144

Table 3.16 – Summary – Hypothesis 1c ...... 145

Figure 3.35 - Platyrrhine Wide - Regression of species means ischium length vs. body mass ...... 147

Figure 3.36 - Callitrichid Only - Regression of species means ischium length vs. body mass ...... 148

Figure 3.37- Within Pithecids - Regression of individual specimens vs. LCL ...... 149

Table 3.17 – Summary - Hypothesis 2a ...... 149

Table 3.18 – Summary - Hypothesis 2b ...... 152

Table 3.19 – Summary - Hypothesis 2c ...... 154

Figure 3.38 - Platyrrhine Wide - Regression of species means pubic width vs. body mass...... 155 19

Table 3.20 – Summary Hypothesis 3a ...... 156

Table 3.21 - Analysis of variance - test for equal means - head height vs. trochanter height ...... 157

Table 3.22 - Tukey's Pairwise comparison - head height vs. trochanter height ...... 157

Figure 3.39 - Least squares means histogram - femoral head height compared to greater trochanter height ...... 158

Figure 3.40 - Platyrrhine Wide - Regression of species means ant. articular surface vs. body mass ...... 160

Table 3.23 - Analysis of variance - test for equal means intertrochanteric crest ...... 161

Table 3.24 - Tukey's Pairwise comparison intertrochanteric crest ...... 161

Figure 3.41 - Least squares means histogram - intertrochanteric crest ...... 162

Table 3.25 - Analysis of variance - test for equal means trochanteric fossa ...... 163

Table 3.26 - Tukey's Pairwise comparison - trochanteric fossa ...... 163

Figure 3.42 - Least squares means histogram - Trochanteric fossa ...... 164

Table 3.27 - Analysis of variance – position of the lesser trochanter - test for equal means ...... 165

Table 3.28 - Tukey's Pairwise comparison - lesser trochanter ...... 165

Figure 3.43 - Least squares means histogram - position of the lesser trochanter ...... 166

Table 3.29 – Summary - Hypothesis 3b ...... 167

Figure 3.44 - Platyrrhine Wide - Regression of species means medial condyle length vs. body mass ..... 168

Table 3.30 – Summary - Hypothesis 3c ...... 169

Figure 3.45 - Platyrrhine Wide - Regression of species means acetabulum width vs. body mass ...... 171 20

Figure 3.46 - Platyrrhine Wide - Regression of species means acetabulum height vs. body mass ...... 172

Table 3.31 – Summary - Hypothesis 4a ...... 172

Figure 3.47 - Platyrrhine Wide - Regression of species means femoral head height vs. body mass ...... 174

Figure 3.48 - Platyrrhine Wide - Regression of species means femoral head width vs. body mass ...... 176

Table 3.32–Summary - Hypothesis 4b ...... 179

Table 3.33 – Ratios of femoral head size to femoral neck size and acetabular width to head size ...... 180

Table 3.34 - Analysis of variance - test for equal means ratio of femoral head size to femoral neck size

...... 181

Table 3.35 - Tukey's Pairwise comparisons - ration of femoral head size to femoral neck size ...... 182

Figure 3.49 - Least squares means histogram - Ratio femoral head size to femoral neck size ...... 183

Table 3.36 - Analysis of variance - test for equal means ratio of acetabulum width to femoral head size

...... 183

Table 3.37 - Tukey's Pairwise comparison - ratio of acetabulum width to femoral head size ...... 184

Figure 3.50 - Least squares means histogram - Ratio of acetabulum width to femoral head size ...... 185

Table 3.38 – Summary Hypothesis 4c ...... 185

Figure 3.51 - Platyrrhine Wide - Regression of species means lateral condyle length vs. body mass ..... 187

Figure 3.52 - Platyrrhine Wide - Regression of species means intercondylar space vs. body mass ...... 188

Table 3.39 - Analysis of variance - test for equal means medial condyle lip ...... 189

Table 3.40 - Tukey's Pairwise comparison ...... 190 21

Figure 3.53 - Least squares means histogram - Medial lip of the patellar groove ...... 191

Table 3.41 – Summary - Hypothesis 4d ...... 192

Table 4.1 - Summary of level of support for the hypotheses ...... 205

Table 4.2 - Brief summary of known platyrrhine fossils ...... 230

Figure 4.1 – Within pithecid scatterlot of dorsal projection vs. LCL. Large data points are species means, small data points are individual specimens...... 233 22

Chapter 1

Introduction

The extant platyrrhines (neo-tropical monkeys) inhabit central and South America, from Mexico to Argentina. Platyrrhines not only have great diversity in size, from the smallest anthropoid

Cebuella pygmaea to the large atelines, they also show great diversity in terms of positional behavior. It is this movement and postural diversity relative to hindlimb anatomy that is the focus of this study.

The primary goal of this study is to determine if subtle shape and anatomical changes at the hip and the knee map to known differences in locomotor or postural behavior. At the group level, 23 analyses of callitrichids and pithecids will focus on the osteology and morphology of the pelvis, femur and tibia. At the larger all-inclusive platyrrhine wide level, it may be possible to determine if subtle morphology indicators are present throughout the radiation that map to their known locomotor modes.

Behavioral research has painstakingly been assembled by many previous researchers and this volume of work will be utilized to test movement and postural hypotheses across the species of platyrrhines examined here. It has been suggested that the platyrrhines are grouped somewhat reliably by their behavior, ecology and morphology (Rosenberger 2002). The atelines tend to be suspensory and are large bodied. The pithecines have been described as seed eaters

(Rosenberger 2002), the cebines are generally quadrupedal, and both the cebines and pithecines are medium sized. Callitrichids are small and diverse in terms of locomotor behavior. The aotines are the only nocturnal anthropoids.

The platyrrhine fossil record is relatively fragmented and very limited in terms of post-cranial elements. Researchers have argued that the earliest fossil platyrrhine, Perupithecus, appears to be the first platyrrhine described from the Eocene, approximately 36 million years ago (Bond et al. 2015). Evolving in relative isolation, platyrrhines exhibit characteristics and habits that differentiate them from their catarrhine relatives. For example, no platyrrhine has yet to adapt to terrestriality. Another feature that is unique to the platyrrhines is caudal prehensility a feature exhibited by several platyrrhine species (including the Atelidae). Callitrichids have evolved twinning, a feature that is rarely seen in other higher primates. Platyrrhines also exhibit cranial morphologies and a dental anatomy that distinguishes them from the catarrhines. Overall, these

New World monkeys have been isolated from other non-human primates for at least 36 million 24 years and this study can test whether this long time span and the lack of primate competitors has influenced their evolutionary history of arboreal locomotor adaptations.

Objectives The primary goal of this research is to identify locomotor adaptations in the underlying anatomy of the hip and knee of platyrrhine primates, using morphological data obtained from forty-five species of platyrrhine primate and locomotor (behavioral) data from corresponding species. The detailed hypotheses are included in Chapter 1 of this dissertation, along with a discussion of previously completed anatomical and behavioral studies.

Significance This study will add to the knowledge and understanding of morphological and locomotor relationships in platyrrhines. However, there are wider implications for this research as well.

With a fragmented and minimal fossil record, the questions regarding platyrrhine adaptation and evolution continue. As more information about the associations between morphology and behavior can be known, more can be said about the fossils that are known and those that may be discovered in the future. As some researchers have been able to hypothesize on the ancestral locomotor mode for platyrrhines/anthropoids (Dagosto 1988, 1990; Ford 1988;Gebo 1989;

Schon Ybarra and Schon 1987), including primary quadrupedalism, leaping, grasping and/or climbing, extant platyrrhines exhibit all of these locomotor behaviors to some extent. The more that can be elucidated by this study; the more that can be said about the relationships between 25 morphology and behavior, platyrrhine origins, and hopefully an expanding platyrrhine fossil record.

For many years, there have been suggestions about the relationships between anatomy (post- cranial), evolution, and behavior within primates in general. This study will help to answer some of these hypothesized morphological and behavioral relationships within platyrrhines. The

“prosimian radiation” of primates was ideal for this kind of morphological and behavior work as these primates possess a diverse locomotor repertoire and variable body sizes. In the 1960’s researchers such as Grand and Lorenz (1968) described shape differences in the lower limb of

Tarsius and made functional hypotheses; while Napier and Walker (1967) described a novel locomotor mode, vertical clinging and leaping. In the 1970’s Oxnard (1973), Walker (1974) and

Ward and Sussman (1979), amongst others, hypothesized about the foundational relationships between arboreal and terrestrial locomotor morphology, leaping and quadrupedal locomotor morphology and many other traits. Crompton (1984), building on locomotor understanding within the prosimians examined functional correlates in Galago. Rose (1973, 1974, 1984, 1993) identified post-cranial features that he linked to various locomotor behaviors in extant and fossil primates. Furthermore, as the behavior data was more rigorously quantified, subsequent researchers continued to identify morphology and behavioral correlates, Dagosto (1986), Gebo

(1986), and Gebo and Dagosto (1989) identified features of the “prosimian” ankle and foot that were linked to locomotor tendencies in early primate radiations. The morphological/behavior work was not relegated to prosimians alone, however, as Fleagle (1976 and 1977) identified various behaviors and anatomical correlates in the Southeast Asian catarrhines that added perspective to this type of work. Fleagle and Anapol (1992) and Fleagle and Meldrum (1988) 26 went beyond the prosimians and catarrhines and described anatomical and locomotor correlates within the platyrrhines. This is a short and in no way exhaustive history of primate locomotor studies that have been used to help provide insight into this work; many of the hypotheses in this work stem from the previously cited studies.

Positional and Locomotor Behavior Previous work This study would not be possible without the work of many researchers who have dedicated time and energy to the field studies of wild primates. Specifically, this study relies on the documented and published work of researchers investigating the positional and locomotor behavior of the platyrrhines. While many species have been studied in the wild, many have little to no quantitative studies concerning positional behavior.

Using the work of others becomes problematic as investigations differ in terms of methodologies and can often be rather complicated. In the best case scenario, every researcher would use the same metrics and the same terminology, thus eliminating any confusion. However, this is not the case. The use of morphological data to infer locomotor behavior or behavioral data to describe morphological data is not new. The issues that arise when one tries to relate behavior and morphology may stem from inconsistencies in the methods of data collection. This issue has been addressed before (see Ripley 1967 or Dagosto and Gebo 1998). It is not the purpose of this dissertation to rehash the problems that can arise with this type of research, suffice it to say that there is a relative lack of behavior (positional) information for several species. In these cases, 27 where there are no quantifiable numbers indicating how often a species may leap or climb, a more generalized behavior description is assumed based on the available literature.

In platyrrhines, information on positional and locomotor behavior may come from researchers studying ecology, diet, and social behavior. Information useful to this study may come from studies and reports that were focused primarily on other issues and not directly interested in locomotor behavior.

When trying to condense locomotor and positional data, it becomes important to recognize individual researcher’s differences in terminology, definitions, scope of the study, and in the amount of detail. Some researchers use similar terminologies to describe very similar or different behaviors, while others may provide multiple definitions for the same behaviors. All of these differences need to be examined before an estimated quantitative percentage of a certain behavior can be ascertained. Table 1.1 contains a list of primate locomotor and postural studies.

This list mostly contains quantifiable (percentages of locomotor behavior) data studies, however, for several species where no quantifiable data is available, studies of a more general nature are also included. Table 1.1 also gives a general locomotor description for each species. 28 7 Locomotor Behavioral Studies of New World Monkeys P. monachus *Leaper - VCL Youlatos 1999a Happel 1982 P. pithecia *Leaper - VCL Fleagle and Mittermeier 1980 Walker 1993, 1994, 1996 and 2005 Fleagle and Meldrum 1988 C. satanas *Primarily Quadrupedal Walker 1996, 1994, 2005 Fleagle and Meldrum 1988 Veiga 2006 - Dissertation

C. rubicundus(calvus) *Quadrupedal Ayres 1986 - Dissertation Walker 1996 Walker and Ayres 1996 C. olivaceus *Primarily Quadrupedal Wright 2007 Youlatos 1998 C. capucinus *Primarily Quadrupedal Gebo 1992 C. albifrons *Primarily Quadrupedal Youlatos 1999a C. apella *Primarily Quadrupedal Wright 2007 Youlatos 1998 C. torquatus Primarily Quadrupedal Lawlor et al. 2006 Kinzey 1977 C. moloch Primarily Quadrupedal Youlatos 1999a S. oerstedii Quadrupedal Boinski 1989 S. sciureus *Quadrupedal Fleagle and Mittermeier 1980 Youlatos 1999a Yoneda 1988 S. boliviensis Quadrupedal Fontaine 1990 C. goeldii *Leaper - VCL Pook and Pook 1981 Porter 2004 and 2007 Garber and Leigh 2001 S. tripartitus Quadrupedal – Limited Leaping Youlatos 1999a S. mystax *Quadrupedal – Limited Leaping 29

Garber 1988, 1991 Garber et al. 1993 Garber and Pruetz 1995 Norconk 1986 and 1990 Nyakatura and Heymann 2010 S. midas *Quadrupedal Youlatos 1995, 1999a, 2004 Fleagle and Mittermeier 1980 S. labiatus *Quadrupedal Garber and Leigh 2001 Porter 2004 S. geoffroyi *Leaper/Quadrupedal – No VCL Garber 1980 - Dissertation, 1984, 1991 Garber et al. 1993 Garber and Sussman 1984 S. fuscicollis *Leaper – VCL? Garber 1988, 1991 Garber and Leigh 2001 Norconk 1986 and 1990 Porter 2004, 2007 Yoneda 1984 Castro 1991 Nyakatura and Heymann 2010 C. jacchus jacchus Quadrupedal Schmitt 2003 Garber et al. 2012 C . pygmaea *Leaper - VCL Youlatos 1999b, 2005, 2009 Kinzey et al. 1975 L. rosalia Quadrupedal Stafford et al. 1994 A. caraya *Climber/Quadrupedal Bicca-Marques JC, Calegaro-Marques C 1995 Prates HM, Bicca-Marques JC 2008 A. fusca *Climber/Quadrupedal Azevedo RB, Bicca-Marques JC 2007 A. pigra Climber/Quadrupedal Cant 1986 A. palliata palliata Climber/Quadrupedal Mendel 1976 A.palliata *Climber/Quadrupedal aequatorialis Gebo 1992 A. seniculus seniculus *Climber/Quadrupedal Schon Ybarra and Schon 1987 A. geoffroyi *Suspensory Fontaine R, 1990 Cant JGH, 1986 Bergeson DJ, 1996, Dissertation 30

Mittermeier 1978 Mittermeier and Fleagle 1976 A. paniscus paniscus *Suspensory Youlatos D, 2002 Fleagle and Mittermeier 1980 L. lagothricha *Climber/Quadrupedal Defler TD, 1999 L. lugens *Climber/Quadrupedal Stevenson PR and Castellanos, 2000 L poeppiggii *Climber/Quadrupedal Cant JGH, Youlatos D, Rose MD, Rose MD, 2001

The above studies mostly include quanitfiable data on locomotor and positional behavior of the new world monkeys. Some of the studies also include general information on locomotor and postural behavior, especially for species where no quantifiable data is available. ‘*’ Indicates a quantifiable percentages of locomotor behavior exist for the species. Table 1.1 - Locomotor Studies of Platyrrhine Primates

Definitions of Locomotor Behavior Primates exhibit a wide variation of locomotor modes and platyrrhines are no exception. The neo-tropical monkeys are not only variable in size, but also in terms of their types of locomotion. An early attempt to characterize platyrrhine locomotion was undertaken by G.E.

Erikson (1963), in which he distinguishes platyrrhines as having more diverse locomotion than the catarrhines, excepting that the platyrrhines lack a terrestrially adapted species.

Erikson (1963) divided the platyrrhines into three locomotor types, based upon limb indices

(intermembral and brachial) and morphology. He identifies a ‘springer’ group typified by

Aotus, but also including the marmosets; a ‘climber’ group typified by Cebus, but also including the pithecids; and a ‘brachiator’ group, which included the atelids. Erikson’s (1963) use of the term ‘brachiator’ applied to the howler, wooly, wooly spider and spider monkeys. While this 31 may seem a natural deduction, some have deemed the term ‘brachiator’ incorrect, others prefer the term ‘suspensory’, while the term ‘brachiator’ is reserved for the true brachiators, the hylobatids. The debate about correct descriptions of brachiation vs. suspensory (Mittermeier and Fleagle 1976) will not be continued here, nonetheless, it appears Erikson is correct in his initial advocation for a ‘brachiator/suspensory’ group. For the purposes of this work, the terms

‘suspensory/suspension’ and/or ‘New-World brachiator/brachiation’ will be used to identify the locomotor and positional behavior of Ateles and Brachyteles. ‘Suspension’ is a descriptive term used to generically describe the positional behavioral of Ateles and Brachyteles. It is forelimb dominated, and thus not overly applicable to this work. However, it has been hypothesized that the link between quadrupedalism and brachiation in the Atelines was tail assisted hindlimb

‘suspension’ (Meldrum 1998 and Jones 2004, 2008). Furthermore, the term ‘brachiation’ refers correctly to the locomotor behavior of Ateles and Brachyteles. While I use the two terms interchangeably, it should be noted that I do so to refer to the group that includes Ateles and

Brachyteles which employ forelimb suspension and brachiation.

Furthermore, no discussion of platyrrhine locomotor behavior would be complete without a discussion of vertical-clinging and leaping. In 1967, Napier and Walker published a description of a ‘new’ locomotor mode. In their now classic paper, vertical clinging and leaping was ascribed to several prosimian species. Leaping from a vertical support (sometimes described as trunk to trunk leaping (Garber et al. 2012) is seen in several platyrrhines as well. Pithecia pithecia (Walker 2005) has been observed to leap from vertical supports, along with Cebuella

(Kinzey et al. 1975, Soini 1988 and Youlatos 1999, 2004) and Callimico (Pook and Pook 1981,

Porter 2004). While there are certainly many differences between the platyrrhines and the 32 prosimians in terms of locomotor behaviors, the above data suggests that vertical clinging and leaping (as a category of locomotor behavior) is not limited to the prosimians. For more insights in VCL in prosimians, see Stern and Oxnard (1973). Many have investigated the anatomical correlates of vertical clinging and leaping behavior (e.g., Napier and Walker, 1967;

Walker, 1974; Stern and Oxnard, 1973; Anemone, 1990; Oxnard et al., 1981) finding many shared characteristics but also noting differences. A further discussion of VCL in platyrrhines will be found in Chapter 4.

Primates exhibit varied locomotor behaviors, as evidenced by the above observational research.

Since Erikson’s original work described above, additional work and ideas have been accomplished. It is now more accurate to say in general terms that platyrrhines fall into one or more of the four basic locomotor behavioral groups. Plattyrhines can be described as being either a quadruped, a leaper, a climber or a New-World brachiating primate. The categories may overlap and multiple categories, (i.e., an atelid may be a majority suspensory animal that also climbs) often are better descriptors of these movement patterns. Using the known behavioral research, it is important to understand that no primate is exclusively limited to one of these movement categories, but rather moves in several different ways depending on the substrate or environmental context (For further discussion of habit-potentiality, see Prost 1965).

For the purpose of this project, the four basic locomotor categories are described as follows:

Quadrupedalism: a pronograde movement occurring above the substrate. Both forelimb and hindlimb contribute to movement; whilst the body is probably maintained compact and close to 33 the substrate with bent or flexed elbows and knees.

Leaping: a movement from one substrate to another that crosses a spatial gap. All limbs will be free from the initial substrate after take-off. I did not discriminate for or against substrate orientation. For example, primates may leap from trunk to trunk or terminal branch to terminal branch. Some field research examines leaping in this regard (i.e., discussions of vertical clinging and leaping, VCL). In general terms, the hindlimb provides the explosive take-off force instrumental in leaping across a gap. The forelimb is not examined in this study, even though it obviously would play a role in landing.

Climbing: an upward pulling movement along an inclined or a vertical support. It is assumed that all limbs are involved in climbing, though only the hindlimb is examined in this study.

New-World brachiation: a unique movement under a substrate (generally horizontal in nature).

Movement, may also be between substrates, as a crossing maneuver. All four limbs may be used, along with the prehensile tail. Based on body orientation, it is assumed that primary movement is fueled by the forelimb with semi-vertical back postures.

There are a variety of sub-categories for the four main movement categories outlined above. In the wild behavioral data (outlined in Table 1.1) many researchers, unfortunately, do not use the 34 same metrics. For the purposes of this project, data is lumped into the four main movement categories. This is not ideal, as better defined data would appear to be better, however, with the inconsistencies between different researchers it is the only realistic option.

Morphological Studies Primates exhibit a great variety of locomotor capabilities and attempting to decipher the morphological features of a platyrrhine hindlimb that distinguish different locomotor groups is the intent of this research. It was important to lay the groundwork for this research, by understanding what is known or hypothesized about the association between locomotion and hindlimb morphology in primates and other groups. This background information follows below.

The Hip An early study by William Straus Jr. (1929) examines differences in the primate pelvis. His study does not make many comments on the functional implications of these shape differences, however, it is an example of research of quantifiable but subtle differences in one anatomical area of closely related species. Fleagle and Anapol (1992) go a step further and make functional hypotheses about quantifiable shape differences. Fleagle and Anapol (1992) examined the ischium in multiple species of prosimians and platyrrhines to determine if the ischium varied extensively between vertical clingers and leapers and other primates. Their research alluded to the idea that vertical clingers and leapers tend to have a dorsally projected ischium, while species which tend to be more pronograde have a distally elongated ischium.

They hypothesize that this may be because a dorsally extended ischium may help to increase the 35 lever arm of the hip extensors while the hip is near full extension. They outlined several measurements of the ischium that they used to come to these conclusions. Some of those measurements were used as guides for my own measurements for this project.

Multiple studies have examined locomotor morphology within prosimian primates. Prosimians are unique in that they are evolutionarily more primitive compared to anthropoids (the monkeys, apes and humans), but they also exhibit quite varied modes of locomotion including true vertical clinging and leaping as defined by Napier and Walker (1967). McArdle (1981) undertook an examination of the morphology of the hip and the thigh in the lorisiformes. His investigation focused on the underlying myology and differences exhibited between the galagos and lorises. Robert Anemone (1990) examined prosimian femoral morphology and showed that while many species may be described as vertical clingers and leapers, not all of them share the same femoral morphology. This implies that there are morphological differences in the proximal femur of prosimians that can discriminate between groups. Alan Walker (1974) identified several features in the hindlimb that he considered morphological correlates for locomotion. In the pelvis he cites an expanded ilium amongst other features that he believes to be more associated with vertical clingers and leapers than with quadrupeds.

Grand and Lorenz’s (1968) study of two species of tarsier provides additional insight to what is functionally occurring at the tarsier hip during leaping. Tarsiers are known for their acrobatic and explosive leaping, and this study helped to describe the muscle action taking place during locomotion. When combined with a morphological description of the shape of the femoral head

(Dagosto and Schmid 1996), it is clear that tarsiers (and galagos) are not only unique for their leaping ability but also their underlying anatomy. 36

The Knee The primate knee joint has been studied for its implications for human bipedalism, but it is also very important in terms of locomotion for all primates. Tardieu (1981) describes the variability present in mammalian knee joints. Unfortunately, she does not delve into platyrrhine knee shape, but she does outline several measurements and characteristics of the catarrhine knee.

Similarly, Walker (1974) hypothesized that because of the high degree of flexion in VCL prosimians during resting posture they should exhibit posteriorly oriented femoral condyles, in essence, alluding to distal femoral morphology that is variable based upon locomotor behavior.

’Tall’ knees have been linked to leaping extant prosimians and several fossil primates, while

‘low’ knees have been identified in the non-leaping lorisiformes and apes (Gebo 2014).

Studies Incorporating Morphology and Behavior A well-known study of primates that combined postural and locomotor behavior with locomotor morphology was published by John Fleagle in 1976. He studied two species of Malaysian leaf- monkeys, Presbytis obscura and Presbytis melalophos. Interestingly these two species (since reclassified into different genera) have different locomotor tendencies. P. obscura moves mostly by quadrupedal walking and running, while P. melalophos tends to move on smaller supports and incorporates more leaping. Fortunately, Fleagle (1976) extended his research beyond mere locomotor behavior and examined the skeletal morphology underlying that behavior. He identifies many features of the hindlimb that are associated with more leaping tendencies or to more quadrupedal tendencies. These include intermembral indices, long ischium, extent of the articular surface of the head of the femur, thickness of the neck of the femur, proximal extension of the patellar groove, prominence of the lateral border of the patellar groove and symmetry of the femoral condyles, among many others. Fleagle’s work is 37 an important combination of behavioral observations and morphological investigation.

Ciochon and Corruccini (1975) examined the platyrrhine femur in an attempt to clarify platyrrhine taxonomy. They identified many measurements on the femur, some of which were incorporated in this study. Similarly, Susan Ford’s (1986) morphological investigations have added to the understanding of platyrrhine anatomy. Her examination of platyrrhine systematics was incredibly valuable at a time before molecular analyses were commonplace. Also, her work (Ford 1990; Ford and Morgan 1986) have helped to clarify the understanding of fossil platyrrhines, while also incorporating discussions of platyrrhine morphology.

Other researchers have provided insight to the morphology of individual species or families within the platyrrhines. Fleagle and Meldrum (1988) published a study of locomotor behavior and skeletal morphology of two pithecine species, Pithecia pithecia and Chiropotes satanas.

Similar to the Fleagle (1976) study, Pithecia tends to incorporate more leaping and acrobatic elements into its locomotor repertoire while Chiropotes is much more quadrupedal in general.

The authors identified many features of the hindlimb that they correlated to either saltatory or quadrupedal tendencies. This work represents an important comparison within the platyrrhines of different locomotor modes and morphology, within one study. Lesa Davis examined the callitrichid primates in her 2002 Ph.D. dissertation where she highlights behavioral, ecological, life-history and morphological variations within the callitrichids. Lesa Davis (1996) also examined the ankle morphology of Callimico goeldii, an enigmatic callitrichid. Kristin Wright

(2007) published a study of behavior and morphology, focusing on two species of capuchin monkey. Her study indicated that locomotor behavior was somewhat different between the two species (Cebus apella and Cebus olivaceus), and that the underlying morphology showed some 38 differences as well.

Other groups of mammals have been studied to elucidate information about the morphology of the hindlimb, especially that of the hip and the knee. Taylor (1976) examined the functional morphology of the hindlimb of the Viverridae, carnivores including the mongoose.

Interestingly, he was able to use the hindlimb morphology to distinguish between multiple types of locomotor tendencies. This is important as it illustrates an ability to take a broad taxonomic group of animals and use hindlimb morphology to come to a conclusion about locomotor potentiality. Jenkins and Camazine (1977) researched the hip structure and locomotion in carnivores specifically examining differences in hip abduction/ adduction and femoral excursion in ambulatory versus cursorial species. Their study is an illustration for subsequent researchers in the actions occurring at the hip joint in animals who employ mostly para-sagittal limb movements, versus animals that move in less restrictive planes.

I have assembled a table (Table 1.2) of hindlimb features that have been linked with a locomotor category on the basis of the research that is discussed above in this chapter. The table is not an exhaustive list, but rather a visual representation of what is known and/or hypothesized.

Leapers Quadrupeds Climbers Suspensory

Dorsal Projection of Ischium Longest Shorter ??? Shortest

Distal Projection of Ischium Longest Shorter ??? ???

Prominent Intertrochanteric Line Present ??? Present ???

??? (Probably Iliac Expansion (Width) Highest Low High Lowest) 39

Femoral Neck Length Shortest Longest Long ???

Less Thick (Relates Femoral Neck Robusticity (Thickness) Thickest Less Thick Less Thick to Head Size)

Lowest Higher Femoral Neck Angle (Perpendicular Higher Angle Highest Angle Angle to Shaft)

Encapsulat Extensive es Encapsulates (Postero- Extension of Femoral Articular Surface Less Extensive Spherical Spherical Femoral Superior Part of Femoral Head Femoral Neck Head

Broad, Flat, Greater Trochanter Size, Shape and Smaller, Less Least Developed, Overhangs ??? Position Overhang No Overhang Shaft Anteriorly

??? (Probably Pubic Ramus ??? ??? Wide Similar to Climbers)

Femoral Head Size ??? ??? Large Largest

Medial Condyle Both Condyles Femoral Condyles Symmetrical More Asymmetrical Antero- Antero-Posteriorly Posteriorly Compressed Longer

???(Probabl Narrow and Wider and More y Similar to Patellar Groove Width and Depth Narrow and Shallow Deep Shallow Suspensory )

Large Lateral More Symmetrical Patellar Groove Lip Low Low Lip Lips

Femoral Condyle Orientation Distal Posterior and Distal ??? ???

Insertion for m. gracilis and m. Proximal Distal ??? ??? semitendinosus Table 1.2 - Hindlimb Features and Locomotor Categories

Hypotheses Based on the previously mentioned behavioral and locomotor studies, I have organized a series of hypotheses to test and these are outlined below:

Leaping: H1 – Platyrrhines that have been shown to include substantial amounts of leaping behavior in their locomotor repertoire, will have shape differences in the pelvis, hip and knee compared to quadrupedal, climbing or suspensory platyrrhines. (e.g., Pithecia vs. other pithecids; Saguinus 40 fuscicollis vs. Saguinus midas; Callimico vs. Callithrix; etc.)

Hypothesis1a – The pelvis of platyrrhines that engage in significant

amounts of leaping from vertical supports will have a longer dorsal

projection of the ischium (Fleagle and Anapol 1992), and platyrrhines

that engage in leaping from horizontal supports will have a dorsally

longer ischium along with a distally longer ischium than quadrupedal,

climbing, or suspensory platyrrhines (Fleagle and Anapol 1992).

The monkeys in the Leaping category leap primarily from a

vertical position, and are therefore expected to exhibit a dorsally

expanded ischium. However, they also engage in a fair degree

of leaping from a horizontal position compared to the

quadrupedal, climbing, or suspensory groups, and therefore may

also exhibit a distally elongated ischium.

Hypothesis 1b - Platyrrhines that engage in a high percentage of

leaping behavior will have a hip that is characterized by a

prominent intertrochanteric line, an expanded ilium compared to

quadrupedal platyrrhines, a short, thick femoral neck set

perpendicular to the femoral shaft, a femoral articular surface that 41

extends onto the superoposterior side of the femoral neck, and a

broad, flat greater trochanter that overhangs the anterior surface

of the femur.

Hypothesis 1c – Platyrrhines that engage in a high percentage of

leaping behavior will have a knee that is characterized by

symmetrical femoral condyles, a narrower patellar groove with a

more prominent lateral lip, and distally oriented femoral condyles

compared to quadrupedal platyrrhines.

Quadrupeds: H2 – Generalized quadrupedal platyrrhines should have a post-cranial skeleton that does not exhibit the specialized characters and features identified for leaping, climbing or suspensory primates.

Hypothesis 2a - Generalized quadrupedal platyrrhines will have a

pelvis characterized by a shorter ischium than found in leaping

platyrrhines.

Hypothesis 2b – Generalized quadrupedal platyrrhines will have a

hip characterized by a longer femoral neck set at a higher angle

(than leapers), a femoral articular surface that does not extend 42

onto the neck of the femur and a moderately sized greater

trochanter that does not overhang the anterior surface of the

femur.

Hypothesis 2c – Generalized quadrupedal platyrrhines will have a

knee characterized by a wider patellar groove (than in leapers),

asymmetrical femoral condyles and femoral condyles oriented

distally and posteriorly.

Climbing: H3 – The pelvis, hip and knee of platyrrhines, which engage in a high percentage of climbing behavior, will be subtly different in morphology than more generalized quadrupeds.

Hypothesis 3a – The pelvis of climbing platyrrhines will be

characterized by a wider pubic ramus and a more expanded ilium

than for more quadrupedally oriented platyrrhines. (Climbing is

not unique amongst any group of primate, for the purposes of this

study, a high degree of climbing is set at 20% or more of a

species locomotor repertoire.)

Hypothesis 3b – The hip of climbing platyrrhines will be

characterized by a femoral head that is higher or equal to the 43

height of the greater trochanter, a femoral articular surface that

extends anteriorly and posteriorly to encapsulate the femoral

head, a prominent intertrochanteric line and crest, a deep

trochanteric fossa and a medially placed lesser trochanter.

Hypothesis 3c – The knee of climbing platyrrhines will be

characterized by a longer medial femoral condyle compared to

quadrupedal platyrrhines.

New-World Brachiation: H4 – The pelvis, hip and knee of platyrrhines, which engage in brachiating behavior, will be different in morphology than generalized quadrupeds.

Hypothesis 4a – The pelvis of brachiating platyrrhines will be

characterized by a shorter ischium and a smaller (in diameter)

acetabulum compared to quadrupedal platyrrhines.

Hypothesis 4b – The hip of brachiating platyrrhines will be

characterized by a larger, spherical femoral head compared to

quadrupedal platyrrhines, an articular surface that covers the

head, extending to the femoral neck, a femoral head height equal

to or exceeding the height of the greater trochanter and a large

lesser trochanter that protrudes medially. 44

Hypothesis 4c – Brachiating platyrrhines will show adaptations at

the hip to increase joint excursion. These adaptations include

increasing the ratio of femoral head to femoral neck size and/ or

increasing the ratio of width of the acetabulum to femoral head

size.

Hypothesis 4d – The knee of brachiating platyrrhines will be

characterized by femoral condyles that are antero-posteriorly

compressed and narrowly separated and a wider patellar groove

with lower/less robust medial and lateral lips compared to

quadrupedal platyrrhines.

Platyrrhine Phylogeny Understanding a group’s phylogeny is important when trying to ascertain morphological or behavioral variables. In the evolutionary construct, an animal’s morphology is likely a combination of adaptation and phylogenetic influences. No two species are likely to respond to external selective forces in exactly the same way, thus knowing a phylogeny can help to decipher a species’ phylogenetic traits versus morphological or behavioral traits. In essence, do the two species of Pithecia represented in this study have the same morphological traits because 45 of shared inheritance, shared ecological link to behavior, or shared behavior?

Because phylogeny is hierarchical, species are not independent data points and there is a chance of statistical error when phylogeny is not considered as part of a regression or statistical analysis (Felsenstein 1985).

The phylogeny of a group of primates is, in essence, a question of the interrelatedness of the group. For platyrrhines, as for other groups of primates there is ongoing discussion and debate as to what constitutes the most correct phylogeny. While morphological investigations produced well studied phylogenies of the living platyrrhines (Rosenberger 1981; Ford 1986), the more recent advent and use of molecular studies of platyrrhine phylogeny has yielded new insights to this debate. Surely, the debate will continue as more fossils are discovered.. I have included a brief discussion of the history of platyrrhine phylogenies.

Philip Hershkovitz (1977), in his immense monograph on the extant platyrrhines, posits the theory that the callitrichids are primitive with relation to the other platyrrhines. He identified three families within the platyrrhines, the Callitrichidae, Callimiconidae and the Cebidae.

While much of this work was revised by later researchers (e.g., Groves, 2001) where he recognizes four families within Platryrrhini, Hershkovitz’ work represents an early attempt to sort out the relationships within the many species of platyrrhines.

Rosenberger (2002) writes that knowing the phylogeny of the platyrrhines is possible for researchers, for several reasons. One reason is that the extant platyrrhines, for the most part, are able to be grouped somewhat reliably, by behavior, ecology and morphology. According to

Rosenberger (2002), the pithecines are ‘dentally bizarre’ seed eaters. The atelines are climbers 46 who have modified their postcranium. The callitrichines are small bodied clingers, with claws for locomotion. The cebines have large heads, are ‘predaceous’ and frugivorous omnivores.

This may be a minimally accurate stereotype of what we know about extant platyrrhines, it does not aid in the interpretation of fossils where behavior is unknown and can only be inferred.

While a description of behavior and morphology can give an idea of relatedness, it is not definitive in any way. The morphological phylogenies of Ford (1986) and Rosenberger (1981) do show some similarities. Both researchers have an ateline clade and a callitrichine clade.

However, while Ford (1986) makes an independent callitrichine clade, Rosenberger (1981) includes Saimiri and Cebus, to form a cebine clade. Ford (1986) places Saimiri either in a clade with Aotus and Callicebus, or possibly alongside Cebus. Amongst the morphologists, there is also some disagreement on where to place Aotus and Callicebus. Rosenberger (1981) puts them in the pithecine clade, sister group to the ateline clade, while Ford (1986) puts them with

Saimiri/Cebus. Ford (1986) advocates a pithecine clade, including Lagothrix, Cacajao and

Pithecia, that is the sister group to the ateline clade.

Fortunately, in recent years molecular studies of platyrrhine phylogeny have also been undertaken. These studies help to enhance the previous morphological work that was done.

Wildman et al. (2009) produced a molecular phylogeny. They used eleven ‘unlinked, non- coding, non-genic, non-repetitive’ nuclear DNA markers that were sequenced in a representative member of each platyrrhine genus. The authors analyzed these markers independently and alongside previously published markers of closely related genes. The authors’ phylogeny suggests that Pithecidae is the sister group to the two other platyrrhine higher groups (Cebidae and Atelidae). Aotus is sister to a clade formed by Saimiri and Cebus. 47

The Cebidae, encompass not only the Aotus, Saimiri and Cebus group, but also the callitrichines. Interestingly, Callicebus is placed within the pithecid group, unlike the morphological phylogeny of Ford (1986), but similar to that of Rosenberger (1981).

More recently, Perelman et al. (2011) published their study, which was relatively exhaustive where they analyzed 54 nuclear gene regions from greater than 90% of all living primates. The resultant phylogeny included a pithecine clade (inclusive of Callicebus) as sister to the two other platyrrhine groups (the Atelidae and the Cebidae). Within the cebine clade, one will find the aotids sister to the callitrichids. This phylogenetic tree was used when phylogenetic regressions were necessary. In order to supplement this tree with divergence dates from taxa not included by Perelman et al., data was extracted from Menezes et al. (2010) for Aotus ;

Buckner et al. (2015) for Saguinus leucopus and S. nigricollis; Botero et al. (2015) for

Lagothrix; and Chatterjee et al. (2009) for Alouatta guariba (fusca). The modified phylogenetic tree can be found in Appendix 2.

Molecular phylogenies have added insight and clarity to the understanding of platyrrhine phylogeny, however, there are continued areas of subtle disagreement. Wildman et al. (2009) indicate that one point of difficulty is the exact placement of Aotus within the cebid group.

Nonetheless, the suggestion that Aotus can be rather confidently placed within the cebid group is an advancement beyond the earlier morphological phylogenies. The conclusion that

Callicebus is sister to the rest of the pithecids is also an important advancement. Surely, as the molecular phylogenetic information augments what is known from morphology, a better understanding of the phylogeny of fossil platyrrhines will become better known.

How to Interpret the ‘Function’ in Functional Anatomy? It would be very simplistic if morphology and behavior always coexisted as an independent relationship. If a morphological feature always corresponded to a certain behavioral trait, then there would be no need for this study or many others that have come before. Unfortunatey, there is no ‘one-to-one’ relationship between individual features and locomotor traits. There is no perfect ‘leaping’ anatomy or ‘climbing’ anatomy for primates. Few if any features correspond to a singular behavior, making the possibility of erroneous conclusions significant.

This is exacerbated when one starts to consider the number of motions that are possible at the various joints studied in a work on locomotion.

Additionally, difficulties are encountered with the number and quality of behavioral data, along with the locomotor categories that are employed. Considering that all behavior research is not done by the same researcher with the same metric, difficulties can arise when condensing or analyzing the data. Combing data from across multiple locomotor ‘categories’ also is not without problems. While the locomotor behavior research is invaluable, it is important to keep in mind that many species are left unstudied and others may be hampered by unknowns.

Chapter 2

Materials and Methods

Introduction This chapter examines the specimens and species used in this study and the methods of analysis employed. The first portion of this chapter will look at the factors that affect the number of specimens and the species used in this study. The second portion examines the behavioral and locomotor information contained in the literature that affects the features examined in this study.

Lastly, this chapter will discuss more specific aspects of the data collection and analysis methodologies.

Extant New World Primates by Genus

Family Callitrichidae Cebuella Mico Callithrix Saguinus Leontopithecus Callimico

Family Cebidae Saimiri Cebus

Family Aotidae Aotus

Family Pithecidae Callicebus Pithecia Chiropotes Cacajao

Family Atelidae Alouatta Ateles Lagothrix Oreonax Brachyteles

* From Rylands et al. (2000). All above genera are represented in this study, with the exception of Oreonax and Brachyteles (Due to insignificant sample size). Table 2.1 - Extant Platyrrhine Genera Taxa Every effort was made to include as many platyrrhine taxa as possible. Table 2.1 lists the extant platyrrhine genera and four major primate collections were examined. These include the

Smithsonian (USNM), the Field Museum of Natural History (FMNH), the American Museum of

Natural History (AMNH) and the Neil Tappen collection, housed at the University of Minnesota,

Department of Anthropology.

Issues affecting the inclusion of taxa (species) There is one main issue affecting the inclusion of taxa within this study. Unfortunately, several platyrrhine taxa are unrepresented or underrepresented in museum collections. Some species are represented only by skins and/or skulls, and these cannot be included in this study. Museums tend to have larger numbers of skins and skulls than they do complete skeletons. This study focuses on the post-cranial features, specifically the hindlimb. This limited the number of taxa within this study, by making it impossible to include species (like Brachyteles) where a statistically significant sample of specimens cannot be obtained. 51

A minor issue affecting the inclusion of taxa within this study is the changing taxonomic nomenclature. With the expanding information from molecular phylogenetic studies re-defining

(and renaming) and dividing species, it is imperative that the museums, likewise, keep their collections up to date. Every effort was made to correctly attribute every specimen used.

Obviously, this has precluded the use of several species that have more recently been named or described. These species are simply not yet represented in the museum collections in numbers that can be used, an example of this is Callibella, the dwarf marmoset.

Issues affecting the inclusion of individual specimens To be useful for this study, there are several factors that determine whether a specimen was usable. Generally speaking, specimens were not photographed if they did not meet the quality standards described here.

1. The specimen must have post-cranial (hindlimb) elements. Often times, only one side of

the specimen was disarticulated. If no hindlimb elements were available, the specimen

was not used. However, if only a partial hindlimb was available, the features that could

be photographed were measured. Several species are represented by specimens where

only a partial percentage of features were able to be measured, simply because the

specimens were not complete.

2. The specimens included in this study were fully adult. Each specimen was examined for

epiphyseal fusion of the long limb bones. This indicates that they were fully adult. If a

specimen was marginal (probably close to adult, but still not completely fused), it was not

included in this study. 52

3. Each specimen was examined for evidence of pathologies. Pathologically damaged

specimens were not included in this study. Evidence of healed fractures and so forth,

precluded a specimen from being included. However, there were several species that are

underrepresented in museum collections, where data was obtained from specimens where

the long bones were broken. It can be assumed that these bones (wild-caught specimens)

were broken post-mortem or during the collection process. Several specimens within the

Pithecidae are examples of this. Unfortunately, for these specimens, it was not possible

to obtain all measurements (i.e., impossible to obtain total femur length on a bone with a

mid-shaft breakage).

4. Preference was always given to the disarticulated specimens. If a specimen was fully

articulated it was excluded from this study. There was not time during the museum visits

to request that articulated specimens be properly disarticulated.

5. When possible, wild-caught specimens were always preferred. For all species, wild-

caught specimens were photographed first. It is assumed that wild-caught specimens best

represent the anatomical and locomotor features of the species. However, it should be

noted that in this study, several species are represented in part (or in total) by captive

specimens. Several species (many of the callitrichids) are represented by captive

specimens in order to obtain a statistically significant sample. In these cases, the four

previous qualifications still apply.

While there are dozens, if not hundreds, of positional and locomotor behavioral studies of the platyrrhines, several species are still not adequately described in terms of locomotor behavior and positional repertoire. This did not preclude these species/specimens from being collected for this study. 53

Species of New World Primates Obtained for this Study

Family Callitrichidae Cebuella Cebuella pygmaea Mico Mico humeralifer Mico argentata Mico argentata melanura Callithrix Callithrix jacchus jacchus Callithrix jacchus penicilatta Callithrix jacchus geoffroyi Saguinus Saguinus oedipus S.o. geoffroyi Saguinus midas Saguinus midas midas Saguinus midas niger Saguinus mystax Saguinus tripartitus Saguinus leucopus Saguinus labiatus Saguinus Imperator Saguinus fuscicollis S.f. fuscus S.f. primitivus S.f. leucoginys S.f. illigeri S.f. lugonatus Saguinus nigricollis Leontopithecus Leontopithecus chrysomelas Leontopithecus rosalia rosalia Callimico Callimico goeldii

Family Cebidae Saimiri

Saimiri sciureus Saimiri sciureus boliviensis Saimiri boliviensis boliviensis Saimiri ustus Cebus Cebus albifrons Cebus albifrons hypoleucus Cebus albifrons cesarae Cebus apella Cebus (apella) libidinosus Cebus capucinus Cebus olivaceus Cebus (nigrivittatus castaneus) Cebus olivaceus apiculatus Cebus olivaceus castaneus

Family Aotidae Aotus Aotus vociferans Aotus (azarae) infulatus Aotus azarae azarae Aotus azarae boliviensis Aotus trivirgatus Aotus (trivirgatus) griseimembra Aotus (trivirgatus) nigriceps Aotus lemurinus

Family Pithecidae Callicebus Callicebus moloch moloch Callicebus cupreus Callicebus cupreus discolor Callicebus torquatus Callicebus moloch donacephilus Callicebus donacephilus donacephilus Callicebus ornatus Callicebus moloch ornatus Pithecia Pithecia irrorata Pithecia pithecia Pithecia monachus 55

Chiropotes Chiropotes satanas Cacajao Cacajao (calvus) rubicundus Cacajao melanocephalus

Family Atelidae Alouatta Alouatta caraya Alouatta fusca Alouatta seniculus Alouatta seniculus seniculus Alouatta seniculus straminea Alouatta seniculus insulans Alouatta palliata palliata Alouatta palliata (aequatorealis) Alouatta belzebul Ateles Ateles fusciceps fusciceps Ateles fusciceps robustus Ateles geoffroyi Ateles geoffroyi frontatus Ateles geoffroyi vellerosus Ateles paniscus paniscus Lagothrix Lagothrix lagothricha cana Lagothrix lagothricha lagothricha Lagothrix lagothricha lugens Lagothrix lagothricha poeppigii Brachyteles Brachyteles arachnoides

The above species are listed by the taxonomy given on the specimen tags when the specimens were collected. This list includes some species that are ultimately not included in this study because of insignificant sample sizes. During the analysis, some of these species were regrouped according to modern taxonomy. This list includes specimens that were both wild-caught and captive.

Table 2.2 - Platyrrhine Species Obtained for this Study 56

Data Collection and Analysis Data Collection

This study required as large a platyrrhine wide sample as possible, within the constraints of time and budget. Table 2.2 shows the species that were obtained for this study. While platyrrhine skins and skulls are relatively available for research, at the major museum collections, platyrrhine post-cranial elements (especially complete specimens) are less available. The three large American museum collections were used, along with a substantial collection housed at the

University of Minnesota, Department of Anthropology. This grouping of primate specimens was collected by Dr. Neil Tappen, and yielded several dozens of wild caught platyrrhines, most with known body weights at time of death. The total data set was collected over the span of three years and yielded statistically significant numbers of specimens from all platyrrhine genera, exclusive of Brachyteles and Oreonax.

Prior to the first museum visit, a metric was developed and streamlined which allowed the specimens to be photographed and features measured from digital photographs. The use of digital photography was preferred over the more traditional caliper measurements since digital photographs are an archival resource that can be re-measured at any time.

Using space in the Evolutionary Morphology laboratory of Dr. Marian Dagosto at Northwestern

University and a few preliminary trips to the Field Museum of Natural History in Chicago, a metric was developed that worked quite well in consistently photographing series of specimens.

A Nikon D3000 Digital SLR camera was used with a telephoto (300 mm lens). The camera was 57 placed at a true perpendicular angle to the specimen. The camera and the specimen were aligned using laser levels to ensure that the perpendicular angle was correct, thus minimizing distortion.

The camera was placed at the exact same height as the specimen to eliminate distortion. Using a common tape-measure, measuring table height and camera height allowed this to be done quickly and easily. Given that table height and workspace differed among the different collections, a set-up method that was easy to maintain was invaluable.

The lens of the camera was used at full zoom, approximately 300 mm (slightly varying depending on fine focus). This was done to ensure that the specimen filled the photographic frame, again to minimize distortion. Since size differences exist between platyrrhines, this meant that the camera was set closer to the worksurface/table for small callitrichids and further away for the larger specimens, including the atelids. The approximate distance of the camera to the specimen for the callitrichids was 4 feet, 7 feet for most of the cebids and pithecids, and 10 feet for the atelids. The workspace available at the different collections, varied slightly, but overall was very consistent in maintaining a true perpendicular angle of the camera to the specimen.

As the camera was set on a traditional tripod, it was relatively easy to set up. Each individual specimen however, required significant time and effort to position prior to each photo. A device of my own fabrication was employed that allowed each individual specimen to be set perpendicular to the camera. The below photograph, Figure 2.1 (a Cebus apella femur), illustrates the device. The device was an oak board, planed to be completely true and straight was attached to two pillars with a sliding clamp in the middle. Within the clamp, sat a plastic insert that was perfectly level to the table and at the same height as the camera lens (thus by 58 eliminating the camera either looking up or down at the specimen). The plastic insert (three different sizes for the variable sizes of the platyrrhines), allowed the specimen to be placed and maintained in position for the photograph. A piece of black artist’s matte board was used to distinguish the specimen and photographic scale from the surrounding environment. If necessary, a small piece of non-oily clay was used to help prop the specimen in the correct position. The device was easily aligned with the leading edge of the table or worksurface, thus making it easy to arrange the camera at a true perpendicular angle.

Figure 2.1 - Photographic Set-up The photographs were taken with a two second delay (from the time the button was pushed), with the purpose being to allow any vibration on the camera to end before the photo was taken.

Fine focus was adjusted anytime a specimen was moved or adjusted. A photo scale was used in 59 each photograph. This photo scale was placed at the same position as the specimen to minimize any distortion. Each photo was viewed on the camera after it was taken, to ensure focus. If the photo was not usable, another photo was taken.

For each specimen, seven photographs were taken: two of the pelvis, four of the femur, and one of the tibia (when it was disarticulated from the fibula). For the pelvis, one photograph was taken in a plane that allowed measurement of the ischial features, while the second photograph was taken in a slightly altered plane to allow better measurement of the pubic and iliac features.

The femur was photographed in an anterior, posterior, medial and lateral view. The tibia was photographed (generally in a lateral view) to measure total tibial length. To ensure that each specimen was properly handled and not confused with another, only one box was open at a time.

All the boxes from a shelf were photographed and returned to the shelf before the next shelf was used. Generally speaking, the post-cranial elements were photographed after the specimen had been examined fully (including skin and skull) to ensure that the specimen matched to its description on the box. The information from the specimen box was written down and corresponded to the specimen numbers (available on the museum databases and printed on each bony element). The camera also assigns a number to each photo taken, and these numbers were written down and used to further associate a photo to a particular specimen.

When working in the museum collections, wild caught platyrrhine specimens were photographed first and captive specimens second. In order to minimize the number of times that the camera set up had to be altered, all specimens within a size range were photographed, before the camera was adjusted. For example, all the cebids and pithecids were measured; then the camera setup was 60 adjusted and the larger atelids were measured, followed by another adjustment of the camera and all the callitrichids were measured. If a specimen was questionable (i.e. the skin did not correctly correspond to the species listed on the box), any issues were rectified before the specimen was photographed.

Two cranial measurements were included in the data set, as potential body size surrogates.

These could not be photographed in the same way as the post-cranial elements, so digital

Mitutoyo calipers were used for bi-zygomatic width and mandible length. In some collections, skulls and skins are housed separately from post-cranial elements, thus the two caliper measurements were taken at the end of the visit to each museum.

Specimen Measurements

After the conclusion of each museum visit, all the digital photographs were downloaded onto a computer and each individual specimen was assigned a folder. Each folder was labeled and double checked to ensure that the photographs associated correctly to each specimen (specimen number). All specimens were measured and entered into a spread sheet. The specimens were measured using ImageJ software. This software allows an individual photo to be loaded, the photographic scale to be set, and the various measurements taken. The measurements were generally recorded to the nearest 1/1000 of a centimeter (three decimal places).

Table 5 contains an illustration of the number of specimens (wild caught vs. captive) included in this study. These are listed according to the taxonomy given on the specimen tags, in some cases they have been regrouped according to more modern naming schemes. This table includes species that may have an insignificant statistical sample. During the analysis and measurement phase of data collection, all specimens that were photographed were measured, even if there was not a significant sample size.

Measurement Error Every effort was taken to ensure that the setup, photography and measuring was as consistent and in-variable as possible. In order to show that the concern for variance in measurements was taken into account a repeatability study for the measurements used in this study was undertaken.

Following Yezerinak et al. (1992), measurement error was determined to be between ~4% to

~10%.

Measurement Error % Measurement Feature Error

Femoral Neck Length 4.036845 Femoral Neck Thickness 4.02822 Femoral Head Height 5.03642 Femoral Head Width 4.18044 Anterior Articular Surface 4.067114 Posterior Articular Surface 4.228137 Greater Trochanter Width 6.99177 Patellar Groove Width 4.113934 Lateral Condyle Width 4.045946 Medial Condyle Width 5.089699 Lateral Condyle Length 4.00326 Medial Condyle Length 8.315995 Intercondylar Width 10.18024 Acetabular Width 4.059204

Acetabular Height 5.031165 Ilium Width 6.57798 Distal Projection of the Ischium 4.55007 Dorsal Projection of the Ischium 4.134422 Ischium Length 6.067935 Pubic Width 8.023008 Femoral Neck Angle 5.468073

Table 2.3 - Measurement Error Percentage by Feature

Morphology Specimen collection As discussed above, the specimens were all examined before being photographed and included in this study. They were removed from use if they did not meet the qualifying factors outlined previously. Obvious pathologies or erroneous attributions excluded specimens from being used in this study. Each element had to match the number on the specimen box in order for it to be included. Many times specimens had been misplaced or incorrectly returned to the shelves.

These issues were always resolved before a specimen was included in the study. For the smaller platyrrhines, it was not uncommon for a specimen to be partially articulated or missing elements.

For this study, incomplete specimens were included, as long as they met the other criteria.

Obviously, the term ‘adult’ can be a bit confusing when referencing skeletal material. For the purposes of this study, a specimen was examined to ensure complete epiphyseal fusion. This minimizes the issues of including multiple ontogenetic age groups within one study. While one could look at other features (such as dental eruption) to make a qualified guess as to approximate age, for this study not every specimen was represented by cranial material. Thus the decision was made to use full epiphyseal fusion as a marker for ‘adulthood’. 63

For the purposes of this study, wild-caught refers to specimens where there is locality data given on the specimen box or tag. Each specimen was examined for locality data prior to photographing. Skins and skulls were examined to see if locality data matched what was given on the specimen boxes. A specimen is considered to be captive if it is listed as a zoo, lab colony or research specimen. Specimens were also considered to be captive if it had no locality data or if it was collected in the wild and died in captivity. An attempt was made to include both male and female specimens. Often times, specimens are not tagged with a gender identification. In these instances if the determination can be made based on the cranial or post-cranial elements that identification was used. When no gender identification can be ascertained, the specimen is listed as ‘unknown’ gender. For most species, there is a relatively balanced number of males and females. For the species where minimal numbers of specimens are available, there is little that can be done to analyze males and female separately.

On the concerns of sexual dimorphism within the platyrrhines, it should be noted that platyrrhines are not nearly as strongly positively dimorphic as many of their catarrhine relatives

(Ford 1994). The majority of platyrrhines are monomorphic or only slightly dimorphic. Ford

(1994) concludes that 42% of the available taxa are monomorphic, while the majority of the remaining taxa are only slightly dimorphic. It should also be pointed out, that of the overall taxa, a limited number of species, Ateles paniscus and Callicebus cupreus, are unusual in that females are larger than males. Also, species with limited wild-caught body weight data may skew the dimorphism data in one direction or another.

Every effort has been made to correctly determine the taxonomy of each specimen used.

Unfortunately, not every specimen in the museum collections is revised for modern taxonomy 64 with every taxonomic revision. When necessary, skins were examined to ensure that the specimens matched the ever changing taxonomic lingo. In the rare instance, that an accurate attribution could not be determined, that specimen was eliminated from this study. In a few species, subspecies were grouped with the ‘parent’ species. This was done when the subspecies either had an insignificant sample size or the subspecies were listed with an outdated taxonomic nomenclature. An example of this is Saguinus fuscicollis, a species with known behavioral data and a limited number of specimens available. Excluding the entire species from this study would be unfortunate. Appendix 1 lists each specimen obtained for this study. The information includes museum number, taxonomic affiliation, specimen gender, locality data (included on the specimen box or skin tag) and any notes I made during the data collection process (such as if certain bones were missing or broken).

Features examined The breadth of the hypotheses in this study mandated a large sampling of both platyrrhine species but also a large number of post-cranial (hindlimb) features. The 29 quantitative measurements obtained were either used directly in this study or were used to obtain other analyses (i.e., bodyweight surrogates). The bones photographed and used in this study were the innominate, femur and tibia (when disarticulated from the fibula).

The measurements were chosen based on several criteria. There were either cited by previous researchers as having a functional or implied importance with regards to locomotor behavior; or they are perceived at having a direct relationship/ functional significance to hindlimb dominated locomotion. 65

Linear Measurements There are 27 hindlimb features and two cranial features and 8 non-quantitative measurements that were measured for this study. The cranial features were investigated as potential body size surrogates. The body size issue will be discussed in more detail later in this chapter. Of the twenty-seven hindlimb features, 26 are linear measurements and 1 is an angle. Table 2.4 lists the features that were measured in this study and a description of each. Figures 2.2 through 2.4 illustrate the linear measurements that were taken for this study (the abbreviations used correspond to Table 2.4).

Measurement Abbr. Description Femur

Femoral Neck Length FNL Most proximal central portion of the femoral head to the intertrochanteric crest.

Femoral Neck Thickness FNT Thickness just distal to the articular surface. A line perpendicular to femoral neck length.

Posterior Articular Most proximal central portion of the femoral head to the most distal portion of the articular Surface PAS surface.

Most proximal portion of the great trochanter to the most distal portion of the lateral Total Femur Length TFL condyle.

Lateral Condyle Width LCW Widest portion of the lateral condyle.

Medial Condyle Width MCW Widest portion of the medial condyle.

Lateral Condyle Most proximal portion of the lateral condyle to the most distal portion of the lateral Length LCL condyle.

Medial Condyle Most proximal portion of the medial condyle to the most distal portion of the medial Length MCL condyle.

Intercondylar Width ICW Widest span between the lateral and medial condyle.

Greater Trochanter Width of the greater trochanter measured at the midline of the femoral head. (not Width GTW illustrated)

Anterior/Posterior Shaft Diameter APD Shaft diameter of the femur measured at the mid-point of the femur.

Lateral Condyle Most anterior portion of the lateral condyle to the most posterior portion of the lateral Height LCH condyle.

Anterior Articular Most proximal central point of the femoral head to the most distal point of the articular Surface AAS surface.

Patellar Groove Width of the patellar groove measured at the middle of the femoral condyles. Includes the Length PGL lip(s) of the patellar groove.

Patellar Groove Most proximal central point of the patellar groove measured to the most distal central point Width PGW of the patellar groove.

Femoral Head Most proximal central point of the femoral head measured to the most distal central point Height FHH of the femoral head.

Femoral Head Most anterior point of the femoral head measured to the most posterior point of the Width FHW femoral head.

Medial Condyle Most anterior portion of the medial condyle measured to the most posterior portion of the Height MCH medial condyle.

Pelvis

Acetabulum Width ACW Width measured at the middle of the acetabulum.

Acetabulum Height ACH Height measured at the middle of the acetabulum.

Ilium Width ILW Width measured at the point of the posterior superior iliac spine.

Ilium Length ILL Measured from the mid-point of the acetabulum to the distal most point of the ilium.

Pubic Length PBL Measured from the mid-point of the acetabulum to the distal most point of the pubis.

Ischium Length ISL Measured from the mid-point of the acetabulum to the distal most point of the ischium.

Distal Projection of the Measured from the mid-point of the acetabulum to the distal most point of the ischio-pubic Ischium DII ramus.

Dorsal Projection of the Ischium DPI Measured from the dorsal most point of the ischium to the line (DII).

Angle

Femoral Neck Angle FNA Angle of the femoral neck to the long axis of the femur.

Skull

Bi-Zygomatic Width BZW Widest point measured by caliper between both zygomatic arches.

Length of mandible measured from the most proximal point of the mandibular condyle to Mandible Length MDL the mandibular symphysis.

Table 2.4 - Features Examined in this Study

Figure 2.2 - Pelvis Measurements

Figure 2.3 - Pelvis Measurements Cont.

Figure 2.4 - Femoral Measurements

Non-Quantitative Features There are eight qualitative long bone features that do not lend themselves to linear measurements. Each feature was identified as having a potential impact on locomotor behavior, and that will be further discussed in chapter 4. For each feature identified an assessment was made and a numerical grade was assigned. The metric was obviously different for each feature; the exact protocol is given below for each feature discussed. Figures 2.5 through 2.12 illustrate the non-quantitative features that are analyzed in Chapter 3.

These features were analyzed against the four platyrrhine typical locomotor groups, leapers, quadrupeds, climbers and suspensory animals. Species (taxa) with known locomotor behavior that that are less generalized and more specialized according to the behavioral data described previously. The leapers were represented by Pithecia, Callimico, Cebuella, Saguinus geoffroyi and Saguinus fuscicollis (group); species were grouped as leapers if they evidenced more than

35% leaping in their locomotor repertoir, preferably across multiple wild studies. The quadrupeds were represented by Chiropotes, Cacajao, Callithrix, Mico and Leontopithecus. The climbers were represented by Alouatta and Lagothrix; species are considered climbers when they include more than 20% climbing in their locomotor repertoir. See chapter 4 and Hunt et al. 69

(1996) for a discussion of the issues related to locomotor categories, including climbing. The forelimb suspensory group is represented by Ateles. An ANOVA is used to determine if there is a significant difference between means for the four locomotor groups. Tukey’s pairwise comparison is used to examine potential significant comparisons between the groups. A simple least squares means histogram is used to illustrate the differences between the groups.

Prominence of Intertrochanteric The robustness/presence or absence of the intertrochanteric line was graded on a scale of 1 to Line Fig. 2.5 4. (1 Distinctly visible line, 2 medium distinct line, 3 barely visible line, 4 absence of line.)

Lateral Margin of the The sharpness or gracility of the lateral margin of the patellar groove is graded on a scale of 1 Patellar Groove Fig. 2.6 to 3. (1 being gracile/rounded while 3 is sharp)

Orientation of the Femoral condyle orientation is graded on a scale of 1 to 4. (1 is distally oriented, 2 is Femoral Condyles Fig. 2.7 posteriorly oriented, 3 is distally and posteriorly oriented, while 4 is unable to be determined). Femoral Head Height Compared to Femoral head height is compared to greater trochanter height on a scale of 1 to 3. (1 both Greater Trochanter features are equal in height, 2 femoral head exceeds height of greater trochanter, 3 greater Height Fig. 2.8 trochanter exceeds height of the femoral head.) Prominence of Intertrochanteric The robustness/presence or absence of the intertrochanteric crest was grade on a scale of 1 to Crest Fig. 2.9 4. (1 distinctly visible crest, 2 medium distinct crest, 3 barely visible crest, 4 absence of crest).

Depth of Fig. The depth of the trochanteric fossa was graded on a scale of 1 to 3. (1 is deep fossa, 2 is Trochanteric Fossa 2.10 medium deep fossa, 3 is shallow fossa). The position of the lesser trochanter is graded on a scale of 1 to 3. (1 is a midline/medial Position of the Fig. placement of the lesser trochanter, 2 is a slightly posterior placement of trochanter, 3 is a Lesser Trochanter 2.11 posterior placement of the lesser trochanter.)

Medial Margin of Fig. The sharpness or gracility of the medial margin of the patellar groove is graded on a scale of 1 the Patellar Groove 2.12 to 3. (1 is a rounded margin, 2 is a medium sharp margin and 3 is a sharp margin) Table 2.5 - Non-Quantitative Features

Presence Robustness of the Intertrochanteric Line The intertrochanteric line is the approximate delineation between the femoral neck and the femoral shaft, anteriorly. It is the attachment point for the iliofemoral and pubofemoral hip capsule ligaments. Photographs of the platyrrhine taxa were examined and grades from one to 4 were assigned. 70

1. Distinctly visible intertrochanteric line (Fig. 2.5) 2. Medium distinct line 3. Barely visible line 4. Absence of visible line (Fig. 2.6)

Figure 2.5 - Alouatta caraya - Prominent intertrochanteric line (1) 71

Figure 2.6 - Saimiri boliviensis - Absence of intertrochanteric line (4)

Lateral Margin of the Patellar Groove The lateral margin of the patellar groove is of interest for the role that it plays in limiting dislocation of the patella during leaping. This will be discussed further in chapter 4. As the quadriceps muscles extend the leg, it is possible for patellar dislocation to occur laterally. Thus in leaping primates it has been hypothesized that a pronounced lateral margin can aid in keeping the patella from dislocating. Photographs of platyrrhine taxa were examined and a grade of 1 to

3 was assigned.

1. Rounded lateral margin – barely distinct (Fig. 2.7) 2. Medium sharp lateral margin – distinct 3. Sharp lateral margin – very distinct (Fig. 2.8) 72

Figure 2.7 - Cacajao calvus - Rounded lateral patellar lip (1) 73

Figure 2.8 - Ateles fusciceps robustus - Sharp/pronounced lateral patellar lip(3)

Orientation of the Femoral Condyles The orientation of the femoral condyles is of interest when one considers weight bearing through the femur to tibia. Femoral condyles that are oriented posteriorly (antero-posteriorly) are more elliptical in shape, while femoral condyles that are distally oriented (proximo-distally) are more circular in shape. Elliptical condyles provide more contact between the femur and meniscus during extension of the leg. Photographs of the platyrrhine taxa were examined and a grade of 1 to 4 was assigned.

1. Distally oriented femoral condyles (Fig. 2.9) 2. Posteriorly oriented femoral condyles 3. Distally and posteriorly oriented femoral condyles 74

4. Neither distally or posteriorly oriented femoral condyles (unable to decipher)

Figure 2.9 - Callimico goeldii - Posteriorly oriented femoral condyles (red arrow), distally oriented condyles (blue arrow) and distally and posteriorly oriented condyles (green arrows)

Femoral Head Height Compared to Greater Trochanter Height The association of femoral head height and greater trochanter height is examined here. The greater trochanter serves as an attachment point for the lateral rotators of the thigh and the hip abductors. This relationship can conceivably aid in joint excursion if the femoral head is equal to or above the greater trochanter, while an elongated greater trochanter would provide an expanded attachment point for the gluteus medius and minimus muscles. Photographs of the 75 platyrrhine taxa were examined and a grade of 1 to 3 was assigned based on the association of the greater trochanter and femoral head height.

1. The femoral head is equal in height to the greater trochanter (Fig. 2.10) 2. The superior most aspect of the femoral head is above the superior most aspect of the greater trochanter (Fig. 2.11) 3. The superior most aspect of the femoral head is below the superior most aspect of the greater trochanter.

Figure 2.10 - Callimico goeldii - Femoral head above greater trochanter (2) 76

Figure 2.11 - Chiropotes satanas - Femoral head equal to greater trochanter height (1)

Presence/Robustness of Intertrochanteric Crest The intertrochanter crest is the approximate delineation between the femoral neck and shaft of the femur, posteriorly. It is also the attachment point for the quadratus femoris muscle.

Photographs of the platyrrhine taxa were examined and a grade of 1 to 4 was assigned.

1. Distinctly visible intertrochanteric crest (possibly extending to the lesser trochanter) (Fig. 2.12) 2. Medium distinct crest 3. Barely visible crest (Fig. 2.13) 4. Absence of visible crest

Figure 2.12 - Ateles fusciceps robustus - distinctly visible crest (1) 78

Figure 2.13 - Callithrix jacchus jacchus - barely visible crest (3)

Depth of the Trochanteric Fossa The depth of the trochanteric fossa is of interest as the general location of four muscles responsible for hip movement. The trochanteric fossa lies medial to the greater trochanter and lateral to the femoral head. Photographs of platyrrhine taxa were examined and a grade of 1 to 3 was assigned.

1. Deep trochanteric fossa (Fig. 2.15) 2. Medium deep trochanteric fossa 3. Shallow trochanteric fossa (Fig. 2.14)

Figure 2.14 - Callimico goeldii - shallow trochanteric fossa (3) 80

Figure 2.15 - Ateles geoffroyi - Deep trochanteric fossa (1)

Position of the Lesser Trochanter The position of the lesser trochanter is of potential significance as an attachment point for flexers of the thigh. The position of the lesser trochanter varies slightly from a medial point (midline) to a ;posterior placement on the femur. A medial placement of the lesser trochanter would allow for the femur to be slightly abducted when fully flexed. Photographs of the platyrrhine taxa were examined and a grade of 1 to 3 was assigned based on the placement of the lesser trochanter.

1. Midline/medial placement of the lesser trochanter (Fig. 2.16) 2. More posterior placement of the lesser trochanter (half way between a midline and medial placement) 81

3. Posterior placement of the lesser trochanter (Fig. 2.17)

Figure 2.16 - Cebuella pygmaea - Medial/midline placed lesser trochanter (1) 82

Figure 2.17 - Alouatta caraya - Posterior placement of lesser trochanter (3)

Medial Margin of the Patellar Groove The medial margin of the patellar groove in primates is generally less distinct and pronounced than the lateral margin. The medial margin of the patellar groove would prevent dislocation of the patella medially in a chronically extended posture. Photographs of the platyrrhine taxa were examined and a grade of 1 to 3 were assigned.

1. Rounded medial margin (Fig. 2.19) 2. Medium sharp medial margin 3. Sharp medial margin (Fig. 2.18)

Figure 2.18 - Alouatta caraya - Robust medial condyle lip (3) 84

Figure 2.19- Leontopithecus rosalia - Rounded medial condyle lip (1)

Femoral Condyle Symmetry Femoral condyle symmetry is investigated to determine if there is a relationship between medial/ lateral symmetry and locomotor preference. Symmetrical condyles likely would be advantageous in adducted limb excursions, whereas abducted joint postures may benefit from a slightly more assymetrical arrangement. The platyrrhine wide sample and callitrichid only sample are represented in graph form. An ANOVA and Tukey’s Pairwise comparison are used to determine if there is significant difference in the means of the groups. Medial condyle width was subtracted from lateral condyle width. That result was divided by lateral condyle width giving a percent difference of symmetry. 85

Sex Specimen Origin Species # Male Female Unknown Wild Captive Comments Pithecia monachus 8 6 1 1 7 1 I assumed captive, no data given on tag Pithecia pithecia 16 8 4 4 14 2 Chiropotes satanas 9 5 4 0 9 0 Cacajao rubicundus 5 2 3 0 1 4 1 assumed wild, collected in wild, no other data given Cebus olivaceus 11 6 5 0 11 0 Cebus capucinus 13 7 4 2 11 2 1 assumed captive, no data given on tag Cebus albifrons 25 9 13 3 25 0 1 assumed wild, specimen tag read 'Amazon' Cebus apella 23 16 6 1 23 0 Callicebus torquatus 3 0 3 0 2 1 Callicebus moloch 9 7 2 0 9 0 Saimiri sciureus 36 17 16 3 36 0 1 assumed wild, specimen tag read 'Suriname' Saimiri boliviensis 22 11 11 0 22 0 Aotus vociferens 3 2 1 0 3 0 Aotus trivirgatus 2 1 1 0 2 0 Aotus nigriceps 4 3 1 0 4 0 Aotus boliviensis 18 7 10 1 18 0 Aotus trivirgatus griseimembra 5 2 3 0 5 0 Aotus lemurinus 8 3 5 0 8 0 Callimico goeldii 13 6 6 1 1 12 Saguinus nigricollis 25 14 9 2 23 2 Saguinus mystax 10 4 5 1 9 1 Saguinus midas 11 3 6 2 10 1 Saguinus oedipus 14 4 6 4 11 3 Saguinus leucopus 4 1 3 0 3 1 Saguinus imperator 3 1 2 0 2 1 Saguinus labiatus 5 3 2 0 0 5 Saguinus geoffroyi 4 2 2 0 4 0 Saguinus fuscicollis 9 2 6 1 4 5 Callithrix argentata (Mico) 5 2 2 1 0 5 Callithrix jacchus geoffroyi 3 1 1 1 0 3 Callithrix jacchus jacchus 10 5 5 0 3 7 Cebuella pygmaea 9 4 5 0 0 9 5 assumed to have died in captivity Leontopithecus chrysomelas 5 2 2 1 0 5 Leontopithecus rosalia 12 4 6 2 0 12 Allouatta caraya 15 7 7 1 15 0 Allouatta fusca 2 0 2 0 2 0 Allouatta belzebul 4 3 1 0 4 0 Allouatta palliata palliata 3 1 1 1 3 0 Allouatta palliata aequatorialis 7 6 1 0 7 0 Allouatta seniculus 20 10 8 2 20 0 Ateles fusciceps robustus 11 7 4 0 11 0 Ateles geoffroyi 5 1 3 1 5 0 Ateles paniscus 2 0 2 0 2 0 Ateles species (unknown ssp) 5 0 1 4 5 0 Brachyteles arachnoides 1 0 0 1 1 0 1 assumed wild, caught in wild and died in captivity Lagothrix lagothricha 5 2 3 0 3 2 Lagothrix lugens 4 3 1 0 3 1 Lagothrix cana 5 4 1 0 4 1 Lagothrix poeppigii 2 0 2 0 2 0 Table 2.6 - Species, Origin and Sexes of Specimens Obtained for this Study 86

Body Size Given the large range of body size among platyrrhines, I attempt to control for body size using regressions (both OLS and RMA) with species mean body mass as the independent variable.

Residuals from these regressions are compared in the analyses (Chapter 3). For the pithecid only analyses, regressions are run on individual specimens, which do not have associated body weights. Therefore, a surrogate for body mass was needed. In an effort to find a body size surrogate for use in analyses performed at the species level as well as in the platyrrhine wide comparisons, accurate body weight data was needed. Unfortunately, very few of the specimens with complete (or nearly complete) post-cranial elements also contain body weight information on the specimen tags or boxes. Table 2.5 shows the species, origin and sexes of the specimens obtained for this study. The Neil Tappen collection did have associated body weights for most of its specimens, however, this totaled very few species in this study overall. The literature was perused to find published wild-caught platyrrhine body weight data. Ford and Davis (1992) and

Smith and Jungers (1997) are collections of published body weight data. These two publications are often cited as sources for body weights of platyrrhines. In this study, a focus was placed on body weight data from wild-caught animals and an effort was made to obtain body weight data that was published in the time since both of these two major studies were done.

Body weight data collected in the wild is obviously rather difficult to obtain, this alone may explain the paucity of large scale body weight datasets. Table 2.6 contains as much of the published body weight data as can be located at the time of this study’s writing. For most of the publications, a combined male and female average was obtained. This is because sometimes the authors do not distinguish the difference between the genders. 87

Wild-Caught Body Weights Body Weight Sampl (gr) e M/F Source/Citation P. monachus 2284.50 2348 ? Ford and Davis 1992 - M+F 2100 5/2 Hershkovitz 1987 - M+F 2330 5/5 Ayres 1986 - M+F Smith and Junger 1997 - M+F - Compilation of 2360 16/10 multiple sources P. pithecia 1703.43 1624 ? Ford and Davis 1992 - M+F 1655 4/4 Ayres 1986 - M+F 1760 10/4 Smith and Jungers 1997 - M+F 2088 3/1 Mittermeier 1977 - M+F 1795 6/3 Oliveira et al. 1985 - M+F 1459 4/1 Hershkovitz 1987 - M+F 1543 5/3 Sanderson 1949 - M+F C. satanas 2806.40 2875 20/19 Hershkovitz 1985 - M+F 2770 18/21 Ayres 1986 - M+F 2482 17 Rosenberger 1992 - Unknown sexes 2875 16/17 Ayres 1981 - M+F - C. s. chiropotes 3030 5/4 Smith and Jungers 1997 - M+F C. rubicundus 3165.00 3165 ? Ford and Davis 1992 - M+F 3165 1/2 Ayres 1986 - M+F C. olivaceus 2499.50 2685 ? Ford and Davis 1992 - M+F 2905 28/10 Smith and Jungers 1997 - M+F 1908 2/1 Hill 1960 - M+F 2500 15/3 Cordero Rodriguez and Boher 1988 Smith and Jungers 1997 - M+F - Compilation of C. capucinus 3133.20 3110 16/10 multiple sources 3217 5/4/21 Crile and Quiring 1940 - M+F - 21 unknown sexes 3290 2/3 Schultz 1940 - M+F 3244 5/1 Schultz 1941 - M+F 2805 3/3 Glander et al. 1991 - M+F C. albifrons 2467.50 2735 26/15 Smith and Jungers 1997 - M +F 2147 ? Ford and Davis 1992 - M+F 2428 15 Rosenberger 1992 - Unknown sexes 2740 9/5 Jungers 1985 - M+F 2439 1/1 Defler 1979 - M+F 2316 2/1 Defler and Hernandez-Camacho 2002 - M+F C. apella 2940.43 3450 9/2 Fleagle and Mittermeier 1980 - M+F 3085 51/38 Smith and Jungers 1997 - M+F 2718 ? Ford and Davis 1992 - M+F 3675 5/2 Mittermeier 1977 - M+F 2110 38 Rosenberger 1992 - Unknown sexes 2910 20/21 Ayres 1986 - M+F 2635 8/8 Jungers 1985 - M+F

Neri et al. 1997 - M+F - Presumed subadults C. personatus 1250.00 1250 5/4 thrown out Smith and Junger 1997 - M+F - Compilation of C. torquatus 1189.67 1245 15/21 multiple sources 1121 14 Rosenberger 1992 - Unknown sexes 1203 1/6 Hershkovitz 1990 - M+F C. cupreus 1011.00 1070 10/2 Smith and Jungers 1997 - M+F 1065 8/2 Hershkovitz 1990 - M+F 898 3/2 Bicca-Marques et al. 2002 - M+F S. sciureus 767.88 688 ? Boinski et al. 2002 - M+F 687 7/4 Fooden 1964 - M+F 914 2/8 Sanderson 1949 - M+F 875 11/9 Jungers 1985 - M+F 860 4/6 Ayres 1986 - M+F 722 36 Rosenberger 1992 - Unknown sexes 764 ? Ford and Davis 1992 - M+F 633 14/17 Personal Data - Tappen Collection S. boliviensis 847.00 872 ? Boinski et al. 2002 - M+F 811 17/19 Smith and Jungers 1997 - M+F 858 ? Ford and Davis 1992 - M+F A. vociferans 703.00 703 20/20 Montoya 1990 - M +F A. trivirgatus 975.90 774.5 20/17 Smith and Jungers 1997 - M+F 860 16 Rosenberger 1992 - Unknown sexes 1220 3 Jungers 1985 - M+F 925 1/2 Ayres 1986 - M+F 1100 1/1 Fernandes 1993 - M+F A. nigriceps 957.50 957.5 1/2 Peres 1993 - M+F A. azarae 1227.50 1205 4/8 Smith and Jungers 1997 - M+F 1250 40/39 Fernandez-Duque 2007 - M+F - ? Wild weights? A. trivigatus griseimembra 966.00 966 20/16 Dixson 1983 - M+F Smith and Junger 1997 - M+F - Compilation of A. lemurinus 896.33 896 18/12 multiple sources 903 6/11 Crile and Quiring 1940 - M+F 890 7/6 Cooper and Hernandez-Camacho 1977 - M+F A. infulatus 1215.00 1215 1/1 Fernandes 1993 - M+F C. goeldii 490 494 1/2 Rowe and Myers 2016 - M+F 361 3/5 Encarnacion and Heymann 1998 - M+F S. nigricollis 449.33 407 13/10 Personal Data - Tappen Collection 465 ?/? Ayres 1986 - M+F 476 8/6 Smith and Jungers 1997 - M+F S. mystax 553.00 576 16/11 Garber and Teaford 1986 - M + F(inc. lactating) 571 30/29 Garber et al. 1993 - M+F 161/10 512 4 Garber and Teaford 1986 - M + F S. midas 546.00 545 34/15 Smith and Jungers 1997 - M+F 505 4/1 Ayres 1986 - M+F 533 16 Rosenberger 1992 - Unknown sexes 640 5/4 Sanderson 1949 - M+F

500 3/1 Mittermeier 1977 - M+F 509 ? Ford and Davis 1992 - M+F 590 23 Pack et al. 1999 - M+F S. oedipus 410.50 411 37/29 Savage et al. 1993 - M +F 410 6/15 Neymann 1978 - M+F S. leucopus 464.67 492 2/2 Hernadez Camacho and Defler 1985 - M+F 440 ? Robinson and Redford 1986 - M+F 462 8 Defler 2004 - M+F S. imperator 453.50 475 4/1 Smith and Jungers 1997 - M+F 432 9/8 Hershkovitz 1977 - M+F S. labiatus 485.70 509.5 136/77 Puertas et al. 1995 - M +F 444 6/3 Buchanan-Smith 1991 - M+F 493 17/12 Yoneda 1981 - M+F 496 34/18 Snowdon and Soini 1988 - M+F - Book 486 5 Garber and Leigh 2001 - M+F S. geoffroyi 522.20 497 53/41 Dawson 1978 - Book - M+F 492 55/40 Dawson and Dukelow 1976 - M+F 504 1/2 Nelson 1975 - M+F 614 2/2 Schultz 1941 - M+F 504 8/5 Hershkovitz 1977 - M+F S. fuscicollis 384.67 358 4/6 Garber and Leigh 2001 - M+F 351 69/55 Snowdon and Soini 1988 - M+F - Book 395 4/4 Ayres 1986 - M+F 366 39/31 Soini 1981 - M+F - S. f. nigrifrons 428 33/11 Garber and Teaford 1986 - M+F 410 4/3 Yoneda 1981 - M+F - S. f. weddelli C. argentata 345.00 345 8/10 Ayres 1986 - M+F C. jacchus geoffroyi 299.50 240 ? Ford and Davis 1992 - M+F 359 46 Rosenberger 1992 - Unknown sexes C. jacchus jacchus 330.00 320 69/86 Araujo et al. 2000 - M + F 340 12 Rosenberger 1992 - Unknown sexes C. pygmaea 120.50 125 14/17 Hershkovitz 1977 - M+F 116 36/27 Soini 1988 - M+F L. chrysomelas 578.00 578 9/6 Rosenberger and Coimbro Filho 1984 - M+F 622/21 L. rosalia 602.00 602 3 Dietz et al. 1994 - M + F mean of both seasons A. caraya 5698.57 5375 58/117 Rumiz 1990 - M + F 5825 10/7 Thorington et al. 1984 - M+F 5575 3/3 Rosenberger and Strier 1989 - M+F 6845 4/3 Jungers 1985 - M+F 4712 8 Rosenberger 1992 - Unknown sexes 5703 ? Ford and Davis 1992 - M+F 5855 14/10 Redford and Eisenberg 1992 - M+F A. fusca 5067.00 5540 4/5 Smith and Jungers 1997 - M+F 5388 3/3 Rosenberger and Strier 1989 - M+F 4273 7 Rosenberger 1992 - Unknown sexes A. belzebul 6086.25 6395 27/26 Peres 1994 - M+ F 90

6180 19/16 Ayres 1986 - M+F 6398 8/10 Rosenberger and Strier 1989 - M+F 5372 62 Rosenberger 1992 - Unknown sexes A. palliata 110/17 palliata 6621.67 6250 7 Peres 1994 - M+ F 6875 1/1 Schultz 1940 - M+F 6798 2/2 Schultz 1941 - M+F 7200 15/15 Thorington et al. 1979 - M+F 6357 10/10 Rosenberger and Strier 1989 - M+F 6250 12/27 Scott et al. 1976 - M+F A. palliata aequatorialis 6457.00 5275 14/18 Glander et al. 1991 - M+F 7200 15/15 Thorington et al. 1979 - M+F 6896 2/2/28 Crile and Quiring 1940 - M+F A. seniculus Smith and Junger 1997 - M+F - Compilation of seniculus 6212.56 5950 81/76 multiple sources 5490 45/32 Cordero Rodriguez and Boher 1988 6820 28/34 Ayres 1986 - M+F 5600 14/4 Rudran 1979 - M+F 6218 10/10 Rosenberger and Strier 1989 - M+F 6690 3/5 Jungers 1985 - M+F 7400 2 Rosenberger 1992 - Unknown sexes 4826 31/29 Braza et al. 1983 - M+F 6919 8/9 Hernandez-Camacho and Defler 1985 - M+F A. fusciceps robustus 9025.00 9025 6/11 Crile and Quiring 1940 - M+F A. geoffroyi 7676.00 7833 ? Ford and Davis 1992 - M+F Smith and Junger 1997 - M+F - Compilation of 7535 25/63 multiple sources 7500 2/8 Fedigan et al. 1988 - M+F 7710 22/34 Schultz 1940 - M+F 7544 20/32 Schultz 1941 - M+F 6/14/6 8110 3 Crile and Quiring 1940 - M+F 7500 2/12 Glander et al. 1991 - M+F A. paniscus paniscus 8393.75 8775 20/42 Smith 1996 - M +F 9020 16/35 Ayres 1986 - M+F 7675 4/7 Mittermeier 1977 - M+F 8105 ? Ford and Davis 1992 - M+F A. species 5809.00 5809 5 Personal Data - Tappen Collection L. lagothricha 6405.67 6920 3/5 Fooden 1963 - M+F 6105 6/7 Ayres 1986 - M+F 6192 16/1 Peres 1994 - M+ F L. lugens 7842.00 7842 2/1 Fooden 1963 - M+F - Very minimal sample L. cana 8310.00 8310 4/1 Peres 1994 - M+ F - Very minimal sample Lu 1999 - M+F - In Primates in Perspective - Di L poeppiggii 5815.00 5815 6/9 Fiore and Campbell Table 2.7 - Published Platyrrhine Bodyweight Data 91

In this study lateral condyle length of the femur was determined to be the best body size surrogate for analyses that take place at the species level. Lateral condyle length was determined to have an r of .990 and a slope of .333; it was also determined to be isometric, the slope of .333 fell within the 95% confidence intervals. Lateral condyle length was not the only (e.g., ilium length among others were also good) post-cranial measurement that was a statistically good fit, it was the best within this data set.

Levitch (1987) and Sears et al. (2008) have found cranial measurements to be statistically good body size surrogates within platyrrhines. Bi-zygomatic breadth and mandible length were measured with digital calipers and analyzed within this study. Unfortunately, neither of these was as good statistically as lateral condyle length.

As previously stated, the Neil Tappen collection did contain several species of platyrrhine with known body weights. These were incorporated into this study, however, because of the limited number of species with known body weights a body size surrogate was still needed. Table 2.7 shows the number of specimens in this study that had associated body weights.

# of Species Specimens Cebus albifrons 3 Cebus apella 1 Saimiri sciureus 30 Saguinus nigricollis 23 *Ateles (Species) 5 *Exact species unknown

Table 2.8 - Specimens with Associated Bodyweight

Statistical Analyses Used in this Study For this study, a combination of Past, Mystat (Systat) and Microsoft Excel softwares were used to produce the statistical outputs. Linear measurements were first examined to ensure that the data was intact; basic stats were run to determine if outliers or anomalies existed. Regressions were run, using Past, of the linear measurement features and published bodyweight data (both natural-log transformed). Regressions were run using both ordinary least squares and reduced major axis techniques. OLS and RMA lines are illustrated on all graphs where the techniques were employed.

For most of the linear measurements, the regressions are presented in three iterations. A platyrrhine wide graph illustrated the regression of the linear feature run against body mass taken from the literature (both variables natural log transformed), all forty-five species within my dataset are represented in these graphs. A callitrichid only regression(s), shows the regressions of the linear measurement against body mass (both variables log transformed), within the callitrichid only radiation. Finally, the pithecids are illustrated in their own graph, when the hypothesis warrants it. The pithecid only regressions are linear measurement versus lateral condyle length (body size surrogate) using individual pithecid specimens. The callitrichids and pithecids are presented separately from the other platyrrhines because the contrasts between leaping, quadrupedalism and climbing (sometimes) is most strongly described in these two radiations. All platyrrhine wide regressions and the vast majority of callitrichid and pithecid regressions are significant. The few regressions that are not significant are detailed in Table 3.1. 93

For non-linear measurements/features, a different approach was employed. The qualitative variables were examined and graded on a scale of 1 -3 or4. The platyrrhines with solid behavioral data or presumed locomotor modes were grouped into one of the four primary platyrrhine locomotor groupings, leaper, quadruped, climber and/or suspensory animals. An

ANOVA was run to determine if a significant difference exists in the means of the groups.

Tukey’s pairwise comparison was used to determine if significant comparisons between groups exists. A histogram of the four groups is also illustrative of the group’s relationships. All of these statistical analyses are expanded upon for each measurement presented in Chapter 3.

Chapter 3

Results Introduction This chapter presents the results from the analyses of the linear, angular, and qualitative variables of the hindlimb across platyrrhines. For the linear measurements, basic statistics and regressions were run using statistical software. For each linear variable discussed here, regressions were run at the platyrrhine-wide level using species means and species mean body mass from the literature

(discussed in Chapter 2). Additionally, regressions within the Pithecidae (using individual specimens and LCL as a size surrogate) and Callitrichidae (using species means and species mean body mass) are illustrated for the leaping and quadrupedal hypotheses because leaping/non-leaping and vertical clinging and leaping/non-VCL contrasts are primarily found in these two groups. For each regression presented, the reduced major axis (RMA) and ordinary least squares (OLS) regression lines are illustrated. The basic statistics are presented in Table

3.1. Functional discussions and additional clarifications will be discussed in Chapter 4.

There are eight qualitative long bone features that do not lend themselves to linear measurements. Each feature was identified as having a potential impact on locomotor behavior, 95 and that will be further discussed in Chapter 4. For each feature identified an assessment was made and a numerical grade was assigned. The metric was obviously different for each feature; the exact protocol is given below for each feature discussed.

These features were analyzed against the four platyrrhine typical locomotor groups, leapers, quadrupeds, climbers and suspensory animals. Species with known locomotor behavior that can be comfortably attributed were used. The leapers were represented by Pithecia, Callimico,

Cebuella, Saguinus geoffroyi and Saguinus fuscicollis (group). The quadrupeds were represented by Chiropotes, Cacajao, Callithrix, Mico and Leontopithecus. The climbers were represented by Alouatta and Lagothrix. The suspensory group is represented by Ateles. An

ANOVA is used to determine if there is a significant difference between means for the four locomotor groups. Tukey’s pairwise comparison is used to examine potential significant comparisons between the groups. A simple least squares means histogram is used to illustrate the differences between the groups.

Platyrrhine Wide Regressions OLS RMA Slope Conf. Int. Intercept r r² p Slope Conf. Int Intercept r r² p Acetabulum Height 0.39102 .375-.406 -2.8874 0.99152 0.98311 0.0001 0.39437 .378-.410 -2.9117 0.99152 0.98311 0.0001 Acetabulum Width 0.38744 .370-.403 -2.8257 0.99142 0.98291 0.0001 0.3908 .374-.406 -2.85 0.99142 0.98291 0.0001 Anterior Articular Surface 0.34954 .334-.365 -2.8927 0.98904 0.97821 0.0001 0.35341 .338-.369 -2.9209 0.98904 0.97821 0.0001 Posterior Articular Surface 0.36208 .347-.377 -2.9505 0.98844 0.97701 0.0001 0.36632 .352-.381 -2.9812 0.98844 0.97701 0.0001 Femoral Head Height 0.36253 .349-.377 -2.8138 0.99178 0.98363 0.0001 0.36554 .352-.381 -2.8356 0.99178 0.98363 0.0001 Femoral Head Width 0.35024 .336-.365 -2.6626 0.99137 0.98281 0.0001 0.35329 .338-.368 -2.6848 0.99137 0.98281 0.0001 Femoral Neck Length 0.33636 .323-.350 -2.0759 0.99167 0.98342 0.0001 0.33919 .325-.353 -2.0964 0.99167 0.98342 0.0001 Femoral Neck Thickness 0.29976 .281-.318 -2.5835 0.98453 0.9693 0.0001 0.30447 .287-.323 -2.6177 0.98453 0.9693 0.0001 Greater Trochanter Width 0.36889 .355-.383 -3.0967 0.98946 0.97902 0.0001 0.37282 .359-.386 -3.1252 0.98946 0.97902 0.0001 Ilium Width 0.29762 .271-.325 -1.89 0.96694 0.93498 0.0001 0.30779 .285-.333 -1.9639 0.96694 0.93498 0.0001 Ilium Length 0.41332 .398-.427 -1.45 0.99444 0.98892 0.0001 0.41563 .400-.429 -1.4668 0.99444 0.98892 0.0001 Intercondylar Space Width 0.37005 .350-.390 -3.4313 0.98481 0.96985 0.0001 0.37576 .358-.395 -3.4727 0.98481 0.96985 0.0001 Medial Condyle Length 0.32529 .311-.340 -2.2008 0.99256 0.98518 0.0001 0.32772 .313-.343 -2.2185 0.99256 0.98518 0.0001 Lateral Condyle Length 0.33281 .317-.348 -2.2642 0.98968 0.97947 0.0001 0.33628 .320-.352 -2.2894 0.98968 0.97947 0.0001 Patellar Groove Length 0.28077 .254-.305 -2.3148 0.97361 0.94791 0.0001 0.28838 .261-.313 -2.3701 0.97361 0.94791 0.0001 Patellar Groove Width 0.4048 .382-.426 -3.2519 0.98164 0.96361 0.0001 0.41237 .389-.434 -3.3069 0.98164 0.96361 0.0001 Pubic Width 0.39368 .365-.420 -2.0623 0.97657 0.95368 0.0001 0.40312 .377-.428 -2.1309 0.97657 0.95368 0.0001 Ischium Length 0.28504 .261-.309 -1.2519 0.97623 0.95303 0.0001 0.29198 .268-.315 -1.3023 0.97623 0.95303 0.0001 Dorsal Projection of Ischium 0.28553 .246-.330 -2.2324 0.92799 0.86117 0.0001 0.30768 .275-.348 -2.3933 0.92799 0.86117 0.0001 Distal Projection of Ischium 0.30804 .287-.330 -1.3951 0.98367 0.96761 0.0001 0.31315 .294-.335 -1.4323 0.98367 0.96761 0.0001 Table 3.1a – Basic stats for platyrrhine-wide regressions discussed in this chapter. Non-significance is indicated in red. Confidence intervals that cover .333 are in bold.

Callitrichid Regressions OLS RMA Slope Conf. Int Intercept r r² p Slope Conf. Int Intercept r r² p Acetabulum Height 0.43397 .381-.548 -3.1521 0.96593 0.93301 0.0001 0.44928 .349-.527 -3.2444 0.96593 0.93301 0.0001 Acetabulum Width 0.42928 .396-.584 -3.0885 0.9739 0.94848 0.0001 0.44079 .409-.573 -3.1579 0.9739 0.94848 0.0001 Anterior Articular Surface 0.34655 .319-.467 -2.8809 0.97041 0.9417 0.0001 0.35712 .334-.454 -2.9446 0.97041 0.9417 0.0001 Posterior Articular Surface 0.365 .308-.569 -2.9472 0.92299 0.85191 0.0001 0.39546 .289-.530 -3.1309 0.92299 0.85191 0.0002 Femoral Head Height 0.39992 .363-.550 -3.0335 0.9642 0.92969 0.0001 0.41476 .358-.531 -3.1231 0.9642 0.92969 0.0001 Femoral Head Width 0.39825 .353-.559 -2.9381 0.95986 0.92134 0.0001 0.41491 .336-.527 -3.0386 0.95986 0.92134 0.0001 Femoral Neck Length 0.40695 .374-.552 -2.4897 0.96843 0.93786 0.0001 0.42022 .383-.520 -2.5697 0.96843 0.93786 0.0001 Femoral Neck Thickness 0.39783 .337-.572 -3.1612 0.95526 0.91251 0.0001 0.41647 .309-.555 -3.2736 0.95526 0.91251 0.0001 Greater Trochanter Width 0.33697 .282-.572 -2.9074 0.90455 0.8182 0.0005 0.37253 .303-.482 -3.122 0.90455 0.8182 0.0002 Ilium Width 0.37318 .305-.674 -2.3484 0.88973 0.79161 0.001 0.41943 .321-.530 -2.6275 0.88973 0.79161 0.0008 Ilium Length 0.35783 .327-.472 -1.1226 0.96655 0.93422 0.0001 0.37021 .328-.455 -1.1973 0.96655 0.93422 0.0001 Intercondylar Space Width 0.40214 .323-.578 -3.6386 0.90723 0.82307 0.0002 0.44326 .256-.511 -3.8867 0.90723 0.82307 0.0002 Medial Condyle Length 0.39431 .361-.545 -2.6247 0.9697 0.94031 0.0001 0.40663 .373-.519 -2.699 0.9697 0.94031 0.0001 Lateral Condyle Length 0.39226 .343-.554 -2.6344 0.94608 0.89507 0.0001 0.41462 .331-.512 -2.7692 0.94608 0.89507 0.0001 Patellar Groove Length 0.41226 .354-.668 -3.1269 0.92846 0.86204 0.0004 0.44402 .369-.620 -3.3185 0.92846 0.86204 0.0002 Patellar Groove Width 0.41425 .356-.614 -3.3296 0.94498 0.89298 0.0001 0.43837 .367-.597 -3.4752 0.94498 0.89298 0.0002 Pubic Width 0.22817 .106-.345 -1.0418 0.86828 0.75392 0.0002 0.26279 .082-.317 -1.2506 0.86828 0.75392 0.0002 Ischium Length 0.40353 .365-.592 -1.9806 0.96483 0.93089 0.0001 0.41824 .387-.571 -2.0694 0.96483 0.93089 0.0001 Dorsal Projection of Ischium 0.34955 .230-.869 -2.6207 0.73676 0.54282 0.0376 0.47443 .381-1.50 -3.3742 0.73676 0.54282 0.036 Distal Projection of Ischium 0.38414 .343-.570 -1.8647 0.95867 0.91905 0.0001 0.40071 .367-.564 -1.9646 0.95867 0.91905 0.0001 Table 3.1b – Basic stats for callitrichid regressions discussed in this chapter. Non-significance is indicated in red. Confidence intervals that cover .333 are in bold.

Pithecid Regressions OLS RMA (Individual Specimens) Slope Conf. Int Intercept r r² p Slope Conf. Int Intercept r r² p Acetabulum Height 0.60408 .067-1.07 0.028888 0.40047 0.16038 0.0317 1.5084 .966-1.96 -0.24168 0.40047 0.16038 0.0332 Acetabulum Width 0.46911 0.12541 0.36271 0.13156 0.0539 1.2933 .754-1.76 -0.12119 0.36271 0.13156 0.0493 Anterior Articular Surface 0.64531 .421-.875 -0.3194 0.74309 0.55218 0.0001 0.86843 .671-1.06 -0.38766 0.74309 0.55218 0.0001 Posterior Articular Surface 0.45142 -0.22888 0.33053 0.10925 0.0857 1.3658 -0.50834 0.33053 0.10925 0.0782 Femoral Head Height 0.83111 .602-1.03 -0.21631 0.84849 0.71993 0.0001 0.97951 .774-1.16 -0.26167 0.84849 0.71993 0.0001 Femoral Head Width 0.80601 .558-1.01 -0.17023 0.81817 0.6694 0.0001 0.98514 .746-1.18 -0.22498 0.81817 0.6694 0.0001 Femoral Neck Length 1.2764 .890-1.57 0.13499 0.84146 0.70806 0.0001 1.5168 1.16-1.83 0.061495 0.84146 0.70806 0.0001 Femoral Neck Thickness 0.30601 -0.31276 0.28443 0.080901 0.1342 1.0759 -0.54807 0.28443 0.080901 0.1377 Greater Trochanter Width 0.42873 .156-.686 -0.3329 0.50292 0.25293 0.0054 0.85248 .596-1.06 -0.46241 0.50292 0.25293 0.0055 Ilium Width 1.0477 .535-1.51 0.18815 0.61377 0.37671 0.0004 1.7071 1.20-2.14 -0.00911 0.61377 0.37671 0.0006 Ilium Length 0.84138 .511-1.13 1.5113 0.70627 0.49881 0.0001 1.1913 .862-1.44 1.4066 0.70627 0.49881 0.0001 Intercondylar Space Width 0.69302 .360-1.07 -0.72962 0.5146 0.26481 0.0048 1.3467 .882-1.73 -0.92942 0.5146 0.26481 0.0049 Medial Condyle Length 0.86543 .641-1.08 0.054394 0.83463 0.6966 0.0001 1.0369 .814-1.22 0.001984 0.83463 0.6966 0.0001 Lateral Condyle Length 0.26549 .083-.450 0.24354 0.40047 0.16038 0.0326 0.66295 .391-.846 0.16022 0.40047 0.16038 0.0299 Patellar Groove Length 0.5247 .116-.838 -0.23709 0.46019 0.21178 0.0134 1.1402 .720-1.43 -0.42521 0.46019 0.21178 0.0146 Patellar Groove Width 0.38712 -0.05549 0.35767 0.12793 0.0526 1.0824 -0.2635 0.35767 0.12793 0.0535 Pubic Width 1.1822 .639-1.64 0.42455 0.65804 0.43302 0.0003 1.7966 1.30-2.21 0.24074 0.65804 0.43302 0.0002 Ischium Length 0.39865 .026-.665 0.86272 0.44976 0.20229 0.0153 0.88635 .541-1.18 0.71685 0.44976 0.20229 0.0131 Dorsal Projection of Ischium -0.80793 (-1.35- - .379) 0.25456 -0.47754 0.22804 0.0094 -1.6919 (-2.06- -1.10) 0.51903 -0.47754 0.22804 0.0104 Distal Projection of Ischium 0.84606 .444-1.16 0.72208 0.64095 0.41082 0.0001 1.32 .836-1.72 0.58027 0.64095 0.41082 0.0003 Table 3.1c – Basic stats for pithecid (individual specimens) regressions discussed in this chapter. Non-significance is indicated in red. Confidence intervals that cover .333 are in bold.

Leaping Hypotheses Hypothesis 1a – The pelvis of platyrrhines that engage in significant amounts of leaping from vertical supports will have a longer dorsal projection of the ischium

(Fleagle and Anapol 1992), and platyrrhines that engage in leaping from horizontal supports will have a dorsally longer ischium along with a distally longer ischium than quadrupedal, climbing, or suspensory platyrrhines (Fleagle and Anapol 1992).

The monkeys in the Leaping category leap primarily from a vertical position, and are therefore expected to exhibit a dorsally expanded ischium. However, they also engage in a fair degree of leaping from a horizontal position compared to the quadrupedal, climbing, or suspensory groups, and therefore may also exhibit a distally elongated ischium.

Dorsal Projection of the Ischium Prediction: VCL taxa (Pithecia, Callimico and Cebuella) will have a long dorsal projection of the ischium.

Species (specimens within the pithecid regressions) that fall above the regression line(s) will indicate a longer dorsal projection of the ischium for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively shorter dorsal projection of the ischium for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical dorsal projection of the ischium length for their associated body size (body size surrogate).

The regressions of dorsal projection of the ischium versus body mass across the platyrrhines

(Fig. 3.1) shows that within the callitrichids, Cebuella evidences a tendency towards a shorter dorsal projection of the ischium in contrast to what would be expected for the hypothesis. The 100 other callitrichids are clustered around the regression line(s), with Mico and Callithrix evidencing a slightly longer dorsal projection, something that would not be expected based on this hypothesis. Saimiri has a potentially shorter dorsal projection of the ischium which would be expected for the hypothesis. The other cebids tend to fall on and/or above the regression line(s) indicating a potentially longer dorsal projection of the ischium in the genus, this would not be expected for this hypothesis. The pithecids support the hypothesis. Pithecia evidences a longer dorsal projection of the ischium, while Cacajao and Chiropotes have a shorter dorsal projection relative to body size supporting the hypothesis. Within the atelids, Alouatta has a shorter dorsal projection relative to body mass, while Ateles has a longer dorsal projection relative to body mass. Alouatta supports the hypothesis as a non-leaper. Interestingly, Ateles has a longer dorsal projection of the ischium; while a nominal leaper, Ateles is not thought to be an acrobatic leaper. This will be further addressed in Chapter 4. An ANCOVA (Table 3.2 and

Figure 3.2) was calculated to illustrate the between group discrepancies. The adjusted means indicate that while leapers do have a longer dorsal projection than the quadrupeds, the brachiating taxa evidence a long dorsal projection as well. 101

0.5

-0.5 Centimeters -1

-1.5 4 5 6 7 8 9 10

Natural Log of Bodymass in Grams Natural Log of Dorsal Projection of the Ischium in in Ischium the of Projection Dorsal of Log Natural Pithecia Chiropotes Cacajao Cebus Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

Figure 3.1 – Platyrrhine Wide - Regression of species means dorsal projection of the ischium vs. body mass.

ANCOVA – DORSAL PROJECTION

Test for equal means, adjusted for covariate

Sum of sqrs df Mean square F p (same) Adj. mean: 0.231126 3 0.077042 5.378 0.003317 Adj. error: 0.573041 40 0.014326 Adj. total: 0.804167 43 Homogeneity (equality) of slopes: F : 1.75 p (same) 0.1737 Mean Adjusted mean Slope Leap -0.3697 -0.089722 0.39126 102

Quad -0.29469 -0.13221 0.29109 Climb 0.16391 -0.31962 0.70384 Suspend 0.52384 -0.047868 0.76716 Table 3.2 - ANCOVA Dorsal Projection

Figure 3.2 - ANCOVA - Dorsal Projection: Black = leapers, Red = Quadrupeds, Blue = Climbers, Green = Brachiators

The regressions of dorsal projection of the ischium versus body mass in the callitrichids (Fig.

3.3) shows that Cebuella falls on the RMA line and below the OLS line indicating a tendency towards a shorter dorsal projection of the ischium relative to body mass. Cebuella does not fit the hypothesis. Saguinus is divided with some species having longer dorsal projections and others shorter relative to body mass. Callithrix and Mico have longer dorsal projections of the ischium relative to body mass in contrast to what would be expected according to the hypothesis.

Leontopithecus supports the hypothesis by having a shorter dorsal projection of the ischium 103 relative to body mass. Callimico falls directly on both regression line(s) indicating an expected dorsal projection for the body size.

-0.2

Callimico -0.4 Saguinus -0.6 Mico

-0.8 Callithrix Cebuella -1

Ischium in Centimeters in Ischium Leontopithecus -1.2 OLS

Natural Log of Dorsal Projection of the the of Projection Dorsal of Log Natural -1.4 RMA 4 4.5 5 5.5 6 6.5 7 Natural Log of Bodymass in Grams

Figure 3.3 – Callitrichid Only - Regression of species means dorsal projection of the ischium vs. body mass. In the regressions of individual pithecid specimens versus LCL (Fig. 3.4), there is no support for the hypothesis. There is very little clustering that would suggest a functional correlation. 104

0.4

0.3 0.2 0.1 Pithecia 0 Chiropotes -0.1 Cacajao -0.2 OLS

the Ischium in Centimeters in Ischium the -0.3 RMA

Natural Log of Dorsal Projection of of Projection Dorsal of Log Natural -0.4 0 0.1 0.2 0.3 0.4 0.5 0.6 Natural Log of Lateral Condyle Length in Centimeters

Figure 3.4 - Within Pithecids - Regression of individual specimens dorsal projection of the ischium vs. LCL

Distal Projection of the Ischium Prediction: Taxa that leap primarily from horizontal supports will have a longer distal projection of the ischium compared to rarely leaping species.

Species (specimens within the pithecid regressions) that fall above the regression line(s) will indicate a longer distal projection of the ischium for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively shorter distal projection of the ischium for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical distal projection of the ischium length for their associated body size (body size surrogate).

The regressions of distal projection of the ischium versus body mass across the platyrrhines (Fig.

3.5) shows that within the callitrichids, Cebuella has a shorter distal projection of the ischium 105 relative to body size in contrast to the hypothesis. Leontopithecus chrysomelas has a slightly longer distal projection of the ischium relative to body size in contrast to the hypothesis. The other callitrichids fall on or close to the regression line(s) indicating an expected distal projection of the ischium for the given body mass. Within the cebids, Cebus has a slightly longer distal projection of the ischium relative to body mass, in contrast to the hypothesis. The pithecids,

Pithecia and Chiropotes, evidence a shorter distal projection relative to body mass while

Cacajao has a slightly longer distal projection relative to body size in contrast to the hypothesis.

Alouatta has a shorter distal projection relative to body mass in support of the hypothesis while two species of Ateles have a longer distal projection relative to body size in contrast to the hypothesis and predictions, though interesting given Ateles longer dorsal projection as well. A regression run with lateral condyle length (size surrogate) instead of body mass, illustrates the same tight fit to the regression line.

106

1.5

0.5

Centimeters 0

-0.5 4 5 6 7 8 9 10 Natural Log of Bodymass in Grams

Pithecia Chiropotes Cacajao Cebus Natural Log of Distal Projection of the Ischium in in Ischium the of Projection Distal of Log Natural Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

Figure 3.5 - Platyrrhine Wide - Regression of species means distal projection of the ischium vs. body mass The regression, of distal projection of the ischium versus body mass in the callitrichids (Fig. 3.6), shows that Mico and Callimico have an expected distal projection for their given body mass.

Cebuella has a slightly shorter distal projection than would be expected for the given body mass, contradicting the hypothesis. Saguinus species are split with some having a slightly longer

(Saguinus fuscicollis included) and some slightly shorter (Saguinus geoffroyi included) distal projection of the ischium than expected for the body mass. The quadrupedal Callithrix jacchus geoffroyi has a longer distal projection of the ischium than expected for the body mass contradicting the hypothesis, and has unexpectedly high residuals compared to its close relative

Callithrix jacchus jacchus. Similarly, Leontopithecus chrysomelas is above the line, while

Leontopithecus rosalia has a shorter distal projection relative to body mass. The expectations of 107 the hypothesis would have both species of Leontopithecus evidence a shorter to normal distal projection of the ischium for its given body mass. With the consideration that Cebuella is likely determining the placement of the line, a regression run without Cebuella (not illustrated) still has two of the three leaping callitrichids below the line.

0.7 0.6

0.5 Callimico 0.4 Saguinus 0.3 Mico 0.2 Callithrix 0.1 Cebuella 0

Ischium in Centimeters in Ischium -0.1 Leontopithecus -0.2 OLS

Natural Log of Distal Projection of the the of Projection Distal of Log Natural -0.3 RMA 4 4.5 5 5.5 6 6.5 7 Natural Log of Bodymass in Grams

Figure 3.6 - Callitrichid Only - Regression of species means distal projection of the ischium vs. body mass. The regression, of individual pithecid specimens versus LCL (Fig. 3.7), shows that Pithecia and

Chiropotes do not stand out as having a longer or shorter distal projection relative to body mass.

Cacajao, however, evidences a longer distal projection of the ischium relative to body size when

OLS is used, but not when RMA is used indicating mixed results, for that species; contradicting the hypothesis.

108

1.3

1.2

1.1

1 Pithecia 0.9 Chiropotes

0.8 Cacajao OLS

Ischium in Centimeters in Ischium 0.7 RMA

0.6 Natural Log of Distal Projection of the the of Projection Distal of Log Natural 0.5 0 0.1 0.2 0.3 0.4 0.5 0.6 Natural Log of Lateral Condyle Length in Centimeters

Figure 3.7 - Regression of individual specimens distal projection of the ischium vs. LCL

Summary Hypothesis 1a Dorsal Projection * 2 leaping Taxa (Pithecia ) support the hypothesis * An ANCOVA within Callitrichids is not significant * Interestingly, two distinct morphotypes within Pithecia in the within Pithecid regressions * Ateles indicates a long dorsal projection of the ischium and a long distal projection of the ischium

Distal Projection * Tight fit to the regression line * No taxa stand out in full support of the hypothesis * No taxa evidence a longer dorsal and distal projection of the ischium

Table 3.3 – Summary – Hypothesis 1a

109

Hypothesis 1b - Platyrrhines that engage in a high percentage of leaping behavior will have a hip that is characterized by a prominent intertrochanteric line (Fleagle and

Meldrum 1988), an expanded ilium compared to quadrupedal platyrrhines (Walker 1974), a short, thick femoral neck set perpendicular to the femoral shaft (Walker 1974; Fleagle and Meldrum 1988), a femoral articular surface that extends onto the superoposterior side of the femoral neck (Fleagle and Meldrum 1988), and a broad, flat greater trochanter that overhangs the anterior surface of the femur (Fleagle and Meldrum 1988).

Presence/Robustness of Intertrochanteric Line Prediction: Leaping taxa will evidence a prominent intertrochanteric line

Sum of df Mean F p (same) sqrs square Between 8.51682 3 2.83894 4.709 0.003448 groups: Within 107.92 179 0.602907 Permutation groups: p (n=99999) Total: 116.437 182 0.00366

omega2: 0.05731 Levene´s test for homogeneity of variance, from means p (same): 0.98 Levene´s test, from medians p (same): 0.8973 Welch F test in the case of unequal variances: F=4.641, df=63.11, p=0.005384 Table 3.4 - Analysis of Variance - Test for equal means - intertrochanteric line

Tukey’s Q below the diagonal, p above the diagonal. Significant comparisons are in red. Leap Quad Climb Suspend 110

Leap 0.995 0.2041 0.01875 Quad 0.343 0.1231 0.008695 Climb 2.769 3.112 0.7746 Suspend 4.12 4.463 1.351 Table 3.5 - Tukey's Pairwise Comparison - intertrochanteric line An ANOVA (Table 3.4) indicates a significant difference between means of the groups. A

Tukey’s pairwise comparison (Table 3.5) indicates significant comparisons exist. As is evidenced in the histogram, suspensory animals are set apart from the leapers and quadrupeds, but not the climbers, indicating suspensory animals evidence a more pronounced intertrochanteric line. With this data, it is not possible to determine more about the relationships between the leapers and quadrupeds, other than what is illustrated in the histogram (Fig. 3.8).

Table 3.6 presents the data as percentage by locomotor category, mimicking what is seen in the

ANOVA and histogram. The hypothesis that leapers would evidence a more pronounced intertrochanteric line than quadrupeds (or climbers/ suspensory animals) is not supported.

Leap Quad Climb Susp

1 0.00% 0.00% 7.46% 0.00%

2 13.46% 10.41% 14.92% 22.22%

3 34.62% 33.33% 44.77% 55.55%

4 52.00% 56.25% 32.83% 22.22%

Table 3.6 – Percentages by Measurement Category 111

Least Squares Means

3 INTERTROLINE 2

Climb Leap Quad Suspend GROUP$ Figure 3.8 - Least Squares Means Histogram - intertrochanteric line

Ilium Width Prediction: Leaping taxa will evidence a wider (more expanded) ilium than generalized quadrupeds

Species (specimens within the pithecid regressions) that fall above the regression line(s) will indicate a wider ilium for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively narrower ilium for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical ilium width for their associated body size (body size surrogate).

112

The regressions of ilium width versus body mass across the platyrrhines (Fig. 3.9) show that within the callitrichids, Cebuella falls has a narrower (less expansive) ilium relative to body mass, contradicting the hypothesis. Callithrix jacchus geoffroyi evidences a wider ilium relative to body size, again, contradicting the hypothesis. The other callitrichid species and cebid species show expected ilium expansion relative to body mass. All of the pithecid species fall above the line(s) indicating a tendency towards a wider (more expansive) ilium within the pithecids. A wider ilium relative to body size would support the hypothesis in regards to Pithecia, however,

Cacajao and Chiropotes contradict the hypothesis. Within the atelids, several Alouatta species evidence a narrower ilium relative to body mass supporting the hypothesis; while several Ateles

1.5

0.5

-0.5

-1

Natural Log of Ilium Width in Centimeters in Width Ilium of Log Natural 4 5 6 7 8 9 10 Natural Log of Bodymass in Grams Pithecia Chiropotes Cacajao Cebus Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA species possess a wider ilium.

113

Figure 3.9 – Platyrrhine Wide - Regression of species means ilium width vs. body mass

The regressions of ilium width versus body mass in the callitrichids (Fig. 3.10) shows that all the callitrichid species evidence an expected ilium width relative to body mass with the exception of

Callithrix jacchus geoffroyi. Mico and Callithrix jacchus jacchus species evidence a slightly narrower ilium, supporting the hypothesis. While, Callithrix jacchus geoffroyi lies obviously above the regression line indicating a wider ilium relative to body mass, contradicting the hypothesis. For the hypothesis to be fully supported, Callimico and Cebuella would need to evidence a wider ilium relative to body size.

0.2 0.1 Callimico 0 Saguinus -0.1 Mico -0.2 Callithrix -0.3 Cebuella -0.4 Centimeters Leontopithecus -0.5 -0.6 OLS Natuarl Log of Ilium Width in in Width Ilium of Log Natuarl -0.7 RMA -0.8 4 4.5 5 5.5 6 6.5 7 Natural Log of Bodymass in Grams

Figure 3.10 – Callitrichid Only - Regression of species means ilium width vs. body mass 114

The regressions of individual pithecid specimens versus LCL (Fig. 3.11) show that regardless of whether RMA or OLS analysis is employed Pithecia and Chiropotes specimens do not cluster in such a way as to evidence a conclusively wider or narrower ilium relative to body mass.

Cacajao specimens have a primarily wider ilium relative to body mass (body size surrogate) when OLS is used. However, when RMA is used Cacajao mimics Pithecia and Chiropotes by not clustering in an obvious way.

0.6

0.5

0.4 Pithecia 0.3 Chiropotes Cacajao

0.2 OLS RMA

0.1 Natural Log of lium Width in Centimeters in Width lium of Log Natural

0 0 0.2 0.4 0.6 0.8 1 Natural Log of Lateral Condyle Length in Centimeters

Figure 3.5 - Within Pithecids - Regression of individual specimens ilium width vs. LCL

115

Femoral Neck Length Predictions: Leaping taxa will have a short femoral neck compared to generalized quadrupeds.

Species (specimens within the pithecid regressions) that fall above the regression line(s) will indicate a longer femoral neck for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively shorter femoral neck for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical femoral neck length for their associated body size (body size surrogate).

The regressions of femoral neck length versus body mass across the platyrrhines (Fig. 3.12) show that Cebuella, with a short femoral neck relative to body mass, supports the hypothesis. Of the other callitrichids, Mico has a slightly longer femoral neck relative to body mass, also supporting this hypothesis. Callimico, however, lies on the line, in contrast to expectations. The pithecids and cebids straddle the regression line(s) and cluster close to it, evidencing average femoral neck length relative to body mass, in contrast to the expectation that Pithecia would have a shorter neck. Within the atelids, Alouatta fusca evidences a shorter femoral neck relative to body mass, contradicting the hypothesis, while Ateles geoffroyi evidences a longer femoral neck relative to body mass. To fully support the hypothesis, Pithecia and Callimico should evidence a shorter femoral neck; Pithecia straddles the regression lines while Callimico falls on the lines, contradicting the hypothesis.

116

1.5

0.5

-0.5

-1 4 5 6 7 8 9 10 Natural Log of Bodymass in Grams Pithecia Chiropotes Cacajao Cebus

Natural Log of Femoral Neck Length in Centimeters in Length Neck Femoral of Log Natural Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

Figure 3.12 - Platyrrhine Wide - Regression of species means femoral neck length vs. body mass

The regression of femoral neck length versus body mass in the callitrichid only sample (Fig.

3.13) show that the species cluster close to the regression line(s). Mico evidences a longer femoral neck relative to body mass, supporting the hypothesis. Callimico has a slightly shorter femoral neck relative to body mass, supporting the hypothesis. Most Saguinus species and

Leontopithecus have expected femoral neck length relative to body size. Cebuella, which supported the hypothesis in the platyrrhine wide regression, falls on the line in this regression.

Also, S. fuscicollis and S. geoffroyi show mixed results, with one above and one below the lines; ultimately the hypothesis is not supported by these mixed results. 117

0.3 0.2 Callimico 0.1 0 Saguinus -0.1 Mico -0.2 -0.3 Callithrix

Centimeters -0.4 Cebuella -0.5 -0.6 Leontopithecus -0.7

Natural Log of Femoral Neck Length in in Length Neck Femoral of Log Natural OLS -0.8 4 4.5 5 5.5 6 6.5 7 RMA Natural Log of Bodymass in Grams

Figure 3.6 - Callitrichid Only - Regression of species means femoral neck length vs. body mass

In the regressions of individual pithecid specimens versus LCL (Fig. 3.14), specimens of

Pithecia show neither a longer nor a shorter femoral neck relative to LCL (body size surrogate).

Chiropotes specimens have a shorter femoral neck relative to LCL, contradicting the hypothesis.

Cacajao specimens show a slight tendency towards a longer femoral neck relative to LCL, subtly supporting this hypothesis.

118

0.9

0.8

0.7

0.6 Pithecia 0.5 Chiropotes 0.4 Cacajao

0.3 OLS RMA 0.2

0.1 Natural Log of Femoral Neck Length in Centimeters in Length Neck Femoral of Log Natural 0 0 0.1 0.2 0.3 0.4 0.5 0.6 Natural Log of Lateral Condyle Length in Centimeters

Figure 3.14 - Within Pithecids - Regression of individual specimens vs. LCL

Femoral Neck Thickness Predictions: Leaping taxa will evidence a thick femoral neck compared to generalized quadrupeds.

Species (specimens within the pithecid regressions) that fall above the regression line(s) will indicate a thicker femoral neck for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively more gracile femoral neck for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical femoral neck thickness for their associated body size (body size surrogate).

The regressions of femoral neck thickness versus body mass across the platyrrhines (Fig. 3.15) shows that Cebuella evidences a more gracile femoral neck relative to body mass, contradicting 119 the hypothesis. With regards to the cebids, Saimiri has a more gracile (less thick) femoral neck relative to body mass, supporting the hypothesis. Pithecia evidences a thicker femoral neck relative to body size, supporting the hypothesis. Within the atelids, two of the three Ateles species have a thick femoral neck relative to body size and Alouatta fusca has a more gracile femoral neck relative to body size. While Ateles is known to leap, it is not generally regarded as an acrobatic leaper. The signal that the atelids are evidencing with regards to femoral neck thickness will be further addressed in hypothesis 4 as well as Chapter 4.

0.5

-0.5

-1

-1.5 4 5 6 7 8 9 10 Natural Log of Bodymass in Grams

Pithecia Chiropotes Cacajao Cebus Natural Log of Femoral Neck Thickness in Centimeters in Thickness Neck Femoral of Log Natural Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

Figure 3.15 - Platyrrhine Wide - Regression of species means femoral neck thickness vs. body mass 120

The regressions of femoral neck thickness versus body mass within the callitrichids (Fig. 3.16) show that Cebuella, Callimico, Mico and Saguinus all evidence a normal femoral neck thickness relative to body size, contradicting the hypothesis. Callithrix and Leontopithecus (both represented here by two species) each straddle the regression line(s) with one species evidencing a thicker femoral neck (Leontopithecus chrysomelas and Callithrix jacchus geoffroyi) relative to body size, while the other species (Leontopithecus rosalia and Callithrix jacchus jacchus) evidences a more gracile femoral neck relative to body size, contradicting the hypothesis. To fully support the hypothesis, Cebuella and Callimico should evidence a thicker femoral neck relative to body size, which they do not, while Mico, Callithrix and Leontopithecus should evidence a more gracile femoral neck relative to body mass, which they evidence mixed results.

The mixed results do not support the hypothesis.

-0.2 Callimico -0.4

Saguinus -0.6 Mico -0.8 Callithrix -1

Cebuella in Centimeters in -1.2 Leontopithecus -1.4 OLS

Natural Log of Femoral Neck Thickness Neck Femoral of Log Natural -1.6 RMA 4 4.5 5 5.5 6 6.5 7 Natural Log of Bodymass in Grams

121

Figure 3.16 - Callitrichid only - Regression of species means femoral neck thickness vs. body mass

The regressions of individual pithecid specimens versus LCL (Fig. 3.17) are not significant (p value > .05), thus the relationship to the regression line is meaningless. The quadrupedal taxa,

Chiropotes and Cacajao tend to cluster in the lower right quadrant of the regression graph, indicating a higher LCL and medium low to medium femoral neck thickness.

-0.05

-0.1

-0.15

-0.2

-0.25 Pithecia Chiropotes

Centimeters -0.3 Cacajao -0.35

-0.4 Natural Log of Femoral Neck Thickness in in Thickness Neck Femoral of Log Natural -0.45

-0.5 0 0.1 0.2 0.3 0.4 0.5 0.6 Natural Log of Lateral Condyle Length in Centimeters

Figure 3.17 - Within Pithecids - Regression of individual specimens femoral neck thickness vs. LCL

Femoral Neck Angle Predictions: Leapers will show a perpendicular femoral neck. 122

Femoral neck angle is examined to determine if there is a relationship between a higher (or lower) angle and any one locomotor grouping. The higher femoral neck angle, likely, relates to a more biomechanically abducted posture. Whereas, a lower femoral neck angle would indicate a femoral neck that is more perpendicular to the long shaft of the femur.

In the platyrrhine wide sample (Fig. 3.18), Callicebus and two of the three Ateles species cluster as having a high femoral neck angle compared to the other platyrrhine taxa. Several Saguinus species, Aotus, and Saimiri fall out as having a lower femoral neck angle. In order to fully support the hypothesis, the leapers (Pithecia, Cebuella, Callimico, etc.) should have a lower femoral neck angle.

136

134 132 130 128 126

124 Angle Neck Femoral 122

Pithecia Chiropotes Cacajao Cebus Callicebus Saimiri Aotus Saguinus Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Callimico

Figure 3.18 - Platyrrhine Wide Femoral Neck Angle in Degrees

123

As is illustrated in the callitrichid only graph (Fig. 3.19), several Saguinus species fall out as having a lower femoral neck angle. Mico has the highest femoral neck angle of the callitrichids, supporting the hypothesis. The leaping callitrichids, Callimico and Cebuella, fall in the middle having neither a high neck angle nor a low one.

132

131

130

Callimico 129 Saguinus 128 Mico 127 Callithrix Cebuella 126 Femoral Neck Angle Neck Femoral Leontopithecus 125

124

123

Figure 3.19 - Callitrichid Only - Femoral Neck Angle in Degrees

Sum of df Mean F p (same) sqrs square Between 186.916 3 62.3053 3.807 0.01119 groups: Within 2912.8 178 16.364 Permutation groups: p (n=99999) Total: 3099.71 181 0.01082

omega2: 0.04423 Levene´s test for homogeneity of variance, from means p (same): 0.4132 Levene´s test, from medians p (same): 0.4644 Welch F test in the case of unequal variances: F=3.444, df=62.08, p=0.02196 124

Table 3.7 - Analysis of Variance - Test for equal means femoral neck angle

Tukey’s Q below the diagonal, p above the diagonal. Significant comparisons are in red. Leap Quad Climb Suspend Leap 0.5937 0.4845 0.0006485 Quad 1.77 0.9982 0.04377 Climb 2.013 0.2428 0.06856 Suspend 5.474 3.703 3.46 Table 3.8 - Tukey's Pairwise Comparison femoral neck angle

For the purpose of clarity, an ANOVA was run to determine if there were significant differences in the means of the four primary platyrrhine locomotor groups with regards to femoral neck angle. The ANOVA (Table 3.7) indicated that a significant difference exists. Tukey’s pairwise comparisons (Table 3.8) indicates that several significant comparisons exist. As is illustrated in the least squares means histogram (Fig. 3.20), Suspensory animals are significantly set apart from leapers and quadrupeds, while comparisons between climbers, leapers and quadrupeds indicate an insignificant relationship. This indicates that suspensory animals have a slightly higher femoral neck angle than either leapers or quadrupeds, given the data used. The hypothesis is not supported by this data, leapers are not indicated as having a specifically more perpendicular femoral neck compared to quadrupeds with the given data.

125

Least Squares Means

147

140

133

126 NECKANGLE

119

112

Climb Leap Quad Suspend GROUP$ Figure 3.20 - Least Squares Means Histogram - Femoral Neck Angle

Posterior Articular Surface of the Femoral Head Predictions: Leaping taxa will have a more expanded posterior articular surface.

Species (specimens within the pithecid regressions) that fall above the regression line(s) will indicate a more expansive posterior articular surface for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively less expansive posterior articular surface for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical posterior articular surface for their associated body size (body size surrogate). 126

The regressions of posterior articular surface versus body mass across the platyrrhines (Fig. 3.21) shows that the majority of species have a normal articular surface relative to body size.

Nonetheless, both Saimiri species evidence a smaller (less expansive) posterior articular surface area relative to body mass, supporting the hypothesis. Mico and Pithecia species have a larger

(more expansive) articular surface area relative to body size; this is supportive of the hypothesis with regards to Pithecia. Within the Atelidae, two of the three Ateles species have a slightly more expansive posterior articular surface area relative to body size.

0.5

-0.5

-1

-1.5

-2 Femoral Head in Centimeters in Head Femoral 4 5 6 7 8 9 10 Natural Log of Bodymass in Grams Pithecia Chiropotes Cacajao Cebus

Natural Log of the Posterior Articular Surface of hte hte of Surface Articular Posterior the of Log Natural Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

Figure 3.21 - Platyrrhine Wide - Regression of species means post. articular surface vs. body mass 127

The regressions of posterior articular surface area versus body mass in the callitrichid (Fig. 3.22) only sample show that Cebuella and Callimico have a normal articular surface extent relative to body size, contradicting the hypothesis. Leontopithecus has a slightly smaller articular surface relative to body mass, supporting the hypothesis. Mico evidences a more expanded posterior articular surface relative to body size contradicting the hypothesis. Callithrix and Saguinus have species that evidence slightly higher positive and negative residuals indicating that species within the genera Callithrix and Saguinus may show expanded or less expansive posterior articular surface areas relative to body size, respectively.

-0.2 Callimico -0.4 Saguinus -0.6 Mico -0.8 Callithrix -1 Cebuella

-1.2 Leontopithecus Centimeters -1.4 OLS -1.6 RMA

Surface of the Femoral Head in Head Femoral the of Surface 4 4.5 5 5.5 6 6.5 7 Natural Log of the Posterior Articular Articular Posterior the of Log Natural Natural Log of Bodymass in Grams

Figure 3.22 – Callitrichid Only - Regression of species means post. articular surface vs. body mass

The regressions of individual Pithecia specimens versus LCL (Fig. 3.23) are not significant (p value > .05) thus the relationship to the regression line(s) is meaningless. The quadrupedal taxa, 128

Chiropotes and Cacajao, tend to cluster on the right side of the regression graph indicating a larger LCL (body size surrogate) and moderate posterior articular surface extent, however, a means test was not significant for Pithecia (leapers) vs. Cacajao and Chiropotes (quadrupeds) (p

= .276) and for a size controlled index (post. Articular surface/ LCL) (p = .102). .

0.3

0.2

0.1

0 Pithecia -0.1 Chiropotes Cacajao

-0.2 Femoral Head in Centimeters in Head Femoral

-0.3 Natural Log of the Posterior Articular Surface of the the of Surface Articular Posterior the of Log Natural -0.4 0 0.1 0.2 0.3 0.4 0.5 0.6 Natural Log of Lateral Condyle Length in Centimeters

Figure 3.23 - Within Pithecids - Regression of individual specimens post. articular surface vs. LCL

Greater Trochanter Width Predictions: Leaping taxa will have a wider greater trochanter than generalized quadrupeds.

Species (specimens within the pithecid regressions) that fall above the regression line(s) will indicate a wider greater trochanter for the assumed body size; whereas species that locate below 129 the regression line(s) will be considered to have a relatively narrower greater trochanter for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical greater trochanter width for their associated body size (body size surrogate).

The regressions of greater trochanter width versus body size across the platyrrhines (Fig. 3.24) show that within the callitrichids, the taxa evidence expected greater trochanter widths relative to body size. In the cebids, taxa show expected greater trochanter widths relative to body mass.

Both species of Pithecia demonstrate a wider greater trochanter relative to body size, supporting the hypothesis, however this is tempered by the Saimiri and Callithrix species that fall above the line, in contrast to the hypothesis. For the most part, the atelids cluster close to the regression line, evidencing normal greater trochanter widths relative to body size. 130

0.5

-0.5

-1

-1.5

-2 4 5 6 7 8 9 10 Natural Log of Bodymass in Grams Pithecia Chiropotes Cacajao Cebus

Callicebus Saimiri Aotus Callimico Natural Log of Greater Trochanter Wdith in Centimeters in Wdith Trochanter Greater of Log Natural Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

Figure 3.24 - Platyrrhine Wide - Regression of species means greater trochanter width vs. body mass The regressions of greater trochanter width versus body mass in the callitrichid only sample (Fig.

3.25) show that the majority of taxa have an expected greater trochanter width relative to body size. Callithrix jacchus geoffroyi evidences a wider greater trochanter relative to body size, contradicting the hypothesis. In order to fully support the hypothesis, the leaping callitrichids,

Cebuella and Callimico, should evidence a wider greater trochanter relative to body mass, however, they both fall on the line. The hypothesis is also not supported by S. fuscicollis (on the line) and S. geoffroyi (below the line). 131

-0.2

-0.4 Callimico

Saguinus -0.6 Mico -0.8 Callithrix -1

Cebuella in Centimeters in -1.2 Leontopithecus -1.4 OLS

-1.6 RMA Natural Log of Greater Trochanter Width Width Trochanter Greater of Log Natural 4 4.5 5 5.5 6 6.5 7 Natural Log of Bodymass in Grams

Figure 3.25 - Callitrichid Only - Regression of species means greater trochanter width vs. body mass

The regressions of individual pithecid specimens versus LCL (Fig. 3.26) show that regardless of the regression analysis used, Pithecia and Cacajao specimens evidence normal greater trochanter widths relative to the body size surrogate. Chiropotes, however, evidences expected greater trochanter width relative to LCL when OLS analysis is employed. When RMA is used

Chiropotes specimens evidence a narrower greater trochanter, supporting the hypothesis.

132

-0.05

-0.1

-0.15 Pithecia -0.2 Chiropotes Cacajao Centimeters -0.25 OLS

-0.3 RMA

Natural Log of Greater Trochanter Width in in Width Trochanter Greater of Log Natural -0.35

-0.4 0 0.1 0.2 0.3 0.4 0.5 0.6 Natural Log of Lateral Condyle Length in Centimeters

Figure 3.26 - Within Pithecids - Regression of individual specimens greater trochanter width vs. LCL

Summary Hypothesis 1b Intertrochanteric Line * Leapers do not evidence a more pronounced Intertrochanteric Line

Ilium Width * Mixed results do not support the hypothesis

Femoral Neck Length * All taxa fit close to the lines, locomotor groups are not distinguished by this feature

Femoral Neck Thickness * Pithecia, Ateles and several quadrupedal taxa evidence a thick femoral neck * The Pithecid only regression is not significant 133

Femoral Neck Angle * Leapers do not have a more perpendicular femoral neck compared to quadrupeds

Posterior Articular Surface * Locomotor groups are not differentiated by this feature * The Pithecid only regression is not significant

Greater Trochanter Width * Pithecia, one Saimiri and one Callithrix evidence a wide greater trochanter. * Majority of taxa cluster close to the regression line

Table 3.9 – Summary – Hypothesis 1b

Hypothesis 1c – Platyrrhines that engage in a high percentage of leaping behavior will have a knee that is characterized by symmetrical femoral condyles (Fleagle and Meldrum 1988), narrower patellar groove (Walker 1974) with a more prominent lateral lip (Fleagle and

Meldrum 1988) compared to quadrupedal platyrrhines and distally oriented femoral condyles (Walker 1974).

Femoral Condyle Symmetry Prediction: Leaping taxa will evidence more symmetrical femoral condyles that quadrupedal taxa.

Femoral condyle symmetry is investigated to determine if there is a relationship between medial/ lateral symmetry and locomotor preference. Symmetrical condyles likely would be advantageous in adducted limb excursions, whereas abducted joint postures may benefit from a slightly more assymetrical arrangement. The platyrrhine wide sample and callitrichid only 134 sample are represented in graph form. Medial condyle width was subtracted from lateral condyle width. That result was divided by lateral condyle width giving a percent difference of symmetry.

Femoral condyle symmetry is illustrated in Fig. 3.27. The atelids, Ateles and Lagothrix, evidence a high asymmetry. The other platyrrhine taxa seem to cluster, indicating a generally slightly wider lateral condyle than medial. The leaping taxa, Pithecia, Callimico, Saguinus geoffroyi and Saguinus fuscicollis evidence more symmetrical condyles, supporting the hypothesis. Cebuella evidences quite high asymetry, while Aotus and Callithrix among other primarily quadrupedal taxa evidence symmetrical condyles, contradicting the hypothesis.

0.3 0.25 0.2 0.15

0.1 0.05

0 Symmetry

Pithecia Chiropotes Cacajao Cebus

Callicebus Saimiri Aotus Saguinus Condyle Femoral of Difference Percent Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Callimico

Figure 3.27 - Platyrrhine Wide femoral condyle symmetry In the callitrichid only sample of femoral condyle symmetry (Fig. 3.28), Cebuella evidences assymetrical condyles, along with several other taxa. Callimico evidences symmetrical condyles compared to the other callitrichids. To fully support the hypothesis, all the leaping taxa would 135 show more symmetrical condyles, while the non-leaping (quadrupedal) taxa would have consistently aymmetrical condyles.

0.16

0.14

0.12 Callimico

0.1 Saguinus Mico 0.08

Callithrix Symmetry 0.06 Cebuella

0.04 Leontopithecus

0.02 Perceent Difference of Femoral Condyle Condyle Femoral of Difference Perceent

Figure 3.28 - Callitrichid Only - femoral condyle symmetry

Sum of sqrs df Mean square F p (same) Between 0.358533 3 0.119511 15.39 <.00005 groups: Within 1.3897 179 0.00776368 Permutation groups: p (n=99999) Total: 1.74823 182 .00001

omega2: 0.1909 Levene´s test for homogeneity of variance, from means p (same): 0.4753 Levene´s test, from medians p (same): 0.4735 Welch F test in the case of unequal variances: F=17.92, df=65.45, p=1.341E-08 Table 3.10 - Analysis of Variance - Test for equal means femoral condyle symmetry 136

Tukey’s Q below the diagonal, p above the diagonal. Significant comparisons are in red.

Leap Quad Climb Suspend Leap 0.646 0.004296 <.00005 Quad 1.654 0.125 <.00005 Climb 4.756 3.102 0.0008204 Suspend 10.14 8.49 5.388 Table 3.11 - Tukey's Pairwise Comparison - Femoral Condyle Symmetry

An ANOVA was used to determine if there is significant differences between the means of the four typical platyrrhine locomotor groups. The ANOVA (Table 3.10) found that a significant difference exists. Tukey’s pairwise comparison (Table 3.11) was run indicating significant comparisons exist. Climbers and suspensory animals fall out as being significantly more asymetrically than leapers and quadrupeds, supporting the hypothesis. Suspensory animals are also significantly higher in terms of assymetry than climbers. The hypothesis would have the leaping taxa being more symmetrical than the quadrupedal taxa, while the relationship between climbers and brachiating taxa is interesting, it will be addressed later. The histogram evidences a size relationship along with condyle symmetry; climbing and brachiating taxa are larger bodied, while the leapers and quadrupeds tend to be smaller bodied. These relationships are illustrated in the least squares means histogram (Fig. 3.29).

137

Least Squares Means

1.0

0.5

0.0 SYMMETRY

-0.5

-1.0

Climb Leap Quad Suspend GROUP$ Figure 3.29 - Least Squares Means Histogram - femoral condyle symmetry

Patella Groove Width Prediction: Leaping taxa will have a narrower patellar groove than more quadrupedal taxa.

Species (specimens within the pithecid regressions) that fall above the regression line(s) will indicate a wider patellar groove for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively narrower patellar groove for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical patellar groove width for their associated body size (body size surrogate). 138

The regressions of patellar groove width versus body mass across the platyrrhines (Fig. 3.30) show that the callitrichids, Cebuella, Mico, Saguinus and Leontopithecus evidence a normal patellar groove width relative to body size. Callithrix species evidence an expected patellar groove width for their body size. The cebids, Cebus and Callicebus show a wider patellar groove relative to body size, supporting the hypothesis. The pithecids all evidence a wider patellar groove relative to body size, Pithecia has the highest residuals and contradicts the hypothesis. Within the atelids, three Alouatta species evidence a narrower patellar groove relative to body size, while two Ateles evidence a wider patellar groove relative to body size.

Mixed results contradict the hypothesis.

0.5

-0.5

-1

-1.5

-2 4 5 6 7 8 9 10 Natural Log of Bodymass in Grams

Pithecia Chiropotes Cacajao Cebus Callicebus Saimiri Aotus Callimico

Natural Log of Patellar Groove Width in Centiimeters in Width Groove Patellar of Log Natural Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

139

Figure 3.30 - Platyrrhine Wide - Regression of species means patellar groove width vs. body mass

The regressions of patellar groove width versus body mass in the callitrichid only sample (Fig.

3.31) show that Cebuella, Callimico and Leontopithecus evidence normal patellar groove widths relative to body size, contradicting the hypothesis. Mico and Callithrix jacchus geoffroyi evidence a wider patellar groove relative to body size, supporting the hypothesis. Callithrix jacchus jacchus has a narrower patellar groove relative to body size and several Saguinus species are mixed above and below the line, contradicting the hypothesis.

-0.2

-0.4 Callimico

Saguinus -0.6 Mico -0.8 Callithrix -1 Centimeters Cebuella -1.2 Leontopithecus -1.4 OLS

Natural Log of Patellar Groove Width in in Width Groove Patellar of Log Natural -1.6 RMA 4 4.5 5 5.5 6 6.5 7 Natural Log of Bodymass in Grams

Figure 3.31 - Callitrichid Only - Regression of species means patellar groove width vs. body mass

The regressions of individual pithecid specimens versus LCL (Fig. 3.32) are not significant (p value > .05), thus relationship to the regressions line(s) is meaningless. Nonetheless, the 140 quadrupedal taxa, Chiropotes and Cacajao cluster in the upper right quadrant of the regression graph indicating a wider patellar groove and larger LCL (body size surrogate).

0.4

0.3

0.2

0.1 Pithecia

0 Chiropotes Centimeters Cacajao -0.1

Natural Log of Patellar Groove Width in in Width Groove Patellar of Log Natural -0.2

-0.3 0 0.1 0.2 0.3 0.4 0.5 0.6 Natural Log of Lateral Condyle Length

Figure 3.32 - Within Pithecids - Regression of individual specimens patellar groove width vs. LCL

Lateral Margin of the Patellar Groove Predictions: Leaping taxa will evidence a sharper more distinct lateral lip than quadrupedal taxa.

Sum of df Mean F p (same) sqrs square Between 1.24532 3 0.415107 0.9383 0.4234 groups: 141

Within 78.3016 177 0.442382 Permutation groups: p (n=99999) Total: 79.547 180 0.425

omega2: 0 Levene´s test for homogeneity of variance, from means p (same): 0.2347 Levene´s test, from medians p (same): 0.08644 Welch F test in the case of unequal variances: F=1.024, df=67.91, p=0.3874 Table 3.12 - Analysis of variance - test for equal means – lateral patellar lip

Tukey’s Q below the diagonal, p above the diagonal. Significant comparisons are in red. Leap Quad Climb Suspend Leap 0.6892 0.9838 0.9271 Quad 1.556 0.8815 0.3152 Climb 0.5117 1.045 0.7623 Suspend 0.8707 2.427 1.382 Table 3.13 - Tukey's Pairwise comparison - lateral patellar lip

An ANOVA (Table. 3.12) indicates that there is a not a significant difference between means for the groups. In essence, for the purposes of this study, the means for the groups are equal. A

Tukey’s pairwise comparison (Table. 3.13) cannot be used, as the p values are not significant.

As can be seen by the histogram (Fig. 3.33), the four groupings do not separate themselves from each other in a way that can be useful to this study. The hypothesis is not supported.

142

Least Squares Means

LATERALLIP 1

Climb Leap Quad Suspend GROUP$ Figure 3.33 - Least squares means histogram - Lateral patellar lip

Orientation of the Femoral Condyles Prediction: Leaping taxa will have more distally oriented femoral condyles than quadrupedal taxa.

Sum of df Mean F p (same) sqrs square Between 63.1918 3 21.0639 31.83 <.00005 groups: Within 117.803 178 0.661813 Permutation groups: p (n=99999) Total: 180.995 181 .00001 143

omega2: 0.3369 Levene´s test for homogeneity of variance, from means p (same): <.00005 Levene´s test, from medians p (same): 0.0513 Welch F test in the case of unequal variances: F=63.38, df=93.03, p=2.082E-22 Table 3.14 - Analysis of variance - test for equal means - condyle orientation

Tukey’s Q below the diagonal, p above the diagonal. Significant comparisons are in red. Leap Quad Climb Suspend Leap 0.9973 <.00005 <.00005 Quad 0.2797 <.00005 <.00005 Climb 8.056 7.776 0.2226 Suspend 10.76 10.48 2.705 Table 3.15 - Tukey's Pairwise comparison - condyle orientation

An ANOVA (Table 3.14) indicated significant differences between groups. A Tukey’s pairwise comparison (Table 3.15) revealed significant comparisons. As can be seen in the histogram (Fig.

3.34), climbers and suspensory animals tend to have femoral condyles that are shaped in such a way that neither a distal nor posterior orientation stands out. Whereas, leapers and quadrupeds have femoral condyles that are more antero-posteriorly oriented, contradicting the hypothesis.

From this data, little can be said about differences between climbers and suspensory animals or leapers and quadrupeds, beyond what is shown in the histogram; however, there is obviously some size distinction as well. The two morpho-types that separate based on condyle orientation are also grouped by size. Leapers and quadrupeds are smaller bodied while the brachiating/suspensory taxa and climbers are larger bodied. 144

Least Squares Means

2 CONDYLEORIENT 1

Climb Leap Quad Suspend GROUP$ Figure 3.34 - Least squares means histogram - Femoral condyle orientation

Summary Hypothesis 1c Femoral Condyle Symmetry *Leaping taxa do not separate themselves from the other taxa *Ateles and Lagothrix have the slightest percentages of asymmetry (and are the largest in terms of size) *Hypothesis is not supported

145

Patellar Groove Width *Pithecia has the highest residuals in the all platyrrhine regression *The hypothesis is not supported

Lateral Margin of the Patellar Groove *The ANOVA is not significant *The hypothesis is not supported

Orientation of the Femoral Condyles *Leapers and quadrupeds separate themselves from brachiators and climbers *Leapers and quadrupeds have more antero- posteriorly oriented condyles *The hypothesis is not supported, because the leapers and quadrupeds are not distinguished from one another Table 3.16 – Summary – Hypothesis 1c

Quadrupedal Hypotheses Hypothesis 2a - Generalized quadrupedal platyrrhines will have a pelvis characterized by a shorter ischium than found in leaping platyrrhines (Fleagle 1977; Fleagle and Meldrum

1988).

Ischium Length Prediction: Quadrupedal taxa will have a shorter ischium than leaping taxa. This hypothesis deals with total ischial length, for a discussion of dorsal and/or distal projection of the ischium see hypothesis 1a.

146

Species (specimens within the pithecid regressions) that fall above the regression line(s) will indicate a longer ischium for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively narrower ischium for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical ischium length for their associated body size (body size surrogate).

The regressions of ischium length versus body mass across the platyrrhines (Fig. 3.35) show that

Cebuella has a short ischium relative to body size, contradicting the hypothesis. The other callitrichids evidence a normal ischium length relative to body size. Species of Cebus evidence a longer ischium relative to body size, contradicting the hypothesis. Cacajao and Chiropotes evidence a slightly shorter ischium relative to body size than Pithecia, supporting the hypothesis.

Two Ateles species evidence a longer ischium relative to body size, while several of the Alouatta species show a shorter ischium relative to body size.

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1.8 1.6 1.4 1.2 1 0.8 0.6 0.4 0.2 0 -0.2 -0.4 4 5 6 7 8 9 10

Natural Log of Ischium Length in Centimeters in Length Ischium of Log Natural Natural Log of Bodymass in Grams Pithecia Chiropotes Cacajao Cebus Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

Figure 3.35 - Platyrrhine Wide - Regression of species means ischium length vs. body mass

The regressions of ischium length versus body mass in the callitrichid only sample (Fig. 3.36) show Cebuella with a slightly shorter ischium relative to body size, contradicting the hypothesis.

Mico and Callimico evidence normal ischium lengths relative to body size. Callithrix jacchus geoffroyi and Leontopithecus chrysomelas, both have a longer ischium relative to body size,

Callithrix jacchus jacchus and Leontopithecus rosalia each fall on/close to the regression line(s).

To fully support the hypothesis, the quadrupedal marmosets, tamarins and lion tamarins should all evidence shorter ischia relative to body size.

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0.7 0.6

0.5 Callimico 0.4 Saguinus 0.3 Mico 0.2 Callithrix 0.1 Centimeters Cebuella 0 Leontopithecus -0.1

Natural Log of Ischium Length in in Length Ischium of Log Natural -0.2 OLS -0.3 RMA 4 4.5 5 5.5 6 6.5 7 Natural Log of Bodymass in Grams

Figure 3.36 - Callitrichid Only - Regression of species means ischium length vs. body mass The regressions of individual pithecid specimens versus LCL (Fig. 3.37) show Pithecia with an expected ischium length relative to LCL, regardless of which analysis is employed. Chiropotes tends to cluster below the regression line(s) especially when RMA is used, indicating a shorter ischium relative to body size, supporting the hypothesis. Cacajao evidences a normal ischium length relative to LCL (falling above and below the regression line(s)).

149

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1 Pithecia 0.9 Chiropotes Cacajao

Centimeters 0.8 OLS 0.7 RMA

Natural Log of Ischium Length in in Length Ischium of Log Natural 0.6

0.5 0 0.1 0.2 0.3 0.4 0.5 0.6 Natural Log of Lateral Condyle Length

Figure 3.37- Within Pithecids - Regression of individual specimens vs. LCL

Summary Hypothesis 2a Ischial Length *Mixed results in the all-platyrrhine and callitrichid only regressions do not support the hypothesis Table 3.17 – Summary - Hypothesis 2a

Hypothesis 2b – Generalized quadrupedal platyrrhines will have a hip characterized by a longer femoral neck set at a higher angle (than leapers) (Walker 1974; Fleagle 1977;

Fleagle and Meldrum 1988), a femoral articular surface that does not extend onto the neck of the femur (Fleagle and Meldrum 1988) and a moderately sized greater trochanter that does not overhang the anterior surface of the femur (Walker 1974; Fleagle and Meldrum

1988). 150

Femoral Neck Length Prediction: Quadrupeds will have a longer femoral neck than leaping taxa.

Please see leaping hypothesis 1b for a more complete discussion of femoral neck length. Fig.

3.12 illustrates that the residuals of these regressions are quite low. However, several quadrupeds (Cebus, Cacajao and Mico) evidence slightly longer femoral neck lengths relative to body size, supporting the hypothesis. Pithecia straddles the regression line, with one species falling above and one below the line(s). In the callitrichid only regressions (Fig. 3.13), Mico stands out as having a longer femoral neck length relative to body size, supporting the hypothesis.

Femoral Neck Angle Prediction: Quadrupeds will have a higher femoral neck angle than leapers.

Please see leaping hypothesis 1b for a more complete discussion of femoral neck angle. The

ANOVA (Table 3.7) and Tukey’s pairwise comparison (Table 3.8) do not distinguish between leapers and quadrupeds in terms of femoral neck angle. Fig. 3.18 shows that in the platyrrhine wide sample, suspensory animals stand out as having an overall higher femoral neck angle, the leapers and quadrupeds are grouped rather tightly in the middle with neither a high nor low femoral neck angle, contradicting the hypothesis.

Posterior Articular Surface Prediction: Quadrupeds will have a less expansive articular surface than leaping taxa.

Please see leaping hypothesis 1b for a more complete discussion of posterior articular surface of the femur. The majority of taxa in the platyrrhine wide sample (Fig. 3.21) show a posterior articular surface that is normal relative to body mass. Few taxa stand out as having a more or less expansive articular surface relative to body mass, excepting Saimiri which has a less 151 expansive articular surface, supporting the hypothesis. A similar situation arises in the callitrichid only sample (Fig. 3.22). The majority of taxa show an articular surface that is normal relative to body mass, with the exception of Mico which has a more expansive articular surface relative to body mass, contradicting the hypothesis.

Greater Trochanter Width Prediction: Quadrupeds will have a less expansive greater trochanter than leaping taxa.

Please see leaping hypothesis 1b for a more complete discussion of greater trochanter width.

Fig. 3.24 illustrates the regression of greater trochanter width versus body mass across the platyrrhines. The majority of quadruped taxa fall on or in close proximity of the regression line(s) indicating a normal or expected greater trochanter width relative to body size, supporting the hypothesis. In the callitrichid only regressions (Fig. 3.25) One Mico and one Callithrix species have a slightly wider greater trochanter relative to body mass, contradicting the hypothesis.

Summary Hypothesis 2b Femoral Neck Length *There is a tight fit to the regression line(s) *Multiple quadrupedal taxa support the hypothesis, one species of Pithecia contradicts it

Femoral Neck Angle *The hypothesis is not supported

Posterior Articular Surface * Most taxa evidence an expected posterior articular surface for their given body size

Greater Trochanter Width *In the callitrichid only regression, a couple of species contradict the hypothesis

152

*Overall, quadrupeds cluster close to the regression line Table 3.18 – Summary - Hypothesis 2b

Hypothesis 2c – Generalized quadrupedal platyrrhines will have a knee characterized by a wider patellar groove (than in leapers) (Walker 1974, Fleagle 1977), asymmetrical femoral condyles (Fleagle and Meldrum 1988), and femoral condyles oriented distally and posteriorly (Walker 1974).

Patellar Groove Width Prediction: Quadrupeds will evidence a wider patellar groove than leaping taxa.

Please see leaping hypothesis 1c for a more complete discussion of patellar groove width. The regressions of patellar groove width versus body mass across the platyrrhines (Fig. 3.30) show that the quadrupedal platyrrhines Callicebus, Cebus and Chiropotes evidence a slightly wider patellar groove relative to body size, supporting the hypothesis. Pithecia, however, also evidences a slightly wider patellar groove, contradicting the hypothesis. One Callithrix species and one Aotus species evidence a narrower patellar groove, contradicting the hypothesis.

The callitrichid only sample (Fig. 3.31) shows that one Callithrix and Mico evidence a wider patellar groove relative to body size, supporting the hypothesis, while one Callithrix species evidences a narrower patellar groove, contradicting the hypothesis. The other callitrichid taxa evidence normal patellar groove width relative to body size.

Femoral Condyle Symmetry Prediction: Quadrupedal taxa will have more asymmetrical femoral condyles than leaping taxa. 153

Please see leaping hypothesis 1c for a more complete discussion of femoral condyle symmetry.

Figs. 3.27, 3.28 and 3.29 do not support the hypothesis that quadrupeds have necessarily more asymmetrical femoral condyles than leapers. Tukey’s pairwise comparison’s (Table 3.11) do illustrate that suspensory animals are more asymmetrical than the other groups. In the callitrichid only sample (Fig. 3.28), Callimico has relatively more symmetrical condyles than

Cebuella, with the other callitrichids falling somewhere in between. This contradicts the hypothesis according to which both leaping callitrichids should evidence symmetry of the femoral condyles.

Femoral Condyle Orientation Prediction: Quadrupedal taxa will have femoral condyles that are oriented distally and posteriorly.

Please see leaping hypothesis 1c for a more complete discussion of femoral condyle orientation.

Tables 3.14 and 3.15 illustrate that there are differences in the means of the four primate locomotor groups. Fig. 3.34 illustrates that suspensory platyrrhines and climbers are significantly different from the quadrupeds and leapers. The data is not able to distinguish differences between quadrupeds and leapers. The hypothesis is supported.

Summary Hypothesis 2c Patellar Groove Width * Mixed results in both the platyrrhine wide and callitrichid only regressions contradict the hypothesis

Femoral Condyle Symmetry *Quadrupeds do not distinguish themselves from leapers, contradicting the hypothesis

Femoral Condyle Orientation *The hypothesis is not supported 154

Table 3.19 – Summary - Hypothesis 2c

Climbing Hypotheses Hypothesis 3a – The pelvis of climbing platyrrhines will be characterized by a wider pubic ramus (Taylor 1976) and a more expanded ilium (Taylor 1976) than quadrupedal platyrrhines.

Pubic Ramus Width Prediction: Climbing taxa (Alouatta and Lagothrix) will evidence a wider pubic ramus than the more quadrupedal taxa.

Species that fall above the regression line(s) will indicate a wider pubis for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively shorter pubis for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical pubic width for their associated body size.

The regressions of pubic width versus body mass across the platyrrhines (Fig. 3.38) show that

Alouatta and Lagothrix evidence a wider pubis or normal pubic width relative to body size, supporting the hypothesis. One Callithrix and Mico evidence positive residuals, contradicting the hypothesis. The cebids tend to cluster close to the regression line(s) with Callicebus falling below the line(s) indicating a slightly narrower pubis relative to body size, supporting the hypothesis. The pithecids all evidence a narrower pubis relative to body size. This hypothesis is complicated by the fact that all platyrrhines incorporate climbing into their locomotor repertoire.

This regression indicates that the more frequent climbers tend towards a wider pubis.

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Natural Log of Pubic Width in Centimeters in Width Pubic of Log Natural 4 5 6 7 8 9 10 Natural Log of Bodymass in Grams Pithecia Chiropotes Cacajao Cebus Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

Figure 3.38 - Platyrrhine Wide - Regression of species means pubic width vs. body mass

Ilium Width Prediction: Climbing taxa will evidence a wider ilium than quadrupedal taxa.

Please see leaping hypotheses 1b for a more complete discussion of ilium width. Fig. 3.9 illustrates the regressions of ilium width versus body mass across the platyrrhines. The climbing platyrrhines, Alouatta and Lagothrix, evidence a less expansive ilium relative to body mass, contradicting the hypothesis. The suspensory atelid, Ateles, evidences a wider ilium relative to body mass, as does Cebus. The quadrupedal platyrrhines, such as Cebus, should evidence a narrower ilium to support the hypothesis. 156

Summary Hypothesis 3a Pubic Width * The climbing taxa tend to evidence a wider pubis compared to many of the other platyrrhines

Ilium Width *The hypothesis is not supported. Table 3.20 – Summary Hypothesis 3a

Hypothesis 3b – The hip of climbing platyrrhines will be characterized by a femoral head that is higher or equal to the height of the greater trochanter (Jenkins and Camazine 1977), a femoral articular surface that extends anteriorly and posteriorly to encapsulate the femoral head (Jenkins and Camazine 1977), a prominent intertrochanteric line and crest

(Grand 1968 – Attachment for muscles of the hip capsule), a deep trochanteric fossa

(Grand 1968 - Accommodating lateral rotators) and a medially placed lesser trochanter

(Taylor 1976).

Femoral Head Height Compared to Greater Trochanter Height Prediction: Climbing platyrrhines will have a femoral head that is higher or equal to the height of the greater trochanter.

Sum of df Mean F p (same) sqrs square Between groups: 10.2931 3 3.43105 8.821 .00002 Within groups: 68.845 177 0.388955 Permutation p (n=99999) Total: 79.1381 180 .00001

omega2: 0.1148 Levene´s test for homogeneity of variance, from means p (same): <.00005 157

Levene´s test, from medians p (same): .00008 Welch F test in the case of unequal variances: F=12.85, df=59.48, p= <.00005 Table 3.21 - Analysis of variance - test for equal means - head height vs. trochanter height

Tukey’s Q below the diagonal, p above the diagonal. Significant comparisons are in red. Leap Quad Climb Suspend Leap 0.0008097 0.003785 0.01905 Quad 5.393 0.9761 0.8022 Climb 4.807 0.5858 0.9612 Suspend 4.113 1.28 0.6941

Table 3.22 - Tukey's Pairwise comparison - head height vs. trochanter height

An ANOVA (Table 3.21) indicates a significant difference between means for the groups. A

Tukey’s pairwise comparison (Table 3.22) indicates that significant comparisons exist. As is illustrated in the histogram (Fig. 3.39), leapers are set apart as being significantly different from quadrupeds, climbers and suspensory animals. Leapers are more likely to have a femoral head that is equal in height to the greater trochanter. Quadrupeds, climbers and suspensory animals are more likely to have a femoral head that extends slightly above the greater trochanter, contradicting the hypothesis. With this data, it is impossible to determine what differences may exist between quadrupeds, climbers and suspensory animals, beyond what is illustrated in the histogram.

158

Least Squares Means

1 HEADTROHEI 0

-1

Climb Leap Quad Suspend GROUP$ Figure 3.39 - Least squares means histogram - femoral head height compared to greater trochanter height

Anterior Femoral Head Articular Surface Prediction: Climbers will have a more expansive articular surface than generalized quadrupeds.

Species that fall above the regression line(s) will indicate a more expansive anterior articular surface for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively less expansive anterior articular surface for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical anterior articular surface for their associated body size. 159

The regressions of anterior articular surface of the femoral head versus body mass across the platyrrhines (Fig. 3.40) shows that atelid species evidence both expanded articular surfaces and less expansive articular surface. Several Alouatta species evidence more expansive articular surfaces relative to body size, supporting the hypothesis; while other Alouatta species contradict the hypothesis. Ateles evidences more expansive articular surfaces. Pithecia has a more expansive articular surface area relative to body size. A majority of the quadrupedal taxa evidence an anterior articular surface that is expected relative to body size. Saimiri has a smaller

(less expansive) articular surface, which supports the hypothesis. Overall the hypothesis is not supported.

0.6 0.4 0.2

0 -0.2 -0.4 -0.6 -0.8 -1 -1.2 -1.4 -1.6 Femoral Head in Centimeters in Head Femoral 4 5 6 7 8 9 10 Natural Log of Bodymass in Grams

Pithecia Chiropotes Cacajao Cebus Natural Log of the Anterior Articular Surface of hte hte of Surface Articular Anterior the of Log Natural Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

160

Figure 3.40 - Platyrrhine Wide - Regression of species means ant. articular surface vs. body mass

Posterior Articular Surface of the Femoral Head Prediction: Climbing taxa will evidence a more expansive articular surface than generalized quadrupeds.

Lagothrix) cluster close to the regression line(s) indicating that they have a normal posterior articular surface relative to body size, contradicting the hypothesis which would expect a more expanded articular surface.

Presence/Robustness of Intertrochanteric Line Prediction: Climbers will have a prominent intertrochanteric line compared to quadrupeds.

Please see leaping hypotheses 1b for a more complete discussion of the robustness of the intertrochanteric line. An ANOVA (Table 3.4) was used to determine that there were significant differences between groups. Tukey’s pairwise comparison (Table 3.5) was used to determine that significant comparisons exist. As is illustrated in Fig. 3.8, suspensory animals are significantly different from leapers and quadrupeds, but not climbers. Climbers are not significantly different from leapers and quadrupeds, contradicting the hypothesis. 161

Presence/Robustness of Intertrochanteric Crest Prediction: Climbers will have a prominent intertrochanteric crest compared to quadrupeds.

Sum of sqrs df Mean square F p (same) Between 23.864 3 7.95468 17.64 <.00005 groups: Within 79.8045 177 0.450873 Permutation p groups: (n=99999) Total: 103.669 180 .00001

omega2: 0.2162 Levene´s test for homogeneity of variance, from means p (same): 0.351 Levene´s test, from medians p (same): 0.5118 Welch F test in the case of unequal variances: F=17.76, df=61.86, p= <.00005 Table 3.23 - Analysis of variance - test for equal means intertrochanteric crest

Tukey’s Q below the diagonal, p above the diagonal. Significant comparisons are in red. Leap Quad Climb Suspend Leap 0.9304 0.001908 <.00005 Quad 0.8564 0.0001666 <.00005 Climb 5.074 5.93 0.1098 Suspend 8.257 9.113 3.183 Table 3.24 - Tukey's Pairwise comparison intertrochanteric crest

An ANOVA (Table 3.23) indicates a significant difference between means for the groups. A

Tukey’s pairwise comparison (Table 3.24) indicates that significant comparisons exist. As is illustrated in the histogram (Fig. 3.41), leapers and quadrupeds are set apart as being significantly different than climbers or suspensory animals. Leapers and quadrupeds are indicated as having a less visible/less obvious intertrochanteric crest. Climbers and suspensory 162 animals are set apart as having a more visible and/or distinct intertrochanteric crest, supporting the hypothesis. With this data, it is impossible to determine what differences may exist between quadrupeds and leapers or climbers and suspensory animals beyond what is illustrated in the histogram.

Least Squares Means

2 INTERTRO

Climb Leap Quad Suspend GROUP$ Figure 3.41 - Least squares means histogram - intertrochanteric crest 163

Depth of the Trochanteric Fossa Prediction: Climbers will have a deep trochanteric fossa.

Sum of df Mean F p (same) sqrs square Between 1.49086 3 0.496953 2.657 0.04992 groups: Within 33.1058 177 0.187039 Permutation p groups: (n=99999) Total: 34.5967 180 0.05098

omega2: 0.02673 Levene´s test for homogeneity of variance, from means p (same): .00005 Levene´s test, from medians p (same): 0.2065 Welch F test in the case of unequal variances: F=6.461, df=74.36, p=0.0006022 Table 3.25 - Analysis of variance - test for equal means trochanteric fossa

Tukey’s Q below the diagonal, p above the diagonal. Significant comparisons are in red. Leap Quad Climb Suspend Leap 0.9479 0.9961 0.008379 Quad 0.771 0.9884 0.04337 Climb 0.3151 0.4559 0.01706 Suspend 4.479 3.708 4.164 Table 3.26 - Tukey's Pairwise comparison - trochanteric fossa

164

An ANOVA (Table 3.25) indicates a barely significant difference between means for the groups.

A Tukey’s pairwise comparison (Table 3.26) indicates significant comparisons exist. As is illustrated in the histogram (Fig. 3.42), suspensory animals set themselves apart as being different from quadrupeds, leapers and climbers. Suspensory animals are indicated as having a deeper trochanteric fossa than the other groups (leapers, quadrupeds and climbers). With the given data, it is impossible to determine what differences may exist between quadrupeds, leapers and climbers beyond what is illustrated in the histogram, contradicting the hypothesis.

Least Squares Means

TROFOSSA 1

Climb Leap Quad Suspend GROUP$ Figure 3.42 - Least squares means histogram - Trochanteric fossa 165

Position of the Lesser Trochanter Prediction: Climbers will have a medial/midline placed lesser trochanter.

Sum of sqrs df Mean square F p (same) Between 40.4585 3 13.4862 41.35 .0262 groups: Within 57.7294 177 0.326155 Permutation p groups: (n=99999) Total: 98.1878 180 .00001

omega2: 0.4008 Levene´s test for homogeneity of variance, from means p (same): <.00005 Levene´s test, from medians p (same): 0.0003238 Welch F test in the case of unequal variances: F=54.21, df=77.83, p= <.00005 Table 3.27 - Analysis of variance – position of the lesser trochanter - test for equal means

Tukey’s Q below the diagonal, p above the diagonal. Significant comparisons are in red. Leap Quad Climb Suspend Leap 1 <.00005 <.00005 Quad 0.05077 <.00005 <.00005 Climb 9.385 9.334 0.5185 Suspend 11.32 11.27 1.937 Table 3.28 - Tukey's Pairwise comparison - lesser trochanter

An ANOVA (Table 3.27) indicates a significant difference between means for the groups. A

Tukey’s pairwise comparison (Table 3.28) indicates that significant comparisons exist. As is illustrated in the least squares histogram (Fig. 3.43), leapers and quadrupeds are significantly set apart from climbers and suspensory animals with a more medially positioned lesser trochanter. 166

Similarly, climbers and suspensory animals are set apart from leapers and quadrupeds with a more posteriorly positioned lesser trochanter, contradicting the hypothesis. With this data, it is not possible to attribute differences between leapers and quadrupeds or climbers and suspensory animals, beyond what is indicated by the histogram.

Least Squares Means

2 LESSERTRO

Climb Leap Quad Suspend GROUP$ Figure 3.43 - Least squares means histogram - position of the lesser trochanter

Summary Hypothesis 3b Head Height compared to Greater Trochanter Height *Hypothesis is not supported

167

Anterior Articular Surface *Hypothesis is not supported

Posterior Articular Surface *Hypothesis is not supported

Intertrochanteric Line *Hypothesis is not supported

Intertrochanteric Crest *Hypothesis is supported; Climbers and brachiators have a distinct crest

Trochanteric Fossa *Hypothesis is not supported.

Position of the Lesser Trochanter *Hypothesis is not supported Table 3.29 – Summary - Hypothesis 3b

Hypothesis 3c – The knee of climbing platyrrhines will be characterized by a longer medial femoral condyle compared to quadrupedal platyrrhines (Grand 1968; Schon Ybarra and

Schon 1987).

Medial Femoral Condyle Length Prediction: Climbers will have a longer medial femoral condyle compared to quadrupedal taxa.

Species that fall above the regression line(s) will indicate a longer medial condyle for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively shorter medial condyle for the assumed body size. Species that fall on (or in 168 close proximity) to the regression line(s) will be considered to have a normal/typical medial condyle length for their associated body size.

The regressions of medial condyle length versus body mass across the platyrrhines (Fig. 3.44) show that the majority of taxa closely fall along the regression line(s) indicating an expected medial condyle length relative to body size. The climbers do not stand out as having a longer medial femoral condyle relative to body size. The hypothesis is not supported.

1.5

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-1.5 4 5 6 7 8 9 10 Natural Log of Bodymass in Grams

Pithecia Chiropotes Cacajao Cebus Natural Log of Medial Condyle Length in Centimeters in Length Condyle Medial of Log Natural Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

Figure 3.44 - Platyrrhine Wide - Regression of species means medial condyle length vs. body mass

169

Summary Hypothesis 3c

Medial Femoral Condyle Length *Hypothesis is not supported Table 3.30 – Summary - Hypothesis 3c

Suspensory Hypotheses Hypothesis 4a – The pelvis of suspensory platyrrhines will be characterized by a shorter ischium (Simons et al. 1992) and a smaller (in diameter) acetabulum (Ruff 1988) compared to quadrupedal platyrrhines.

Ischium Length Prediction: Brachiating platyrrhines will have a shorter ischium than many of the quadrupedal taxa.

Please see quadrupedal hypothesis 2a for a more complete discussion of ischium length. The regressions of ischium length versus body mass across the platyrrhines (Fig. 3.35) show that

Ateles has a longer ischium relative to body size than many of the quadrupedal platyrrhines, contradicting the hypothesis. Callicebus and Cebus also have a longer ischium relative to body size, as quadrupeds this supports the hypothesis. Alouatta, an atelid, has a shorter ischium relative to body size. Overall, the hypothesis is not supported.

Acetabulum Width Prediction: Ateles will have a smaller acetabulum than quadrupedal taxa.

Species that fall above the regression line(s) will indicate a wider acetabulum for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively narrower acetabulum for the assumed body size. Species that fall on (or in close 170 proximity) to the regression line(s) will be considered to have a normal/typical acetabular width for their associated body size.

The regressions for acetabulum width versus body mass across the platyrrhines (Fig. 3.45) show that Ateles has normal acetabulum width relative to body size. Several quadrupeds, including

Cebus, Cacajao, Saimiri and several Aotus species have a wider acetabulum relative to body size, supporting the hypothesis; however the hypothesis is contradicted by Cebus and the pithecids that fall above the line. The hypothesis is not supported. For this variable, the taxa fall predominantly along the regression line(s) with very low residuals.

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-1.5 4 5 6 7 8 9 10

Natural Log of Bodymass in Grams Natural Log of Acetabulum Width in Centimeters in Width Acetabulum of Log Natural Pithecia Chiropotes Cacajao Cebus Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

171

Figure 3.45 - Platyrrhine Wide - Regression of species means acetabulum width vs. body mass

Acetabulum Height Prediction: Ateles will have a smaller acetabulum than quadrupedal taxa.

Species that fall above the regression line(s) will indicate a higher acetabulum height for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively shorter acetabulum for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical acetabular height for their associated body size.

The regressions of acetabulum height versus body mass across the platyrrhines (Fig. 3.46) show that Ateles cluster close to the regression line(s) indicating an expected acetabulum height relative to body size. Cebus and several Aotus species have a taller acetabulum relative to body size, supporting the hypothesis; however, overall the hypothesis is not supported by Cebus and the pithecids that evidence acetabulum height that is as tall or taller than Ateles.

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Pithecia Chiropotes Cacajao Cebus

Natural Log of Acetabulum Height in Centimeters in Height Acetabulum of Log Natural Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

Figure 3.46 - Platyrrhine Wide - Regression of species means acetabulum height vs. body mass

Summary Hypothesis 4a Ischium Length *Hypothesis is not supported.

Acetabulum Width *Hypothesis is not supported

Acetabulum Height *Hypothesis is not supported Table 3.31 – Summary - Hypothesis 4a 173

Hypothesis 4b – The hip of suspensory platyrrhines will be characterized by a larger, spherical femoral head (Ruff 1988; Zihlman et al. 2011) compared to quadrupedal platyrrhines, an articular surface that covers the head, extending to the femoral neck (Ruff

1988), a femoral head height equal to or exceeding the height of the greater trochanter

(Zihlman et al 2011) and a large lesser trochanter that protrudes medially (Stern 1971 –

Hip joint excursion).

Femoral Head Height Prediction: Ateles will have a large femoral head compared to quadrupedal taxa.

Species that fall above the regression line(s) will indicate a higher femoral head height for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively shorter femoral head height for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical femoral head height for their associated body size.

The regressions of femoral head height versus body mass across the platyrrhines shows (Fig.

3.47) that the suspensory species, Ateles, has a larger femoral head height relative to body size, supporting the hypothesis; while Cacajao, several Aotus and Mico contradict the hypothesis by also evidencing a larger femoral head relative to body size. Furthermore, many quadrupedal species, including several Cebus, Chiropotes, Saimiri, and several Aotus have a smaller femoral head height relative to body size, supporting the hypothesis. The climber, Lagothrix, evidences a smaller femoral head height relative to body size, this neither supports nor contradicts the 174 hypothesis. Pithecia, a non-suspensory, leaping platyrrhine stands out, as well, having a larger femoral head height relative to body size.

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Natural Log of Bodymass in Grams Natural Log of Femoral Head Height in Centimeters in Height Head Femoral of Log Natural Pithecia Chiropotes Cacajao Cebus Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

Figure 3.47 - Platyrrhine Wide - Regression of species means femoral head height vs. body mass

Femoral Head Width Prediction: Ateles will have a large femoral head compared to quadrupedal taxa.

175

Species that fall above the regression line(s) will indicate a wider femoral head for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively narrower femoral head for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical femoral head width for their associated body size.

The regression, of femoral head width versus body mass across the platyrrhines (Fig. 3.48), shows that Ateles species have a higher femoral head width relative to body size, supporting the hypothesis. The hypothesis is also supported by the quadrupedal taxa, Cebus, Chiropotes,

Callicebus, Saimiri, and Callithrix that evidence a shorter femoral head width relative to body size. Similar to femoral head height, Lagothrix evidences a smaller femoral head width relative body size, neither supporting nor contradicting the hypothesis. Interestingly, Aotus species fall on, above and below the regression lines, indicating that Aotus species evidence variable femoral head sizes relative to body size. This is functionally interesting and not explained by the hypothesis.

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Natural Log of Femoral Head Width in Centimeters in Width Head Femoral of Log Natural Natural Log of Bodymass in Grams

Pithecia Chiropotes Cacajao Cebus Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

Figure 3.48 - Platyrrhine Wide - Regression of species means femoral head width vs. body mass

Posterior Articular Surface of the Femoral Head Prediction: Ateles will have an expansive articular surface.

Please see leaping hypothesis 1b for a more complete discussion of posterior articular surface.

The regressions of posterior articular surface of the femoral head versus body mass across the platyrrhines (Fig. 3.21) shows that the suspensory species, Ateles, have a more expansive articular surface relative to body size, supporting the hypothesis. Several other species, also 177 have a more expansive articular surface relative to body size, Pithecia, Mico, and one Callicebus.

Several quadrupedal taxa evidence a less expansive articular surface relative to body size,

Saimiri and two Aotus, supporting the hypothesis.

Anterior Articular Surface of the Femoral Head Prediction: Ateles will have an expansive articular surface.

Please see climbing hypothesis 3b for a more complete discussion of anterior articular surface of the femoral head. The regressions of anterior articular surface of the femoral head versus body mass across the platyrrhines (Fig. 3.40) shows that Ateles (supporting the hypothesis), one

Alouatta, Pithecia, and one Aotus evidence a more expansive articular surface relative to body size. Several taxa, Saimiri, two Alouatta, Lagothrix and two Cebus evidence a less expansive anterior articular surface of the femoral head, supporting the hypothesis. The articular surface expansive indicates that there is a tendency in Ateles towards a larger femoral head with an expansive articular surface.

Femoral Head Height Compared to the Height of the Greater Trochanter Prediction: Ateles is will have a femoral head that exceeds the height of the greater trochanter.

Please see climbing hypothesis 3b for a more complete discussion of femoral head height compared to the height of the greater trochanter. An ANOVA (Table 3.21) was used to determine if there were differences in the means of the four primary platyrrhine locomotor groupings. Tukey’s pairwise comparison (Table 3.22) showed that significant comparisons exist.

Suspensory animals were found to have a significant differences over leapers. Climbers and 178 quadrupeds also were found to have a significant difference over leapers. Suspensory animals, climbers and quadrupeds were more likely than leapers to have a femoral head height that exceeded the height of the greater trochanter. The hypothesis cannot be strongly supported, however, because there is not a significant difference between suspensory animals and quadrupeds.

Position of the Lesser Trochanter Prediction: Brachiating taxa will have a medially positioned lesser trochanter.

Please see climbing hypothesis 3b for a more complete discussion of the position of the lesser trochanter. An ANOVA (Table 3.27) indicates a significant difference between means for the groups. A Tukey’s pairwise comparison (Table 3.28) indicates that significant comparisons exist. As is illustrated in the least squares histogram (Fig. 3.43), leapers and quadrupeds are significantly set apart from climbers and suspensory animals with a more medially positioned lesser trochanter. Similarly, climbers and suspensory animals are set apart from leapers and quadrupeds with a more posteriorly positioned lesser trochanter, contradicting the hypothesis.

With this data, it is not possible to attribute differences between leapers and quadrupeds or climbers and suspensory animals, beyond what is indicated by the histogram.

Summary 4b Femoral Head Height *While Ateles evidences a larger femoral head, so do many other non-brachiating taxa

Femoral Head Width *While Ateles evidences a larger femoral head, so do many other non-brachiating taxa 179

Femoral Head Articular Surface *Ateles, along with other non-brachiating taxa, evidences a tendency towards a larger articular surface

Femoral Head Height Compared to Greater Trochanter *Hypothesis is not strongly supported

Position of the Lesser Trochanter *Hypothesis is not supported Table 3.32–Summary - Hypothesis 4b

Hypothesis 4c – Suspensory platyrrhines will show adaptations at the hip to increase joint excursion. These adaptations include increasing the ratio of femoral head to femoral neck size (Ruff 1988 and/ or increasing the ratio of width of the acetabulum to femoral head size

(Ruff 1988).

Species Group AceWid/HeadWid Headsize/Necksize Pmonachus Leap 1.267829957 1.193737489 Ppithecia Leap 1.145522136 1.269429288 Csatanas Quad 1.199504058 1.347630522 Crubicundus Quad 1.174735126 1.423048869 Colivaceus Quad 1.18239232 1.370603807 Ccapucinus Quad 1.175036829 1.325268052 Calbifrons Quad 1.183630285 1.223427962 Capella Quad 1.254564731 1.293360951 Ctorquatus Quad 1.107928601 1.236884803 Ccupreus Quad 1.120781528 1.142073505 Ssciureus Quad 1.156474164 1.202231598 Sboliviensis Quad 1.136816776 1.157274807 Avociferans Quad 1.149430324 1.314559617 Anigriceps Quad 1.114143095 1.320576317 Aazarae Quad 1.168575645 1.258852031 Atrivigatus(griseimembra) Quad 1.10994864 1.257647351 180

Alemurinus Quad 1.153059541 1.217929876 Cgoeldii Leap 1.052978545 1.157115356 Snigricollis Quad 1.099882326 1.123589995 Smystax Quad 1.080856716 1.135518689 Smidas Quad 1.09524502 1.131621476 Soedipus Quad 1.017685988 1.170825336 Sleucopus Quad 0.977407848 1.203995794 Simperator Quad 0.988384372 1.186813187 Slabiatus Quad 1.026713872 1.108865979 Sgeoffroyi Leap 0.998112495 1.133928571 Sfuscicollis Leap 1.019724244 1.13911779 Cargentata Quad 1.02241504 1.181693364 Cjacchusgeoffroyi Quad 1.072545341 1.108903606 Cjacchusjacchus Quad 1.073965097 1.164467005 Cpygmaea Leap 0.985572299 1.147983871 Lchrysomelas Quad 1.045146061 1.109769094 Lrosalia Quad 1.054778555 1.212539498 Acaraya Climb 1.168347352 1.381962339 Afusca Climb 1.127065303 1.47922938 Abelzebul Climb 1.142202586 1.400142653 Apalliataaequatorialis Climb 1.131401432 1.331998856 Aseniculusseniculus Climb 1.159321453 1.393252322 Afuscicepsrobustus Suspense 1.106180008 1.515816866 Ageoffroyi Suspense 1.037866224 1.427104377 Apaniscuspaniscus Suspense 1.177684798 1.313374806 Llagothricha Climb 1.140718563 1.377911647 Llugens Climb 1.152739615 1.34947121 Lcana Climb 1.177677744 1.335587644 Lpoeppiggii Climb 1.264502762 1.321045264 Table 3.33 – Ratios of femoral head size to femoral neck size and acetabular width to head size

Ratio of Femoral Head Size to Femoral Neck Size Prediction: Ateles will have increase joint excursion by increasing the ratio of femoral head size to femoral neck size.

In order to determine if suspensory animals increase joint excursion by increasing the ratio of femoral head size to femoral neck size, a ratio of the two variables was computed in 181 representatives of the four primary platyrrhine locomotor groups. An ANOVA was used to determine if significant differences existed between the means of the groups; and Tukey’s pairwise comparisons were used to determine if significant comparisons existed.

Sum of sqrs df Mean square F p (same)

Between 0.28225 3 0.0940832 15.34 <.00005 groups:

Within 0.251461 41 0.00613319 Permutation p groups: (n=99999)

Total: 0.533711 44 .00001 omega2: 0.4888 Levene´s test for homogeneity of variance, from means p (same): 0.1361 Levene´s test, from medians p (same): 0.183 Welch F test in the case of unequal variances: F=22.12, df=7.654, p=0.0003919

Table 3.34 - Analysis of variance - test for equal means ratio of femoral head size to femoral neck size

Tukey’s Q below the diagonal, p above the diagonal. Significant comparisons are in red. Leap Quad Climb Suspense Leap 0.731 0.0004398 0.0001707 Quad 1.462 0.006572 0.0004792 Climb 6.375 4.913 0.7545 Suspense 7.778 6.317 1.404 182

Table 3.35 - Tukey's Pairwise comparisons - ration of femoral head size to femoral neck size

An ANOVA (Table 3.34) determined that significant differences exist in the means of the locomotor groups. Tukey’s pairwise comparisons (Table 3.35) determined that significant comparisons exist between the groups. As is illustrated in the least squares means histogram

(Fig.3.49), brachiating and climbing animals separate themselves as having a significantly higher ratio of femoral head to femoral neck size compared to leapers and quadrupeds, supporting the hypothesis. This data does not support any differences between leapers and quadrupeds.

Least Squares Means

1 RATIO1 0

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Climb Leap Quad Suspense GROUP$ 183

Figure 3.49 - Least squares means histogram - Ratio femoral head size to femoral neck size

Ratio of Acetabulum Width to Femoral Head Size Prediction: Ateles will increase joint excursion by increasing the ratio of acetabulum width to femoral head size.

In order to determine if suspensory animals increase joint excursion by increasing the ratio of femoral head size to femoral neck size, a ration of the two variables was found in representatives of the four primary platyrrhine locomotor groups. An ANOVA was used to determine if significant differences existed between the means of the groups; and Tukey’s pairwise comparisons were used to determine if significant comparisons existed.

Sum of sqrs df Mean square F p (same) Between 0.0296853 3 0.00989508 1.954 0.136 groups: Within 0.207648 41 0.00506458 Permutation p groups: (n=99999) Total: 0.237333 44 0.1356 omega2: 0.05978 Levene´s test for homogeneity of variance, from means p (same): 0.06421 Levene´s test, from medians p (same): 0.1881 Welch F test in the case of unequal variances: F=2.73, df=7.308, p=0.1204

Table 3.36 - Analysis of variance - test for equal means ratio of acetabulum width to femoral head size

Leap Quad Climb Suspense Leap 0.8732 0.1759 0.8908 Quad 1.071 0.5525 1 Climb 2.945 1.875 0.5262 Suspense 1.011 0.06008 1.935 184

Table 3.37 - Tukey's Pairwise comparison - ratio of acetabulum width to femoral head size

An ANOVA (Table 3.36) determined that no significant differences exist in the means of the locomotor groups. Tukey’s pairwise comparisons (Table 3.37) determined that no significant comparisons exist between the groups. As is illustrated in the least squares means histogram

(Fig.3.50), suspensory animals do not separate themselves as having a significantly higher ratio of acetabular width to femoral head size compared to climbers, contradicting the hypothesis.

Suspensory animals are not significantly different from leapers, quadrupeds or brachiators.

Least Squares Means

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Figure 3.50 - Least squares means histogram - Ratio of acetabulum width to femoral head size

Summary Hypothesis 4c Ratio Femoral Head Size to Femoral Neck Size *Hypothesis is supported, Ateles has a higher ratio than quadrupedal taxa

Ratio Acetabulum Width to Femoral Head Size *Hypothesis is not supported Table 3.38 – Summary Hypothesis 4c

Hypothesis 4d – The knee of suspensory platyrrhines will be characterized by femoral condyles that are antero-posteriorly compressed and narrowly separated (Tardieu 1981) and a wider patellar groove with lower/less robust medial and lateral lips compared

(Tardieu 1981) to quadrupedal platyrrhines.

Medial Condyle Length Prediction: Ateles will have femoral condyles that are antero-posteriorly compressed (short) relative to quadrupedal taxa.

Please see climbing hypothesis 3c for a more complete discussion of medial condyle length. The regressions of medial condyle length versus body mass across the platyrrhines shows (Fig. 3.44) show that two of the three Ateles species evidence a longer medial condyle relative to body mass, contradicting the hypothesis. Two Cebus species also have a longer medial condyle relative to body mass. Lagothrix and Callithrix evidence a shorter medial condyle relative to body mass, neither supporting nor contradicting the hypothesis. 186

Lateral Condyle Length Prediction: Ateles will have femoral condyles that are antero-posteriorly compressed (short) relative to quadrupedal taxa.

Species that fall above the regression line(s) will indicate a longer lateral condyle for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively shorter lateral condyle for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical lateral condyle length for their associated body weight.

The regressions of lateral condyle length versus body mass across the platyrrhines (Fig. 3.51) show that two of the three Ateles species evidence a longer lateral condyle relative to body size, contradicting the hypothesis. Cebus olivaceus, Cebus albifrons and Leontopithecus chrysomelas, also, evidence a longer lateral condyle relative to body size. Lagothrix and Chiropotes evidence a shorter lateral condyle relative to body size, neither supporting nor contradicting the hypothesis.

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Natural Log of Bodymass in Grams Natural Log of Lateral Condyle Length in Centimeters in Length Condyle Lateral of Log Natural Pithecia Chiropotes Cacajao Cebus Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

Figure 3.51 - Platyrrhine Wide - Regression of species means lateral condyle length vs. body mass

Intercondylar Width Prediction: Ateles will have condyles that are narrowly separated (narrow intercondylar space).

Species that fall above the regression line(s) will indicate a wider intercondylar space for the assumed body size; whereas species that locate below the regression line(s) will be considered to have a relatively narrower intercondylar space for the assumed body size. Species that fall on (or in close proximity) to the regression line(s) will be considered to have a normal/typical intercondylar space width for their associated body size.

188

The regressions of intercondylar width versus body mass across the platyrrhines (Fig. 3.52) show that two of the Ateles species have a slightly wider intercondylar width relative to body size, contradicting the hypothesis. Cebus, Pithecia, and some Saguinus have a wider intercondylar width relative to body size, while Chiropotes, three of the five Alouatta species, and Callithrix jacchus geoffroyi have a narrow intercondylar width relative to body size. To support the hypothesis Ateles should have a narrower intercondylar width compared to the more quadrupedal species.

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Natural Log of Bodymass in Grams Natural Log of Intercondylar Width in Centimeters in Width Intercondylar of Log Natural Pithecia Chiropotes Cacajao Cebus Callicebus Saimiri Aotus Callimico Mico Callithrix Cebuella Leontopithecus Alouatta Ateles Lagothrix Saguinus OLS RMA

Figure 3.52 - Platyrrhine Wide - Regression of species means intercondylar space vs. body mass 189

Patellar Groove Width Prediction: Ateles will have a wider patellar groove relative to generalized quadrupeds.

Pithecia, Callicebus, Cebus and Chiropotes also evidence a wider patellar groove relative to body size contradicting the hypothesis. Saimiri, Lagothrix and three of the five Alouatta species evidence a narrower patellar groove relative to body size, also, supporting the hypothesis. If one was to just look at the larger bodied species within the regression, Ateles would likely have support for the hypothesis. However, platyrrhine wide, the hypothesis is not supported.

Medial Margin of the Patellar Groove Prediction: Ateles will have less robust condylar margins.

Sum of df Mean F p (same) sqrs square Between 16.4605 3 5.48682 17.57 <.00005 groups: Within 55.2743 177 0.312284 Permutation groups: p (n=99999) Total: 71.7348 180 1 .00001

omega2: 0.2155 Levene´s test for homogeneity of variance, from means p (same): 0.1104 Levene´s test, from medians p (same): 0.3933 Welch F test in the case of unequal variances: F=16.6, df=63.83, p= <.00005 Table 3.39 - Analysis of variance - test for equal means medial condyle lip

190

Tukey’s Q below the diagonal, p above the diagonal. Significant comparisons are in red. Leap Quad Climb Suspend Leap 0.9793 .00003 0.06125 Quad 0.557 .00001 0.02043 Climb 6.527 7.084 0.1455 Suspend 3.523 4.08 3.004 Table 3.40 - Tukey's Pairwise comparison

An ANOVA (Table 3.39) indicates a significant difference between means for the groups. A

Tukey’s pairwise comparison (Table 3.40) indicates that significant comparisons exist. As indicated in the histogram (Fig. 3.53) climbers set themselves apart as being different from leapers and quadrupeds, but not suspensory animals. Suspensory animals set themselves apart from quadrupeds as having a sharper/more distinct medial patellar facet. In generally, leapers and quadrupeds have a less sharp/distinct medial patellar facet, while climbers and suspensory animals have a sharper/more distinct facet, contradicting the hypothesis. With the given data, little can be said about any differences in the medial facet between leapers and quadrupeds.

191

Least Squares Means

MEDIALLIP 1

Climb Leap Quad Suspend GROUP$ Figure 3.53 - Least squares means histogram - Medial lip of the patellar groove

Lateral Margin of the Patellar Groove Prediction: Ateles will have less robust condylar margins.

Please see leaping hypothesis 1c for a more complete discussion of the lateral margin of the patellar groove. An ANOVA (Table. 3.12) indicates that there is a not a significant difference between means for the groups. In essence, for the purposes of this study, the means for the groups are equal. A Tukey’s pairwise comparison (Table. 3.13) cannot be used, as the p values 192 are not significant. As can be seen by the histogram (Fig. 3.33), the four groupings do not separate themselves from each other in a way that can be useful to this study.

Summary Hypothesis 4d Medial Condyle Length *Hypothesis is not supported

Lateral Condyle Length *Hypothesis is not supported

Patellar Groove Length *Hypothesis is not supported

Intercondylar Width *Hypothesis is not supported

Lateral Margin of the Patellar Groove *Hypothesis is not supported

Medial Margin of the Patellar Groove *Hypothesis is not supported. Ateles has sharper margin than quadrupeds. Table 3.41 – Summary - Hypothesis 4d 193

Chapter 4

Discussion Introduction There is little debate that platyrrhine monkeys demonstrate a wide variety of locomotor behaviors. Climbing, quadrupedal walking and running, leaping, vertical clinging and leaping, forelimb and hindlimb suspensory movements and various combination of these may be evidenced by the New World monkeys. It is more difficult to ascribe a 100% link between a specific category of locomotor behavior with an underlying anatomy. Researchers have tried to find specific links between platyrrhine movements and morphology (e.g., Fleagle and Anapol

1992; Fleagle and Meldrum 1988; Ford 1980; Ford 1990; Davis 2002, while other researchers have looked for locomotor and morphology links in other radiations of primates (see Chapter 1).

With this in mind, this study was designed to see what, if any, morphological and behavioral correlates of positional behavior can be found in the lower limb of platyrrhines. All of this work has met with varying amounts of success.

Chapter 4 reviews the initial hypotheses and discusses what hindlimb traits stand out in each locomotor category and what traits are do not vary across multiple locomotor categories.

Furthermore, this chapter discusses other factors that may influence the ability to uncover the behavior/morphology links. Lastly, I will contemplate future work that may go forward from this project as well as a discussion of what data could enhance this type of work in the future.

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Summary of the Hypotheses Leaping The four hypotheses outlined in Chapter 1 with their results presented in Chapter 3 are discussed below. These hypotheses are presented by primary locomotor behavior. The first set of hypotheses investigate specific features of the hip, thigh and knee to determine if they correlate with the locomotor behavior leaping especially as contrasted with quadrupedalism.

Hypothesis 1a. The hip of leaping platyrrhines is hypothesized to evidence a longer ischium

(dorsal and/or distal depending on the angle of leap takeoff) compared to quadrupedal platyrrhines. Fleagle and Anapol (1992) found that vertical clinging and leaping prosimians exhibited a longer dorsal projection of the ischium and showed that a longer distal projection of the ischium was related to a quadrupedal leaping takeoff (leaping from a pronograde position).

They suggested that the same trend could be evidenced by a small sample of platyrrhines. My study is based on an expanded sample of platyrrhine taxa. A summary of the finding follows.

Platyrrhine-wide (callitrichid and pithecid leapers) do not all conform to the hypothesis. The callitrichid leapers do not evidence a longer dorsal projection compared to primarily quadrupedal callitrichids. Within the pithecids, this hypothesis is confirmed. The leaping pithecids, Pithecia monachus and Pithecia pithecia, evidence high positive residuals, while the quadrupedal pithecids (Cacajao and Chiropotes) show negative residuals (Fig. 3.1). Interestingly, Pithecia pithecia, which has been described as VCL, has less strongly positive residuals compared to

Pithecia monachus (behavior as yet unstudied).

Among callitrichids, however, there does not seem to be a strong relationship between dorsal projection and locomotor mode., Callimico, described as VCL, has modestly positive residuals, 195 but is not greatly different from the other callitrichids, some of which have been described as more pronograde (e.g., Leontopithecus rosalia, (Rosenberger and Stafford, 1994; Stafford et al.,

1994). On the other hand, Cebuella, which also adopts VCL behavior (although not as often as previously thought (Garber et al. 2012; Youlatos 1999b, 2009), has unexpectedly strong negative residuals on all regression lines. Callithrix jacchus geoffroyi (with no behavioral data to suggest it is a prominent leaper, let alone a VCL; Stevenson and Poole, 1976) unexpectedly has the highest positive residuals among callitrichids (and among platyrrhines).

Interestingly, outside of the leaping/quadrupedal comparisons other platyrrhine species that have not been described as VCL have positive residuals. For example, species of Ateles have very high residual values compared to Alouatta. Although these species, A. geoffroyi and A. paniscus, have been noted to leap (Mittermeier and Fleagle 1976; Fleagle and Mittermeier 1980; Cant

1986 (1%), Fontaine 1990 (13.22 %) they have never been described as VCLs. Saimiri also evidences low residuals compared to Cebus or Aotus, when behavioral descriptions suggest that these species should be more similar in leaping behavior. This indicates that there is more input into dorsal projection than just leaping posture or frequency. These results hold if the regressions are re-run without atelids or without Cebuella.

The distal projection of the ischium is less variable amongst the platyrrhine taxa examined here.

Illustrated in Fig. 3.4, the taxa that stand out are species of Alouatta and Cebuella, both of which have low residuals although Ateles paniscus has a longer than predicted distal projection. This may indicate a general propensity for pronograde quadrupedalism and leaping from pronograde postures in platyrrhines. Alouatta rarely leaps, and this may be reflected in the apparently shorter ischium, both dorsally and distally. Although Pithecia species as expected have a slightly 196 smaller distal projection than Cacajao (but not Chiropotes), Cebuella is the only VCL taxon that stands out as having a shorter distal projection relative to the other callitrichids. Again, these comparisons hold if the regressions are re-run without atelids or without Cebuella.

Hypothesis 1b. Comparing Pithecia and Chiropotes, Fleagle and Meldrum (1988) found several anatomical correlates to leaping vs. quadrupedalism. The thigh of leaping platyrrhines should show a prominent intertrochanteric line. An expanded ilium compared to quadrupedal platyrrhines was hypothesized by Walker (1974) within the prosimians. Taylor (1976), working within the Viverridae, hypothesized a short, thick femoral neck compared to quadrupedal taxa.

Walker (1974) hypothesized a femoral articular surface that extends onto the superoposterior side of the femoral neck as a leaping character as well as a broad greater trochanter (Fleagle and

Meldrum 1988). Frequent leaping platyrrhines, however, do not show a strong intertrochanteric line, in fact, both climbers and suspensory animals have a more prominent intertrochanteric line.

Leapers do not separate themselves from quadrupeds in terms of the intertrochanteric line.

Fleagle and Meldrum (1988) found a difference in the robustness of the intertrochanteric line between Pithecia and Chiropotes; an ANOVA (p value = .807) of these two species, however, was not significant in this current study with respect to the robustness of the intertrochanteric line. Please see subsequent section about muscle rugosity and osteological markings for more discussion.

Pithecia does show evidence of an expanded ilium, however, its positive residuals are similar to those of Cacajao and Chiropotes, more quadrupedal taxa. Likewise, within the callitrichids, leapers do not stand out as having a significantly more expanded ilium than do the quadrupedal 197 callitrichids. Once again, however, Ateles has positive residuals and Alouatta evidences negative residuals, which is not predicted by the hypothesis.

Leapers should show a short and thick femoral neck anatomy according to this hypothesis.

Pithecia and the leaping callitrichids do not show any evidence of a shorter femoral neck relative to the quadrupedal species, however, Pithecia does show a thicker femoral neck relative to its body mass than either of its close relatives, Cacajao or Chiropotes. However, femoral neck thickness is not discriminatory within the callitrichids. The callitrichid leapers do not demonstrate a thicker femoral neck anatomy compared to the quadrupedal species. In fact, several quadrupedal taxa such as Leontopithecus and Callithrix present the highest positive residuals within the Callitrichidae.

In terms of the articular surface expansion and breadth of the greater trochanter, the theme is consistent. Pithecia has a more expansive articular surface and a wider greater trochanter than its quadrupedal sister taxa. However, for the callitrichids, the more frequent leaping taxa do not stand out as having a more expansive articular surface or a wider greater trochanter. Thus, this hypothesis is only partially supported, with regards to the pithecids, and not supported at all within the callitrichids.

Hypothesis 1c. The knee of leaping platyrrhines should evidence symmetrical condyles (Fleagle and Meldrum 1988), a narrow patellar groove (Walker 1974) with a prominent lateral lip

(Fleagle and Meldrum 1988) and distally oriented condyles (Walker 1974). Leapers and quadrupeds do not distinguish themselves from each other in terms of condyle symmetry, 198 however, they do distinguish themselves from climbers and suspensory animals. Specifically, the atelids have the most asymmetrical condyles relative to the other groups.

Pithecia stands out with the highest positive residuals of patellar grove width; this means that this taxon has the widest patellar groove relative to its body size, and this anatomical condition contradicts Hypothesis 1c. Callitrichid leapers do not support the hypothesis either. Leapers do not stand out against the other movement groups as having a more prominent lateral lip. The leaping and more quadrupedal platyrrhines do set themselves apart from the climbers and suspensory monkeys in terms of condyle orientation. The leapers and quadrupeds show more distally or posteriorly oriented condyles, while the climbers and suspensory monkeys are more distally and posteriorly oriented. Hypothesis 1c is not supported across platyrrhines and leaping platyrrhines do not set themselves apart.

Climbing Hypothesis H3a. The pelvis of more climbing oriented platyrrhines should show a wide pubic ramus (Taylor 1976) and an expanded ilium (Taylor 1976). The climbing platyrrhines, Alouatta and Lagothrix, do tend to have a wider pubic ramus relative to body size relative to the more quadrupedal platyrrhine taxa. Pithecia demonstrates the narrowest pubis, indicating a non- climbing orientation of the pelvis. In contrast, Alouatta and Lagothrix have a narrow and less expanded ilium than do the other platyrrhine taxa. In fact, Alouatta has the highest negative residuals of all platyrrhines examined. The hypothesis is supported by the wider pubic ramus of

Alouatta and Lagothrix but is contradicted by the less expanded ilium. A wide pubic ramus is not unexpected as the origin for adductors of the thigh. 199

Hypothesis 3b - The hip of climbing platyrrhines should be characterized by a femoral head that is higher or equal to the height of the greater trochanter (Jenkins and Camazine 1977 – Jenkins and Camazine compared three groups of carnivores and made hypotheses about the functional morphology of the hindlimb), a femoral articular surface that extends anteriorly and posteriorly to encapsulate the femoral head (Jenkins and Camazine 1977), a prominent intertrochanteric line and crest (Grand 1968 – Alouatta – Grand examined the gross anatomy of Alouatta), a deep trochanteric fossa (Grand 1968 – accommodating the hip lateral rotators) and a medially placed lesser trochanter (Taylor 1976). The femoral head of climbing platyrrhines is, in fact, slightly higher than the greater trochanter. Climbers do not in fact distinguish themselves from quadrupeds or suspensory monkeys. This feature is hypothesized in carnivores to be linked to adducted posture during climbing. Within platyrrhines, this is likely a more generalized morphology. Climbers are not distinguished from the more quadrupedally oriented platyrrhines in terms of articular surface (anterior or posterior). Few taxa stand out as having a more or less expanded articular surface. Further, climbers do not stand out from the other groups as having a more prominent intertrochanteric line. Climbers do distinguish themselves from leapers and quadrupeds in terms of the robustness of the intertrochanteric crest however, partially supporting this hypothesis. Climbers are not set apart from quadrupeds or leaping platyrrhines in terms of the depth of the trochanteric fossa; but with regards to the position of the lesser trochanter, climbers and suspensory monkeys have a more posteriorly placed lesser trochanter than do leapers or quadrupeds. On the whole, the Hypothesis 3b is not supported by the given data.

Hypothesis 3c - Climbing platyrrhines should demonstrate a longer medial femoral condyle compared to quadrupedal platyrrhines (Grand 1968; Schon Ybarra and Schon 1987 – Schon 200

Ybarra and Schon examined Alouatta seniculus and commented on the relatively longer medial condyle of the femur and hypothesized its relationship to the howler monkey’s climbing behavior). The locomotor groups examined here do not demonstrate any discrimination based on medial condyle length. Hypothesis 3c is not supported. Overall, this dataset does not provide support for the three climbing hypotheses.

Suspensory Behavior Hypothesis 4a - The pelvis of suspensory platyrrhines should be characterized by a shorter ischium (short lever arm for the hamstrings – potentially linked to hindlimb suspensory behavior in the giant sloth lemur Babakotia (Simons et al. (1992)) and a narrower acetabulum (Ruff 1988

– Hominodea – Ruff examined the articular joint surfaces within the great apes and hypothesized about ways to increase joint excursion at the hip). The atelids do not provide anatomical evidence for a shorter ischium, actually, they show a longer ischium relative to the climbing atelids and many of the quadrupedal platyrrhines. Ateles does not show any evidence for a narrower acetabulum compared to the representatives of the other locomotor groups. Hypothesis

4a is not supported by either anatomical feature.

Hypothesis 4b - The hip of suspensory platyrrhines is characterized by a larger femoral head

(Ruff 1988; Zihlman et al. 2011 – Gorilla vs. Pongo – Zihlman et al. examined the gross anatomy of gorillas vs. orangutans. They made several comments about the underlying skeletal anatomy), an articular surface that covers the head (Ruff 1988), a femoral head height equal to or exceeding the height of the greater trochanter (Zihlman et al. 2011) and a large lesser trochanter that protrudes medially (Stern 1971 – Stern evaluated Cebus to determine implications 201 for bipedality). As expected, Ateles does show a larger femoral head height and femoral head width relative to its body size. Pithecia and several of the callitrichids, however, also show evidence of a larger femoral head. Ateles further shows an expanded anterior articular surface as the acetabulum as do several other species (in Pithecia and for several quadrupeds as well).

Ateles has a slightly increased posterior articular surface as do other platyrrhine species. These results partially support Hypothesis 4b, though not conclusively. Climbers, suspensory monkeys, and quadrupeds were all more likely than leapers to have a femoral head height that exceeds the height of the greater trochanter. Suspensory monkeys do not separate themselves from quadrupeds, and neither observation can confirm nor support this hypothesis. The suspensory monkeys do not have a more medially placed lesser trochanter, a condition that contradicts this hypothesis.

Hypothesis 4c - Suspensory platyrrhines should show adaptions to increase joint excursion at the hip. Suspensory animals do show evidence of increased joint excursion by increasing the ratio of femoral head size to femoral neck size (Ruff 1988). Suspensory animals are significantly set apart from climbers, quadrupeds and leapers, supporting the hypothesis. The data does not support any differences between leapers, quadrupeds and suspensory animals with regards to the ratio of acetabulum width to femoral head size. Suspensory animals do show a significant difference when compared to climbers. The hypothesis is partially supported by the ratio of femoral head size to femoral neck size.

Hypothesis 4d - The knee of suspensory platyrrhines should have short (antero-posteriorly compressed) femoral condyles (Tardieu 1981 – examination of the primate knee with emphasis on differences between the great apes – including inferences for hominid evolution) that are 202 narrowly separated, a wide patellar groove and less robust medial and lateral patellar margins

(Tardieu 1981). Femoral condyle length (lateral and medial) is closely associated with body size. That being said, Ateles does show longer medial and lateral condyles, contradicting the above hypothesis, while the majority of platyrrhine species fall close to the regression lines.

Furthermore, intercondylar width does not support this hypothesis either. Ateles has a slightly wider intercondylar width relative to its body size. Pithecia and many other species demonstrate even wider intercondylar spaces. However, several species of Saguinus, Chiropotes and

Alouatta show narrower intercondylar spaces. Hypothesis 4c is supported by Ateles as it possesses a relatively wide patellar groove compared to taxa such as Saimiri, Lagothrix and

Alouatta. The hypothesis is also supported by Ateles with its less robust medial femoral condyle relative to that of quadrupedal platyrrhines. Unfortunately, the lateral condyle lip robusticity is not significant across taxa. The overall Hypothesis 4 is only partially supported by patellar groove width and medial condyle lip gracility.

Quadrupeds Hypothesis 2a - Generalized quadrupedal platyrrhines should have a pelvis characterized by a shorter ischium than found in leaping platyrrhines (Fleagle 1977 – Fleagle undertook a comprehensive skeletal anatomy study of two Presbytis species (since then, these species have been classified in separate genera); Fleagle and Meldrum 1988). This hypothesis is not supported by the data. Cebus evidences a longer ischium than any other species. Alouatta has a shorter ischium relative to body size but is not generally regarded as a generalized quadruped. 203

Hypothesis 2b - Generalized quadrupedal platyrrhines should have a hip characterized by a longer femoral neck set at a higher angle (than leapers) (Walker 1974; Fleagle 1977; Fleagle and

Meldrum 1988), a less expanded femoral articular surface (Fleagle and Meldrum 1988) and a moderately sized greater trochanter (Walker 1974; Fleagle and Meldrum 1988). Cebus, Mico, several Saguinus species and Leontopithecus stand out as having a longer femoral neck than many of the climbing and leaping taxa, supporting the hypothesis. The quadrupeds do not stand out as having a higher femoral neck angle than leapers, contradicting the hypothesis. Suspensory animals and climbers evidence the highest femoral neck angles. Few taxa stand out as having a significantly more or less expansive articular surface, excepting Saimiri which evidences a less expansive articular surface, supporting the hypothesis. The greater trochanter width does not stand out as discriminating between the locomotor groups. Overall, the hypothesis is only partially supported by the given data.

Hypothesis 2c - Generalized quadrupedal platyrrhines should have a knee characterized by a wider patellar groove (than in leapers) (Walker 1974; Fleagle 1977), asymmetrical femoral condyles (Fleagle and Meldrum 1988) and femoral condyles oriented distally and posteriorly

(Walker 1974). Cebus, Cacajao and Chiropotes evidence a wider patellar groove relative to body size, however, Pithecia evidences an even wider patellar groove, contradicting the hypothesis. Quadrupeds have femoral condyles equal in symmetry to the leapers, contradicting the hypothesis. The suspensory animals have the most asymmetrical femoral condyles. The hypothesis is also not supported by femoral condyle orientation. Leapers and quadrupeds are distinguished from one another, whereas suspensory animals are more likely to be oriented distally and posteriorly. Overall, the hypothesis is not supported by the given data. 204

Platyrrhine Wide Callitrichid Pithecid Leaping Hypothesis 1a (dorsal ischium) mixed no yes (distal ischium) mixed no yes/partially

Hypothesis 1b (expanded ilium) mixed no yes/partially (neck thickness) mixed no yes/partially (Posterior. Articular surface) mixed no yes/partially (Greater Trochanter Width) mixed no yes/partially (intertrochanteric line) No No No (neck length) No No no

Hypothesis 1c (condyle symmetry) Partially No No (patellar groove width) No No No (lateral lip) No No No (Distally oriented condyles) Partially No No

Quadrupedal 2a (ischium length) No No No

Hypothesis 2b (neck length) yes yes/partially no (Posterior Articular surface) mixed no no (Greater Trochanter width) Mixed No Partially

Hypothesis 2c (patellar groove width) Mixed No (asymmetrical condyles) No No (condyle orientation) No no

Climbing Hypothesis 3a (pubic width) yes (ilium expansion) No

205

Hypothesis 3b (intertrochanteric crest) yes (intertrochanteric line) No (lesser trochanter) No (trochanteric fossa) No (femoral head articular surface) No (head/gr. Trochanter height) No

Hypothesis 3c (medial femoral condyle length) No

Hindlimb Suspension Hypothesis 4a (ischial length) No (acetabulum width) No

Hypothesis 4b (head width) yes (head height) yes (post. Articular surface) mixed (lesser trochanter) No (head/gr. Trochanter height) No

Hypothesis 4c (ratio head size to neck size) yes (ratio head size to acetabular width) no

Hypothesis 4d (patellar groove width) yes (medial condyle lip) yes (femoral condyle length) no Table 4.1 - Summary of level of support for the hypotheses

206

On the whole, the hypotheses have only limited support based on this data. Table 4.1 summarizes the hypotheses and the level of support for each. Pithecid leapers are different from their quadrupedal sister taxa (Chiropotes and Cacajao) as they show longer dorsal and/or distal projections of the ischium. Pithecid leapers also have an expanded ilium, a thicker femoral neck, an expansive posterior articular surface of the femoral head and a wide greater trochanter. In contrast, the callitrichid leapers are not distinguished from their more quadrupedal relatives in any way and across platyrrhines as a whole as the frequently leaping callithrichid species do not stand out uniquely in these regression analyses. I concur with Youlatos (2009) that as yet there are very few clear relationships between morphology and positional behavior in callitrichids.

Platyrrhine climbers (Lagothrix and Alouatta) show that a wide pubis and a pronounced intertrochanteric crest separates them from more quadrupedal platyrrhine taxa. Platyrrhines that employ hindlimb suspensory behavior evidence a larger femoral head, a possible expanded posterior articular surface, a wide patellar groove and a prominent medial condyle lip, separating them from more quadrupedal platyrrhines. The suspensory taxa also have increased the ratio of femoral head to femoral neck size in order to increase joint excursion at the hip.

It does appear overall, that the anatomical correlates of leaping, climbing and hindlimb suspensory behavior within the platyrrhines is not nearly as distinct as in other groups of primates. Prosimians (lemurs, galagos and tarsiers) have more exaggerated anatomical adaptations for leaping, but they also show more acrobatic and frequent leaping behaviors. The tarsiers and galagos leap more and probably differently from any of the platyrrhines and this is likely captured by the rather generalized leaping morphology in platyrrhines as evidenced by this study. This is also likely true of the brachiating apes (hylobatids and Pongidae) animals. The 207 hypotheses that relied on suggestions from the pongids and hylobatids only translate partially to the atelids. The catarrhine brachiators likely are not employing the same exact behavior as the atelids, hence the debate over the terminology brachiation vs. semi-brachiation (see discussion in this chapter). The atelids clearly have a few features that separate their unique anatomy and behavior from the quadrupedal platyrrhines, but it is not as pronounced as the differences between the hylobatid/pongid brachiators and the terrestrial/arboreal quadruped catarrhines.

Moreover, there may be selection within the platyrrhine radiation for a more generalized anatomical form. No platyrrhine stands out as having a truly unique morphology, within the construct of the four primary locomotor modes. As an example, the callitrichids show species that leap, climb, locomote quadrupedally, and even suspend (sometimes bipedally). It can be generally stated that the callitrichids do show a combination of a generalized arboreal morphology and behavior. The same can be said for cebids, some of which use a prehensile tails adapted for arboreal use. The platyrrhine morphology may be such that it is generalized in such a way as to provide the ability to adapt to any of the platyrrhine locomotor modes.

Taxa that ‘Stand Out’ It is important to identify taxa that support any of the before mentioned hypotheses as well as noting platyrrhine taxa that do not fit the predictions noted above. Chapter 3 and the preceding section of Chapter 4 outline these noteworthy taxa.

As has been discussed previously, the hypothesis proposed by Fleagle and Anapol (1992) is generally confirmed within the pithecids. The leaping taxa, Pithecia species, have a longer 208 dorsal projection of the ischium, while the quadrupedal taxa, Cacajao and Chiropotes, have a shorter dorsal projection. The distal projection is not as illustrative of the proposed hypotheses, nor is the hypothesis confirmed in the callitrichids. However, it is interesting to note where the atelid species fall (in reference to the regression lines) in terms of dorsal and distal projection of the ischium. Ateles evidences a longer dorsal projection of the ischium (all three species lie above the regression line(s)), Alouatta evidences a shorter dorsal projection of the ischium (all five species lie below the regression line(s)), and Lagothrix straddles both sides of the regression line(s) indicating an expected dorsal projection length. This could be potentially explained by the atelids leaping potentiality; Alouatta rarely leaps, Ateles has been documented to leap

(Mittermeier and Fleagle 1976; Fontaine 1990) and Lagothrix is not a renowned leaper.

However, it seems unlikely that the signal of dorsal projection would be captured best in the

Atelidae, as they do not employ leaping to nearly the extent of many of the other platyrrhines

(e.g., Pithecia, Callimico and/or Cebuella). The same pattern is seen with the regressions of distal projection versus body mass. Ateles evidences a longer distal projection, while Alouatta evidences a shorter distal projection. A longer distal projection would be expected in taxa where leaping from a pronograde/horizontal position was common. Unfortunately, there is not a lot of information about leaping takeoff position in Ateles, but again, it seems unlikely that this signal would be expressed better in the atelids than in the callitrichids where the behavioral data is more conclusive. Thus, the data begs the question of whether hindlimb suspensory activity is signaled by dorsal (and/or distal) projection of the ischium. Perhaps the kinematics of leaping in Ateles versus climbing in Alouatta could explain some of the differences in the data. As an attachment point for the hamstrings, it seems plausible that some aspect of locomotor behavior is influencing 209 the underlying ischial anatomy. This is potentially an area where gross dissection of atelid specimens could indicate muscular differences thereby adding some clarity to the data.

The hindlimb suspensory taxa, in this study, encompass three species of Ateles. There is little doubt that Ateles employs significant forelimb suspensory behavior (Fontaine 1990; Cant 1986;

Mittermeier 1978; Mittermeier and Fleagle 1976; Youlatos 2002 and 2008; Fleagle and

Mittermeier 1980), however, it may seem counterintuitive to look for morphological correlates to forelimb suspensory activity in the hindlimb. This is explained by the studies (Cant 1986;

Youlatos 1998 and 2008) that show Ateles using the hindlimb (suspension) and tail (in combination) as a positional behavior. Furthermore, it has been hypothesized that tail assisted hindlimb suspension (Meldrum 1998 and Jones 2008) is the evolutionary link between quadrupedalism and brachiation in the atelines. This could partially explain the increased hip joint excursion that was illustrated in this study and hypothesized to be a feature of Pongidae.

(Youlatos 2008; Rosenberger et al. 2008; Ruff 1988 (Pongidae)). Additionally, increased range of motion was shown in living specimens of Pongo and Ateles (Hammond 2014), suggesting these species have adapted themselves to a unique arboreal habitat. It should also be mentioned that both the climbers and suspensory animals in this study are the largest bodied species of platyrrhines (excepting Brachyteles). This has been explained in part as a result of body stability; a large animal is more stable below a branch than above the same sized branch (Fleagle and Mittermeier 1980; Cartmill 1985; Sarmiento 1995; Almecija et al., 2007; Ward 2007); not to discount the understanding that as the body increases in size, so does the reach of the animal below the branch (Grand 1972). Additionally, many researchers (Napier and Walker 1967;

Grand 1972 and 1984; Fleagle 1976; Godfrey 1988; Jungers et al. 1991; Larson 1998; (across the 210 mammalian groups) have speculated that brachiation/forelimb suspensory activity evolved as a result of pressure to feed on terminal branches.

Cebuella is enigmatic in many ways. As the smallest anthropoid, it is well studied with multiple wild behavioral, postural, and locomotor studies (see Chapter 1 for citations of behavioral data).

Interestingly, Cebuella often stands out in the data of this study. In the platyrrhine-wide regressions Cebuella falls below the regression line(s) in all but three. In only one regression, pubic width, does Cebuella evidence larger/longer feature relative to body weight. With regards to posterior articular surface and greater trochanter width Cebuella straddles the regression line indicating a normal feature length/width. Ford and Davis (2009) also found that Cebuella has a shorter than expected hindlimb, with most measurements being less than expected from its size

(using ratios). It is always possible that Cebuella is totally unique anatomically, in fact, Cebuella does not exhibit the expected leaping features and often deviates in the opposite direction. In my analyses of Cebuella, it falls on the regression line(s) in most of the callitrichid only regressions, indicating that the callitrichid only regressions are probably strongly influenced by body size. Furthermore, in the platyrrhine wide regressions, Cebuella will statistically ‘draw’ the line to it. Because it is so small and there are no similiarly sized species with varying locomotor behavior, the functional and morphological interpretation of the results for Cebuella is made difficult. As will be discussed further, it is possible that the Cebuella morphological data in this study is hampered in part by using captive specimens. There are few if any available wild- caught post-cranial remains for this taxon. While captive specimens are not ideal, they are all that is available and Ford and Davis (2009) for the most part used the same specimens.

Theoretically, it is possible that captive specimens do not yield the same level of evidence for the 211 leaping signals that have been hypothesized. This could occur as captive animals do not have the same environmental context and input that their wild counterparts do. Additionally, it is possible that the body weight data for Cebuella, which incorporates the most current available in the literature, are not from the same population as the morphological sample, and therefore may not be as representative.

In addition, as better behavioral studies become available, it has become clearer that Cebuella may not leap as much as had been hypothesized previously (Garber et al. 2012; Youlatos 1999;

Youlatos 2009). Perhaps this partially explains why it does not fit the expectations of the hypotheses.

Cebuella is likely a phylogenetic dwarf (Ford 1980; Ford and Davis 1992; Garber 1992;

Montgomery and Mundy 2013) and some of its unique characteristics may be related to that.

Cebuella’s morphology may be better understood if and when more specimens of Callibella, another presumably independently dwarfed marmoset, become available. Ford and Davis

(2009) report that Callibella (based on an N of 1) lacks some of the highly derived traits evidenced in Cebuella, and likely is more quadrupedal than Cebuella and more vertically oriented than Mico.

Cebus is of interest for where the species cluster with respect to the regression line(s) in the features associated with leaping tendency. Cebus species have been relatively well studied in terms of behavior, see Chapter 1 for citations of Cebus locomotor behavior. Cebus has been determined to be primarily quadrupedal, however, interestingly, it evidences features 212 hypothesized for leaping behavior. Cebus has a longer dorsal and distal projection of the ischium relative to body size. These features are indicative of leaping from vertical and from pronograde posture, respectfully. Cebus also evidences features of the thigh and knee hypothesized for leaping. With the exception of posterior articular surface and femoral neck length, Cebus species signal leaping tendency. Clearly, there is some disconnect between the hypotheses, Cebus’ leaping features, and their locomotor behavior. It is highly unlikely that

Cebus is an active/frequent leaper compared to the other generalized platyrrhines, considering the behavior data that is available. It is possible that, while the hypotheses fit the model within

Pithecia, within Cebus (and perhaps other generalized quadrupeds) the signal is picking up a generalized quadruped’s limited leaping tendency.

Callimico is considered a prominent leaper, including being described as a vertical clinger and leaper (or leaping from vertical supports), see Chapter 1 for citations of Callimico locomotor behavior. Callimico does not stand out in this study as evidencing conclusive leaping features, however. In the platyrrhine wide regressions, the only feature where Callimico stands out as having a leaping feature is femoral neck thickness. In the callitrichid only regressions, Callimico evidences several features that may be linked to leaping, including a slightly shorter femoral neck, a slightly thicker femoral neck and a slightly wider greater trochanter. It should be noted however, that in both sets of regressions, when Callimico does not stand out as having a significant leaping feature (being above or below the regression line(s)), it falls on the regression line(s) indicating a normal sized feature relative to body size. That is to say, that Callimico does not evidence contradictory quadrupedal versus leaping features, but rather only evidences a handful of leaping features. 213

Factors that Influence the Results There is a series of factors that may influence the way the data is collected, analyzed and/or interpreted. These factors can only be partially controlled for and affect most, if not all studies that attempt to link behavior and morphology. These factors include body weight data, locomotor/behavioral data, sample size and taxonomic/species data.

Interspecific Scaling of Variables In the platyrrhine-wide regressions isometry is present for many variables, however, roughly half of the features measured show negative or positive allometry. Please see Table 3.1 for the basic statistics of the regressions. Nearly all of the features measured correlate highly to body size, this is not unexpected given the range of body size in the sample. Perhaps the slopes of the lines

(positive or negative allometry) can provide support or refutation for the hypotheses.

An example of this is dorsal projection of the ischium. Dorsal projection is negatively allometric

(in OLS, but not RMA) indicating that as body size increases the relative size of the dorsal projection of the ischium does not increase as quickly as would be expected if it were isometric.

This is an important consideration because in platyrrhines the leapers tend to be smaller in body size while the largest bodied animals of climbers and brachiators. The fit of the line, being negatively allometric, subtly adds support to the hypothesis that leapers should/will have a relatively longer dorsal projection, however, this does not clarify whether it is clearly a leaping feature or possibly a ‘small’ size feature. It is important to acknowledge that dorsal projection is one of several variables where this is applicable, also this is only doable in platyrrhines because 214 the locomotor differences are somewhat body size dependent. If there were a large bodied platyrrhine that was a significant leaper, then the fit of the line seen in the dorsal projection regressions would not have as much meaning. Furthermore, we should expect all features hypothesized to be larger in leapers to evidence negative allometry and this is not the case.

Dorsal projection, distal projection, ilium width, femoral neck thickness, femoral articular surface and greater trochanter width are all expected to be larger in leaping taxa; therefore one would expect them all to be negatively allometric. However, while dorsal projection distal projection and ilium width are negatively allometric (OLS), neck length is isometric while articular area and greater trochanter width is positively allometric. Continuing with this theme, features hypothesized to be larger in climbers/suspensory taxa should evidence positive allometry, while those features hypothesized to be smaller should evidence negative allometry, this is not the case; indicating that the fit of the line does not necessarily provide support for the hypothesis(es).

Muscle Rugosity and Osteological Markings It should be noted that with reference to some of the non-quantitative features, the issue of muscle rugosity comes into play. For the purposes of this study, it is assumed that a line, crest, ridge, etc. is the attachment point for a muscle(s), ligament and/or tendon. It is also assumed that the larger more pronounced the osteological feature, the larger the muscle that is attaching to it.

A larger muscle generally equates to more force exerted by the muscle.

Vertebrate paleontologists have been interested in equating osteological features to muscle size as a way of interpreting fossil specimens. Since soft tissue does not preserve in fossils, being 215 able to suggest muscle size based on osteological features would be valuable. However, it has been shown that tendinous and aponeurotic muscle attachments often times yield a pronounced osteological feature, while fleshy muscle attachments tend not to mark the bones in as pronounced a manner (Bryant and Seymour 1990, Perry and Prufrock 2018). Furthermore, it has been suggested that the power of a muscle is not best shown by its size at the attachment point, but rather by its diameter/size in the mid-section of the muscle (Bryant and Seymour 1990).

Bryant and Seymour (1990) show that in Canis and Ursus it is sometimes possible to determine myological information from osteological/paleontological specimens. However, even in groups such as carnivores, one must have adequate knowledge of the myology of extant taxa in order to extrapolate the muscle-bone relationships of fossil taxa. In essence, it is important to have an understanding of closely related species in order to ascribe information based on muscle size, and so forth to other taxa. Within this study, this is not deemed to be an issue, considering all the taxa studied are phylogenetically close in relationship. As opposed to trying to determine muscle size based on specimens from different orders, all of the specimens in this study come from one radiation of primates.

It should be noted that Demes and Creel (1998) report that in prosimian leapers, overall muscle mass and propulsive muscle mass scale with negative allometry, showing that larger bodied animals have relatively smaller and less powerful muscles than smaller bodied species. If this translates to platyrrhines, this could explain the lack of osteological markings in some species where one would expect to see them. Furthermore, it could explain the presence of some markings in species where they are unexpected. It is without question that more data needs to be gathered about the cross-sectional properties of muscles in platyrrhines. With more data and 216 an understanding of how platyrrhine muscles scale relative to body size, possibly, then we may be able to determine if some of these features are present because they are linked to locomotor behavior, are present because they are linked to body size or are present because of a combination of both. Ultimately, with such limited data about platyrrhine myology, this question is not resolved.

With reference to the data in this study, brachiating taxa have a larger intertrochantic line than leapers or climbers. If this is because of absolutely larger ligament size, this somewhat contradicts that idea that they would need a looser hip joint not a tighter one. There is little data to add to the overall discussion of ligament size in the hindlimb of the platyrrhines.

Additionally, intertrochanteric crest should be larger in climbers, but is actually so in quadrupeds and smallest in suspensory taxa. This begs the question of whether suspensory taxa (the largest bodied platyrrhines) have smaller intertrochanteric crests because of negative allometry in muscle mass or if there are unanswered questions of functional requirements in quadrupedal locomotion. There is a similar issue with reference to trochanteric fossa, where suspensory taxa evidence shallower fossae. Is this because of negative allometry in regards to muscle/ligament size or are there functional signals that are not being picked up. Unfortunately, this study does not have the data to further expound upon these ideas.

Bodyweight Data Very few of the morphological specimens used in this study have associated body weights.

Therefore, species means of both morphological measurements and body weights were used instead. As noted above, for Cebuella, there is always a possibility for a mismatch between the 217 morphological and body mass samples. As was discussed in Chapter 2, an attempt was made to gather as much of the published platyrrhine body mass data as possible. Body mass data is vital as it is an integral part of the statistical analyses employed. Two significant published collections of primate wide/platyrrhine wide bodyweight data exist (Ford and Davis 1992; Smith and

Jungers 1997). These published works are an excellent beginning to determine accurate bodyweights within the platyrrhines. Unfortunately, both these reports are nearly twenty or more years old, and do not represent the entire swath of species within the platyrrhines. As species are divided and renamed, new body weight data must be assembled that is appropriate to the new species, but also takes into account the ever-changing taxonomy.

Additionally, trying to decipher the mechanism that explains differences amongst the published accounts is nearly impossible. For example, in this study, differences in wild body mass data of

Cebuella is only 9 grams (roughly 1 percent of overall body weight), a slight difference.

However the difference in the wild body mass data of Callimico is 131 grams (roughly 27 percent of overall body weight). Average male and female bodyweight for Callimico is assumed to be roughly 490 grams, for this study. This number was settled upon after using published data by Ford and Davis (1992) and Rowe and Myers (2016). This number excludes the 361 grams value published by Encarnacion and Heymann (1998), as it appears to this author to be substantially low overall. Rowe and Myers (2016) includes data that while small in sample size is known to be of wild weighed animals. This difference is significant and could have influenced the results of the analyses. It is not possible to know what exactly accounts for differences in the published weights beyond general measurement error, seasonality (in small bodied taxa), disease, male/female dimorphism, etc. 218

For this study, male and female weights were averaged, in part because the species’ means morphological data were averaged between the genders. For species where sample sizes were small (roughly half of the species examined in this study) it simply was not possible to conduct an analysis that is gender specific (but this factor is probably not relevant for Callimico, because dimorphism is not strong). Ultimately, the question of how best to handle unknown or poorly known body weight data has to be answered. The simplest overall answer is to assemble as much data as possible, theoretically, that way, high or low body weight data gets mitigated by an increased number of data points. However, that is not always possible or perfect; in this study that would have resulted in using a body weight for Callimico that was unacceptably low.

Bodyweight discrepancy may further explain the divergence of Leontopithecus and Callithrix species evidenced in many of the regressions. As was discussed previously, there is little behavioral data that would indicate a significant difference in the locomotor morphology of the lion tamarin species and/or the Callithrix subspecies, however, they (represented by two species each) are often separate from each other in the regression analyses. It is possible that inexact bodyweight data for individual species of Leontopithecus and Callithrix is responsible for the unexpected differences; or more likely that a combination of inexact bodyweight data coupled with inadequate locomotor data.

Body Size, Ecology and Locomotion Evolutionary questions surrounding body size, ecology and locomotion persist. Forest/canopy utilization, diet, mechanical/anatomical advantages and other factors have all been linked to body size(s) differences in primates. Fleagle and Mittermeier (1980) identified several factors that 219 they linked to body size. They demonstrated in a comparison of several plattyrhine species that as body size increases leaping decreases and brachiation and climbing increase. They argue that leaping occurs most often in the discontinuous understory of the forest, while other locomotor modes occur higher in the canopy. Small animals encounter more ‘gaps’ to cross than would a larger bodied primate. Larger bodied primates would likely suspend themselves in order to reach food on terminal branches. Suspension from multiple supports, plus tail assistance would help provide balance. Furthermore, larger body size is disadvantageous should an animal fall from the canopy. Larger body mass means more energy has to be dissipated when hitting the ground (Cartmill and Milton 1977).

Other researchers have argued that while some of Fleagle and Mittermeier’s (1980) observations are consistent, many are not applicable to other primate radiations. It is overly simplistic to just say that leaping decreases as size increases. Gebo and Chapman (1995) and McGraw (1998) illustrate that leaping and climbing are not associated with body size in cercopithecid monkeys the way they are in platyrrhines, since some of the larger monkeys (Colobus) are among the most frequently leaping. Within prosimians, tarsiers (and galagos) and sifakas are acrobatic leapers, but significantly different in terms of body size. On the other hand, brachiation does seem to be relegated to larger bodied species (Ateles, Brachyteles, hylobatids and Pongo are all larger bodied species within their respective radiations.) Furthermore, McGraw (1998) shows that a high percentage of leaping is not relegated to the understory, supporting the idea that ecological and locomotor correlations are complicated.

Diet has long been thought to be linked to body size as well. In some ways this likely is true.

Small bodied primates can be insectivorous while leaf eating increases with body size. Fruit 220 eaters likely will supplement their diet with either insects or leaves depending on body size (Kay

1984). In platyrrhines, Callimico and other callitrichids have been shown to incorporate high percentages of exudates into their diet (Porter 2007). Gumnivory is non-existent/unusual in other platyrrhine families. This is likely also linked to the prevalence of VCL behavior in some species of callitrichids, in that vertical clinging is necessary to obtain the best exudates on the larger main trunks of trees.

Ultimately, the evolutionary advantage/disadvantage to small or large body size is intimately linked to ecology and locomotion and is probably not consistent within every radiation.

Platyrrhines do tend to leap less as body size increases, however this is not a hard and fast rule; there are exceptions. For example, Ateles and Alouatta are similar in body size and differ greatly in locomotor behavior.

Locomotor and Behavioral Data It needs to be acknowledged that not all locomotor data is equal. All locomotor data is valuable and important to the overall understanding of an animal’s behavior, however. It would be wonderful if every field study used the same metric, the same locomotor descriptions and the same timeframe, etc. That is not the case, however. One researcher’s description of a locomotor behavior may be equal to three or four locomotor behaviors to another researcher. One researcher may report only ‘quadrupedal’ while another may subdivide quadrupedalism into

‘quadrupedal clamber, quadrupedal walk, quadrupedal run’, etc. This necessitates the lumping of locomotor modes into the broadest categories. For the platyrrhines in this study the locomotor 221 data was condensed into four categories, generalized quadrupedalism, leaping, climbing and hindlimb suspensory activity.

Where this becomes most problematic is when a quantifiable percentage of locomotor behavior is needed. This study sought as much data related to individual species’ locomotor preferences as possible. Some of these studies evidenced significant long-term field studies with quantifiable locomotor percentages, while other studies are more descriptive in style, and do not have quantifiable numbers to back up the descriptions. That resulted in this study using multiple sources whenever possible to garner, as accurately as possible, a description of a primate’s locomotor tendencies. Several researchers (Porter, Garber, Youlatos, or Walker) use consistent methodology across multiple studies (sometimes including different localities and different species). This data is invaluable because it allows easy and consistent comparison of species and behaviors. Suffice it to say that, this study attempted to assign a general locomotor category to a species based on as much data as was available at the time of writing.

Another issue that relates to locomotor behavior is the definition of certain categories. Two examples exist, vertical clinging and leaping and brachiation. Vertical clinging and leaping is a category of leaping behavior identified in the prosimians and attributed to Cebuella (Youlatos

1999b, 2009; Kinzey et al. 1975), Callimico (Porter 2004, 2007) and Pithecia (Walker 2005).

Please see discussion in Chapter 2 of VCL. The issue becomes clearer as no platyrrhine locomotes in the same way as the true prosimian vertical clingers and leapers. The acrobatic tarsiers, galagos, and indriids, are the progenitors of the VCL definition. It is ascribed to some of the platyrrhines based on their tendency to have a smaller body size and live in areas where bamboo and other vertical substrates are common, not to mention having a relatively high 222 leaping percentage in their repertoire. For Callimico (Porter 2007) and other callitrichids that consume high quantities of exudates, the vertical clinging posture is somewhat linked to diet

(Garber 1992). Minimally, it can be problematic to equate the prosimian VCL taxa with the platyrrhine leapers. It seems important to point out that while Cebuella, Callimico and/or

Pithecia show evidence of a relatively high percentage of leaping behavior and may leap from vertical supports (see behavioral data outlined in Chapter 1); there are likely functional and kinematic differences in the leaping that separate platyrrhine leapers from the prosimians beyond the VCL label, and this may be why we do not see the kind of morphological adaptations to that behavior that we see in prosimians. Differences, in the kinematics of leaping and trunk to trunk leaping, are evident within the Callitrichidae as well (Youlatos 2009b; Garber et al. 2005; Garber and Leigh 2001).

A similar discussion has taken place with regards to the use of the term ‘brachiation’. Others

(Mittermeier and Fleagle 1976) have proposed the differentiation between brachiation and suspensory activity. Please see Hunt (1996) for a more complete discussion of postural descriptions. This does not pose many problems, (other than hypothesized brachiator anatomical features have been suggested as potential forelimb suspensory features as well) however, it needs to be mentioned as there are likely functional and kinematic differences between the two groups that were not the focus of this study.

Locomotor Categories and the Pitfalls of ‘Lumping’ Behavioral Modes As has been discussed previously in this work, ideally all locomotor data would be based on the same metric. Unfortunately, most researchers differ in their definitions and use of terminology related to locomotor behavior. The problems associated with this are compounded when data is 223 lumped into categories, however, this cannot be avoided. The use of locomotor categories is virtually mandated in a study, such as this, that covers an entire radiation of primates.

The issues associated with using locomotor categories are not newly discovered. Ripley (1967) and Kinzey (1967) discussed problems stemming from the paucity of locomotor/behavioral data and discontinuous/non-existent locomotor definitions. These issues have not been completely rectified to this day and have been the subject of continued scholarship (Hunt et al. 1996,

Dagosto and Gebo 1998, Walker 1998). When quality locomotor data exists, there, often times, is not a consistent use of the same definitions within categories by different researchers. This necessitates the lumping of data into categories.

One of the main problems associated with the lumping of behavioral data into categories is that often behaviors do not lend themselves to one word descriptions. In order to fully appreciate the data and make it most applicable, it would appropriate to know as much about the behavior as possible (orientation, substrate, distance, etc., etc.) However, this is not present in many studies, so lumping the data is the only option. Another problem associated with use of categories is ensuring that the category takes into account differences in morphology (Hunt et al. 1996,

Walker 1998). The use of categories that combine behaviors that use opposite muscular actions

(i.e. abducted postures lumped with adducted postures) will only serve to obscure any morphological behavioral correlation. Ideally, a rigorous and complete system of behavioral definitions would be used (Hunt et al. 1996), however, there still exist problem categories.

‘Climbing’ has been identified as a potential problem category because of the number of locomotor behaviors and actions that get lumped together. 224

The use of locomotor categories is mandated by the scope of this study and many others. The selection of categories is based in part by the known behavioral repertoires of platyrrhines and the desire to have categories that are differentiated by anatomical requirements. There is little question that using categories does obscure or eliminate some kinematic differences between locomotor function and behavior, however, that concession is standard for morphological and behavioral studies. It has been more than twenty years since Dagosto and Gebo (1998), Walker

(1998) and Hunt et al. (1996) implored researchers to use standardized definitions and categories and unfortunately there is still limited consistency across studies. Fortunately, however, the number of long term observational studies has increased drastically since Ripley (1967) identified the issue.

Sample Size A robust sample size is desired for most statistical analyses. However, it is not always possible to obtain large numbers of postcranial specimens. In this study, 22 of the 45 species were represented by five or fewer individual specimens. Ideally, more would have been obtained, however, that was not possible because of the limitations of time and money. Furthermore, there is no guarantee that every species is represented by large numbers of specimens, if time and money were limitless. Skulls and pelts are preserved and catalogued far more often than disarticulated post-cranial elements. 225

It is possible that the small sample sizes of several species are skewing the data in one direction or another. However, there is no way to predict this, nor is there any way to correct for the unknown. Precautions were taken to work most often with species’ means which helps to mitigate a small sample. There is one circumstance when a small sample size is guaranteed; the attribution of function, body size, etc. to fossil specimens. When working with fossils, one is likely guaranteed an N of one. Thus, it is important to understand the issues surrounded limited sample size, but not exclude data just because there is a limited sample.

Species Data Great care was taken during data collection to ensure that each specimen matched the species to which they were supposed to belong. However, even as data collection was taking place, genetic evidence was leading researchers to divide and sub-divide species. The museum collections cannot possibly keep up with the taxonomy. Unfortunately, location data is often missing or incomplete, and I failed to photograph the skins (when skins were present).

I tried to ensure that each specimen matched its designated species by examining the skin, skull and post-crania to make sure that museum numbers matched. Location data (when available) was used to group specimens. I checked the actual skins against photographs of known species and used Groves (2000) to corroborate the accuracy of the location data. Nonetheless, it is impossible to be certain of a specimen’s affinity. Deference is given to the species name on the specimen box and the data on the skin tag. It should be noted, that this is primarily a problem within the callitrichids. Ultimately, when there was concern for a specimen’s affinity, I excluded it from the study. 226

Missing Data Ideally, this study and others would not be hampered by the unknown of missing data.

Specimens of all species would be available, bodyweight data would be consistent and behavioral data would be available for every species. Unfortunately, that is not the case. I will try to identify the missing pieces of data that would aid this study in the future.

There are several species that are not represented in this study because they are unavailable at the museums for data collection. Brachyteles is under-represented in American museums. I was only able to locate one Brachyteles specimen and it was hampered by being of unknown origin and likely juvenile. There is speculation that the Erikson collection contained specimens of

Brachyteles, unfortunately that could not be verified. Furthermore, in order to obtain a sample size of Brachyteles, one would need to visit the foreign (Brazilian and possibly East Berlin) museums. Brachyteles is of interest because it is the largest platyrrhine and engages in significant suspensory activity. It could help to verify the data that is presented for Ateles.

There is currently only one specimen of Callibella, the dwarf marmoset. It was not possible to examine this specimen. Callibella would be of interest considering its diminished body size and position within the callitrichid radiation. It could conceivable aid in the understanding of

Cebuella’s unique morphology. Unfortunately, there is limited behavioral data on Callibella, so work is needed in multiple areas.

Besides an increased sample size of species that are under-represented in this study, one species is completely lacking, Saimiri oerstedii. There is valuable behavioral data on this species, unfortunately, there are no museum collections of post-cranial specimens. It would be beneficial to link the behavioral data with confirmed S. oerstedii specimens. 227

For the specimens used in this study, bodyweight data is limited for several species. Cacajao rubicundus has body mass data that is only represented by three individuals. Callimico and

Lagothrix lugens have limited body weight samples. Leontopithecus species have been studied significantly in captive collections, however, wild caught data is less common. Leontopithecus is hampered by strong seasonal variation, so a long term study is required. It would be beneficial to have additional data. Unfortunately, active field studies are expensive and not always possible. Additionally, trap and release of animals to obtain body weight data is not always done, even when a species is being studied.

In terms of behavioral data, there is no such thing as too much data. Each species could benefit from additional wild observational behavior data. Several species have been under-studied however. Callithrix, Mico and Leontopithecus have all been studied in captive situations, however, there is a paucity of wild behavioral data. Additionally, several species have been studied and in the time since the publication of the data, those species have been divided or regrouped. Unfortunately, it is not always possible to accurately assign affinities to the published data. It is assumed that the data is representative of the species that they claim to be from. Furthermore, it can be assumed that closely related species probably share some behaviors in common. This is primarily a problem within the Callitrichidae and smaller cebids.

Future Studies It is important to acknowledge that considering the limitations imposed by this study and examined previously, there is significant areas of platyrrhine morphology and behavior that continue to be unresolved. While the examination of ischial shape was a continuation of a 228 hypothesis that was first published by Fleagle and Anapol (1992) with regards to leaping versus quadrupedal behavior and its association and evidence for hominid bipedalism; the hypotheses focusing on the hip and knee were assembled with data and inferences from across the primate

(and mammalian) spectrum. There is future work likely with regards to the hip, particularly as acetabular size and depth relate to femoral head size within the suspensory groups. Hip joint excursion is imperative for the behavior evidenced by Ateles. There is certainly the possibility of further examination of suspensory behavioral correlates to hip anatomy beyond that which was discussed in this work.

Furthermore, future areas of work include the functional anatomy of the platyrrhine knee.

Building upon the initial hypotheses presented in this work along with the research that exists covering the swath of knee morphology in the African catarrhines and great apes up to human bipedalism (including work by Tardieu and others) may help to elicit information about platyrrhine knee morphology. Likely there are differences at this joint between the locomotor groups that have yet to be completely determined.

Notwithstanding the great work done by primate paleontologists to provide insight into the complex and enigmatic primate fossil record, the platyrrhine fossil record is not without its frustrations. Few platyrrhine taxa (in the fossil record) have post-cranial elements with which it is possible to comfortably attribute locomotor tendency (Table 4.2). Furthermore, the majority of platyrrhine fossils are described in terms of their extant counterparts, meaning that the elusive early platyrrhine/catarrhine platyrrhine link is somewhere yet discovered. I included this in the section describing future work, not because many great researchers have not spent time and 229 energy looking into this very subject, but rather because basal platyrrhine morphology, locomotor behavior, and body size remain of personal interest to me.

Subfamily Species Post-cranial elements Citation Pitheciinae Soriacebus No Fleagle et al. ameghinorum 1987 Soriacebus No Fleagle 1990 adrianne Proteropithecia Talus Kay et al. 1998 neuquenensis Homunculus Femur, radius, ulna, Ameghino 1891 patagonicus humerus Carlocebus scapula, ulna, femur, Fleagle 1990 carmenensis tibia, tali Carlocebus No Fleagle 1990 intermedius Cebupithecia Significant postcranial Stirton and sarmientoi elements - No pelvis Savage 1951 Nuciruptor Talus Meldrum and rubricae Kay 1997 Xenothrix No Williams and mcgegori Koopman 1952 Antillothrix No MacPhee et al. bernensis 1995 Paralouatta humerus Rivero and varonai Arredondo 1991

Cebinae Dolichocebus Talus Kraglievich 1951 gaimanensis Chilecebus No Flynn et al. 1995 carrascoensis Neosaimiri fieldsi Humerus, ulna, femur, Stirton 1951 tibia, calcaneus, tali Laventiana Talus, tibia Gebo et al. 1990 annectens

Aotinae Tremacebus No Rusconi 1933 harringtoni 230

Branisella No Hoffstetter 1969 boliviana Aotus dindensis Talus Setoguchi and Rosenberger 1987

Atelinae Stirtonia No Stirton 1951 tatacoensis Sirtonia victoriae No Kay et al. 1987

Callitrichinae Mohanamico No Luchterhand et al. hershkovitzi 1986 Patasola No Kay and magdalenae Meldrum 1997 Lagonimico No Kay 1994 conclutatus Micodon kiotensis No Setoguchi and Rosenberger 1985

Atelinae Protopithecus Femur, humerus Hartwig and brasiliensis Cartelle 1996 Caipora Significant skeleton Cartelle and bambuiorum Hartwig 1996 Table 4.2 - Brief summary of known platyrrhine fossils

The relative paucity of platyrrhine fossil post-crania has not (nor should it have) prevented the discussion of fossil locomotor behavior. Cebupithecia, represented by significant post-cranial elements, is thought to evidence Pithecia like locomotor behaviors (Ford 1990; Meldrum and

Lemelin 1991); likely employing a combination of arboreal quadrupedalism, leaping and potentially suspensory activities. Carlocebus is thought to have employed arboreal quadrupedalism and climbing as its main locomotor modes (Anapol and Fleagle 1988). The suite of features evidenced by Homunculus seems to indicate a primate that departed slightly 231 from arboreal quadrupedalism to employ more leaping behaviors (Ford 1990). The talus of

Dolichocebus has been interpreted to represent an arboreal quadruped (with some indications for leaping) (Gebo and Simons 1987). Proteropithecia (represented by a talus) is said to resemble the extant Callicebus (Kay et al. 1998). Neosaimiri has been studied from several post-cranial elements including multiple tali. It has been described as predominantly quadrupedal with leaping employed to cross gaps (Nakatsukasa et al 1997). Aotus dindensis has been said to have likely employed arboreal quadrupedalism with possible leaping (Gebo et al. 1990).

The preceding brief synopsis of the platyrrhine fossil record (as post-cranial elements are concerned) is interesting for the lack of highly specialized locomotor behavior features. These fossils do not appear to be representing highly innovative and overly specialized forms compared to their extant counterparts. In deed many of these fossil taxa are described based on the affinities they have to their extant relatives. Some of these represent species that are in some way partially indicative of the presumed earliest platyrrhine (Ford 1988). However, it seems to me that this likely indicates a stagnation for several million years in favor of the generalized platyrrhine form.

Locomotor Behavior in Fossil Platyrrhines The attribution of locomotor behavior to fossil platyrrhines has been attempted by researchers, including Ford (1990), Meldrum and Lamelin (1991), Anapol and Fleagle (1988), Gebo and

Simons (1987), Kay et al. (1998), Nakatsukasa (1997) and Gebo et al. (1990) among others. The process is made difficult by several factors including the relative lack of post-cranial remains and in this study the lack of a strong signal related to locomotor tendency. 232

The ancestral platyrrhine is thought to be an arboreal quadruped and of small body size (Ford

1988). The attempt to ascribe body size to fossil platyrrhines (Sears et al. 2008) has not altered the presumed locomotor tendency of the ancestral platyrrhine. This associated with the diversity of body size in platyrrhines makes it relatively straightforward to hypothesize that large bodied fossil playrrhines would likely be brachiators or climbers while leapers would be of small body size and generalized quadrupeds would be of moderate body size. As has been discussed known fossil platyrrhines, for the most part, are relatively easily ascribed to the extant platyrrhine families. Should a fossil pithecid be discovered with ischial fragments, it might be possible to say whether it was more likely VCL or a quadruped depending on where the fossil specimen fell relative to known extant specimens. Figure 4.1 illustrates dorsal projection of the ischium relative to lateral condyle length (body size surrogate) in extant pithecid specimens. If a fossil specimen fell within the blue oval, one could comfortably deduce that the species incorporated

VCL/Leaping in its repertoire. However, the cluster of specimens below the oval are mixed between quadrupeds and leapers. This is an example of the relatively difficult task of determining locomotor tendencies of fossil primates. One requires post-cranial fossil elements as well as a strong locomotor signal.

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Figure 4.1 – Within pithecid scatterlot of dorsal projection vs. LCL. Large data points are species means, small data points are individual specimens.

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Conclusion Platyrrhines are unique among primates. They exhibit great diversity in terms of body size and locomotor behavior, however, they seem to be more generalized overall in terms of their postcranial morphology relative to their prosimian and catarrhine relatives. Fleagle and Anapol

(1992) and Fleagle and Meldrum (1988) identified features within the pithecids that they believed were morphological correlates to the pithecid behaviors of leaping (Pithecia) and quadrupedalism (Chiropotes and Cacajao). While partially confirmed in this work, neither study has conclusively shown to be applicable across platyrrhines. Leaping behavior, it seems, is likely of a more generalized nature than that seen in the prosimians and not evidenced as robustly in the underlying morphology. While some features, such as ischial projection, are linked to leaping, other features were not proven to be conclusively linked to a particular locomotor behavior in any group or species. Furthermore, climbers evidenced a unique anatomy with regard to several pelvis features, however, overall climbers did not show a convincing anatomical feature that could be singularly correlated with this movement. The atelid’s forelimb suspensory behavior is often compared to brachiation of the Old World pongids and hylobatids, however, in this study Ateles stood out often times for its hindlimb oddities (including ischial projection – a feature linked to leaping). Ateles did show some evidence of increased joint excursion at the hip, however, more work is required to fully explain the implications of this feature. The taxa that have been described as primarily quadrupedal evidenced a combination of traits that would lead one to believe in a more generalized platyrrhine form that is capable of multiple locomotor behaviors, rather than any one specialized locomotor morphology. In a brief survey of platyrrhine fossil remains, it is also evidenced that perhaps the generalized platyrrhine 235 locomotor tendency shown in part by this study is seen in the known platyrrhine fossil record as well.

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Appendix 1

Species Specimen # M/F Lococation Info. FMNH Cebus albifrons 13242 F Colombia: Magdalena, Bonda FMNH 18867 ? Colombia: Magdalena, Bonda FMNH 70632 M Colombia: Caqueta, Tres Troncos FMNH 70633 M Colombia: Caqueta, Tres Troncos FMNH 70634 M Colombia: Caqueta, Tres Troncos FMNH 98043 M Peru: Madre de Dios, Altamira NMNH 398444 F Colombia: Leticia NMNH 398448 F North Colombia: Barranquilla NMNH 398445 F Amazon AMNH 188018 F Peru: Loreto, Rio Samiria AMNH 188020 M Peru: Loreto, Rio Samiria, Yanayaquillo AMNH 211582 F Bolivia: Dept. Beni, Yacuma River mouth AMNH 211574 F Bolivia: Dept. Beni, 23 km W San Javier AMNH Bolivia: Dept. Beni, 1 km above Ibare River 211562 M Mouth Cebus albifrons AMNH hypoleucus 23403 ? Colombia: Bonda No Skull, No mandible AMNH

27 23401 F Colombia: Bonda

8 AMNH F Colombia: Bonda Broken Zygo, No Mandible

23402 AMNH 23399 ? Colombia: Cacagualita AMNH 23404 M Colombia: Bonda NMNH Cebus albifrons cesarae 281606 M Colombia: El Orinoco (Hershkovitz 1942) No Mandible NMNH Colombia: Colonia Agricola de Ceraco Licito, 281565 M Magdalena (Hershkovitz 1942) NMNH 281569 M Colombia: Colonia Agricola (Hershkovitz 1942) NMNH 281570 F Colombia: Colonia Agricola (Hershkovitz 1942)

Cebus apella FMNH 70606 M Colombia: Huila, Rio Aguas Claras FMNH 70610 F Colombia: Huila, Rio Aguas Claras FMNH 70613 M Colombia: Huila, Rio Aguas Claras FMNH 70614 M Colombia: Huila, Rio Aguas Claras FMNH 70624 M Colombia: Caqueta, Tres Troncos FMNH 93261 M Suriname: Nickerie, Keyser Gerbergte Airstrip FMNH 94300 M Brazil: Sao Paolo, Rocha FMNH 94303 F Brazil: Sao Paolo, Rocha FMNH 94304 M Brazil: Sao Paolo, Rio Verde FMNH 95336 M Suriname: Nickerie, Wilhelmina Mts. FMNH 27

95474 M Suriname: Nickerie, Wilhelmina Mts.

FMNH 95465 M Suriname: Brokopondo, Saramacca FMNH 95472 F Suriname: Nickerie, Wilhelmina Mts. FMNH 95473 M Suriname: Nickerie, Wilhelmina Mts. FMNH 98044 M Peru: Madre de Dios, Altamira FMNH 98046 M Peru: Madre de Dios, Altamira FMNH 70609 F Colombia: Huila, Rio Aguas Claras FMNH 70621 M Colombia: Caqueta, Tres Troncos FMNH 95470 M Suriname: Nickerie, Wilhelmina Mts. NMNH British Guyana: Rupununi District, 60 miles East 361020 M of Dadanawa Ranch NMNH 547900 F Brazil: Amazonas, Manaus NMNH Brazil: Amazonas, Manaus (4 km. East of the 62 547902 F Km. point on the Manaus Itacoatiara Road) Tappen 73 ? Brazil: Teresinha

NMNH Cebus (apella) libidinosus 270360 F Brazil: Between Barra do Rio and Caceres

Cebus capucinus FMNH 22396 F Honduras: Cortes, San Pedro FMNH 68837 M Colombia: Sucre, Las Campanas FMNH 68841 M Colombia: Cordoba, Catival

FMNH 2

80 68842 F Colombia: Cordoba, Catival

FMNH 68843 M Colombia: Cordoba, Catival FMNH 69650 F Colombia: Choco, Unguia NMNH 339874 ? Panama No Skull Available NMNH 338122 M Panama: Darien, Cerro Mali (4700 ft.) NMNH 338121 M Panama: Darien, Cerro Mali (4700 ft.) NMNH 338118 F Panama: Darien, Cerro Mali (4700 ft.) NMNH 338119 M Panama: Darien, Cerro Mali (4700 ft.) AMNH 14016 M Central Park Zoo, died 1893 AMNH 135414 ? No data

Cebus olivaceus FMNH 93521 F Suriname: Nickerie, Keyser Gerbergte Airstrip FMNH 93523 F Suriname: Nickerie, Keyser Gerbergte Airstrip NMNH 338960 F British Guyana: Rupununi, Kuitaro River AMNH 30200 M Venezuela: Rio Macho Cebus (nigrivittatus NNMH British Guyana: Rupununi District, 60 miles East castaneus) 361021 F of Dadanawa Ranch Cebus olivaceus AMNH apiculatus 30196 F Venezuela: Mariba, Rio Cauca AMNH 30195 M Venezuela: Mariba, Rio Cauca AMNH

30198 M Venezuela: Rio Macho, Rio Cauca Broken Zygo 2

AMNH M Venezuela: Mariba, Rio Cauca

30197 Cebus olivaceus AMNH castaneus 42319 M Guyana: Kartabo AMNH 42884 M Guyana: Kartabo AMNH 42873 F Guyana: Kartabo

AMNH Pithecia irrorata 248723 M Bolivia: Dept. Bando, rio Nareuda

Pithecia pithecia FMNH 93252 M Suriname: Nickerie, Keyser Gerbergte Airstrip FMNH 93251 M Suriname: Nickerie, Keyser Gerbergte Airstrip FMNH 95504 M Suriname: Brokopondo, Saramacca NMNH British Guyana: Rupununi District 50 miles E of 339659 F Dadanawa No Pelvis NMNH 300794 ? National Zoo (NZP 14454) AMNH 70377 M Zoo, NYZS AMNH 149149 M British Guyana: 'east side' Sanderson AMNH 42854 ? Guyana: Mazaruni, Potaro, Kortabo AMNH 42418 F Guyana: Mazaruni, Potaro, Kortabo AMNH 64089 F Guyana: Mazaruni, Potaro, Kortabo AMNH 48123 F Guyana: Mazaruni, Potaro, Kortabo 28

AMNH M Guyana: Mazaruni, Potaro, Bartica

42324 AMNH 48144 M Guyana: Mazaruni, Potaro, Kortabo AMNH 142939 ? Guyana: Mazaruni, Potaro, Kortabo AMNH 64088 ? Guyana: Kortabo

Pithecia monachus FMNH 70638 M Colombia: Caqueta, Tres Troncos FMNH 122796 M Peru: Loreto, Rio Samiria FMNH 70635 M Colombia: Caqueta, Montanita FMNH 70641 M Colombia: Putumayo, Rio Mecaya NMNH 395692 M AMNH 187988 M Peru: Loreto Bluntschli AMNH 187978 ? Peru: Loreto, Rio Samiria AMNH 187984 F Peru: Loreto, Rio Samiria Bisected Skull

Chiropotes satanas FMNH 95518 M Suriname: Nickerie, Wilhelmina Mts. FMNH 93255 M Suriname: Nickerie, Keyser Gerbergte Airstrip FMNH 95512 M Suriname: Brokopondo, Saramacca FMNH 93522 F Suriname: Nickerie, Keyser Gerbergte Airstrip

Skull Not Present (Borrowed), NMNH Brazil: Para - Altamira - 52 km. SSW of The East proximal femur broken and 549519 F Bank of Rio Xingu missing NMNH 338961 F British Guyana: Rupununi, Kuitaro River NMNH British Guyana: Rupununi, 25 miles E of 339661 F Dadanawa Skull Not Present; No pelvis AMNH 95760 M Brazil: Rio Tapajoz, Limaal Olalla Bros AMNH 96123 M Brazil: Rio Xinqu, Porto de Moz Olalla Bros

Cacajao (calvus) NMNH rubicundus 302626 M National Zoo Skull Not Present (Borrowed) NMNH 302627 F National Zoo Skull Not Present (Borrowed) NMNH 519570 F National Zoo AMNH 201122 F Collected in Field, No Location Data AMNH 70192 M Zoo, NYZS No Skull

Cacajao melanocephalus NMNH 221483 ? Brazil: Rio Negro No long bones present

AMNH Callicebus moloch moloch 94977 M Brazil: Rio Tapojoz, Tauary Olalla Bros.

FMNH Callicebus cupreus 122786 M Peru: Loreto, Rio Tigre FMNH 122785 M Peru: Loreto, Rio Tigre

Callicebus cupreus AMNH 28

discolor 130361 F Ecuador: Andus district, 800m 4

FMNH Callicebus torquatus 70691 F Colombia: Caqueta, Tres Troncos FMNH 70692 F Colombia: Putumayo, Rio Mecaya FMNH 38885 M Brazil: Amazonas, Rio Purus NMNH 398212 F San Diego Zoo

Calliceb us moloch AMNH Bolivia: Dept. Beni, Camiaco, (12 km NW donacephilus 211489 F Limoquise) AMNH Bolivia: Dept. Beni, Camiaco, (12 km NW 211488 M Limoquise) Broken Zygo AMNH Bolivia: Dept. Beni, Camiaco, (12 km NW 211487 M Limoquise) Callicebus donacephilus AMNH donacephilus 221490 F Bolivia: Dept. Beni, 10 km E. San Antonio AMNH 211492 M Bolivia: Dept. Beni, 10 km E. San Antonio AMNH 211493 M Bolivia: Dept. Beni, 10 km E. San Antonio

NMNH Proximal femur broken and Callicebus ornatus? 397933 M Colombia: Meta, Barbascal, Monte Socay missing Callicebus moloch AMNH ornatus 136217 M E. Colombia: Meta, Villavicencio, 500 m.

FMNH Aotos vociferans 125020 M Ecuador: Napo, Laguma Zacudo Cocha AMNH 239852 F Peru: Oxa Pampa, Dept. Pasco, Nevat Broken Zygo

AMNH 28

239851 M Peru: Oxa Pampa, Dept. Pasco, Nevat Bisected Skull 5

AMNH Aotus (azarae) infulatus 94992 F Brazil: Rio Tapojoz, Tauary AMNH Paraguay: Dept. Charo, 50 km. WNW Fortia Aotus azarae azarae 248393 M Madrejon AMNH 209916 F Brazil: Territory Rondonia, near Costa Marques AMNH Bolivia: Dept. Santa Cruz, 7 km N and 17 km W Aotus azarae boliviensis 246659 M Buena Vista, 353 m AMNH Bolivia: Dept. Beni, Mamore River, ~130 211463 M degrees 35' S AMNH Bolivia: Dept. Beni, Mamore River, ~130 211462 M degrees 35' S Broken Zygo, No Mandible AMNH Bolivia: Dept. Beni, Mamore River, ~130 211460 F degrees 35' S AMNH Bolivia: Dept. Beni, Mamore River, ~130 211464 F degrees 35' S AMNH 211466 F Bolivia: Dept. Beni, Puerto Caballo AMNH 211472 M Bolivia: Dept. Beni, 23 km W San Javier AMNH 211470 F Bolivia: Dept. Beni, 23 km W San Javier Broken Zygo AMNH 211478 F Bolivia: Dept. Beni, 20 km S San Joaquin AMNH 211482 M Bolivia: Dept. Beni, 20 km S San Joaquin Broken Zygo AMNH 211473 F Bolivia: Dept. Beni, 23 km W San Javier AMNH 211475 M Bolivia: Dept. Beni, 20 km S San Joaquin AMNH 211484 F Bolivia: Dept. Beni, ~ 10 km W San Pedro Broken Zygo

AMNH Bolivia: Dept. Beni, 20 km S San Joaquin, 215048 F Estancia Yutiole 28

AMNH Bolivia: Dept. Beni, 20 km S San Joaquin, 215052 ? Estancia Yutiole AMNH Bolivia: Dept. Beni, 20 km S San Joaquin, 215050 F Estancia Yutiole AMNH Bolivia: Dept. Beni, 20 km S San Joaquin, 215052 ? Estancia Yutiole

NMNH Brazil: Tabatinga, near Amazonas (Died San Aotus trivirgatus 337318 M Diego Zoo) AMNH 187963 F Brazil: Marajo

Aotus (trivirgatus) NMNH griseimembra 337317 F Colombia: Barranquilla NMNH Colombia: (Died at Walter Reed Army Institute of 396381 F Research) NMNH 337315 F Colombia: Barranquilla NMNH 337316 M Colombia: Barranquilla NMNH 396444 M Colombia

Aotus (trivirgatus) FMNH nigriceps 98037 M Peru: Madre de Dios, Altamira NMNH 396734 F Peru: Iquitos NMNH 396725 M Peru: Iquitos NMNH Peru: Iquitos (Name on box was scratched out, 396753 M individual bones says 'Peru')

FMNH Aotus lemurinus 69606 F Colombia: Antioquia, Bellavista FMNH 28

69608 M Colombia: Antioquia, Bellavista

FMNH 69607 F Colombia: Antioquia, Bellavista FMNH 69609 M Colombia: Antioquia, Bellavista FMNH 69610 F Colombia: Antioquia, Bellavista FMNH 69613 F Colombia: Antioquia, Rio Currulao FMNH 68860 M Colombia: Cordoba, Catival FMNH 68858 F Colombia: Cordoba, Catival

FMNH Saimiri sciureus 70644 F Colombia: Huila, Rio Aguas Claras FMNH 70650 M Colombia: Huila, San Adolfo FMNH 70668 M Colombia: Putumayo, Rio Mecaya FMNH 93519 ? Suriname: ?, ? FMNH 70646 F Colombia: Huila, San Adolfo NMNH 547907 F Brazil: Amazonas, Manaus Body Weight = 370 gr. NMNH 547903 F Brazil: Amazonas, Manaus Body Weight = 410 gr. NMNH 547905 M Brazil: Amazonas, Manaus Body Weight = 550 gr. NMNH 547909 F Brazil: Amazonas, Manaus Body Weight = 400 gr. NMNH 547908 ? Brazil: Amazonas, Manaus Body Weight = 370 gr. NMNH 547906 M Brazil: Amazonas, Manaus Body Weight = 590 gr.

Brazil: Trapped within 20 miles of Leticia 28

Tappen 4 M (Colombia) 8

Brazil: Trapped within 20 miles of Leticia Tappen 5 F (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 23 F (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 10 M (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 9 M (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 8 M (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 14 M (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 19 M (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 18 M (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 31 F (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 30 F (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 32 M (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 39 F (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 49 F (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 67 F (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 56 M (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 82 M (Colombia)

Brazil: Trapped within 20 miles of Leticia

28 Tappen 70 M (Colombia)

Brazil: Trapped within 20 miles of Leticia Tappen 92 M (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 88 ? (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 105 F (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 101 F (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 99 F (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 98 F (Colombia) Brazil: Trapped within 20 miles of Leticia Tappen 97 F (Colombia)

Saimiri sciureus NMNH boliviensis 397667 F Peru: Pucallpa NMNH 397669 F Peru: Pucallpa NMNH 398621 F Bolivia Saimiri boliviensis AMNH boliviensis 211592 M Bolivia: Dept. Beni, 6 km S. Buena Hora AMNH 211594 M Bolivia: Dept. Beni, 6 km S. Buena Hora AMNH 211591 F Bolivia: Dept. Beni, 5 km NW Alejandria AMNH 211598 M Bolivia: Dept. Beni, 6 km S. Buena Hora AMNH 211596 M Bolivia: Dept. Beni, 6 km S. Buena Hora AMNH 211601 M Bolivia: Dept. Beni, opposite Cascajal

AMNH Bolivia: Dept. Beni, Ibare River, 27 km. from 2

90 211610 M mouth

AMNH Bolivia: Dept. Beni, Ibare River, 27 km. from 211609 F mouth AMNH Bolivia: Dept. Beni, Ibare River, 27 km. from 211606 F mouth AMNH Bolivia: Dept. Beni, Ibare River, 27 km. from 211613 F mouth AMNH Bolivia: Dept. Beni, Ibare River, 27 km. from 211614 F mouth AMNH Bolivia: Dept. Beni, Rio Mamare, 12 degrees 211616 F and 26' S AMNH Bolivia: Dept. Beni, Rio Mamare, 12 degrees 211618 M and 26' S AMNH Bolivia: Dept. Beni, Rio Mamare, 12 degrees 211615 F and 26' S AMNH Bolivia: Dept. Beni, Rio Mamare, 12 degrees 211649 M and 26' S AMNH Bolivia: Dept. Beni, Rio Mamare, 12 degrees 211651 M and 26' S AMNH 211624 M Bolivia: Dept. Beni, 17 km. SE Puerto Julio AMNH 211627 M Bolivia: Dept. Beni, Puerto Siles AMNH 211631 F Bolivia: Dept. Beni, Puerto Siles

AMNH Brazil: Territory Rondonia, opposite Baures Saimiri ustus 209935 F River mouth

FMNH Callimico goeldii 98034 M Peru: Madre de Dios, Altamira FMNH 159976 F Zoo

FMNH 2

153715 M Zoo 1

FMNH 134520 F Zoo FMNH 134517 F Zoo FMNH 134522 F Zoo FMNH 134512 M Zoo FMNH 57999 M Zoo - San Diego (1970) NMNH 573934 F Zoo NMNH 464991 F Zoo NMNH 395455 M National Zoo NMNH 303323 M National Zoo AMNH 183289 ? Ecuador: L. rhue?? (name or place?) No mandible

FMNH Saguinus oedipus 69941 F Colombia: Antioquia, Rio Currulao FMNH 69286 F Colombia: Cordoba, Socorre FMNH 69290 M Colombia: Sucre, Las Campanas FMNH 127390 F Zoo FMNH 127388 M Zoo FMNH 104898 F Zoo NMNH 485000 ? Colombia

NMNH F Colombia: North Central Region NMNH M Colombia: North Central Region 29

NMNH 501106 F Colombia: North Central Region NMNH S.o. geoffroyi 25313 ? Panama NMNH 240425 ? Panama: Rio Chico NMNH 257345 ? Panama Canal Zone NMNH Panama - Died San Diego Zoo Institute of 397249 M Comparative Biology FMNH 69952 F Colombia: Choco, Unguia FMNH 69953 M Colombia: Choco, Unguia FMNH 69948 F Colombia: Choco, Unguia FMNH 69946 M Colombia: Choco, Unguia

FMNH Saguinus midas 93239 M Suriname: Nickerie, Kayser Gebergte Airstrip FMNH 93515 F Suriname: Nickerie, Kayser Gebergte Airstrip FMNH 93516 F Suriname: Nickerie, Kayser Gebergte Airstrip NMNH 362118 F British Guyana: Kuitaro River NMNH Brazil: Para, Altamira, 52 km. SSW of East Bank 549521 F of Rio Xingu NMNH Brazil: Para, Altamira, 52 km. SSW of East Bank 549522 M of Rio Xingu AMNH 266480 F French Guiana: Paracou, near Sinnamary

AMNH 29

266481 F French Guiana: Paracou, near Sinnamary 3 AMNH Saguinus midas midas 148453 ? NYZS - zoo Broken skull

AMNH Saguinus midas niger 97316 M Brazil: Rio Tocantins, Cameta Olalla Bros AMNH 77693 ? Brazil: bought in Bahia

FMNH Saguinus mystax 124563 M Zoo FMNH 134479 M Zoo NMNH Peru: Department of Loreto, Cochiquinas River 543487 F near Iquitos NMNH Peru: Department of Loreto, Cochiquinas River 544382 M near Iquitos NMNH Peru: Department of Loreto, Cochiquinas River 544383 F near Iquitos NMNH Peru: Department of Loreto, Cochiquinas River 543486 F near Iquitos Skull Not Present NMNH Peru: Department of Loreto, Cochiquinas River 543488 M near Iquitos AMNH 188178 F Peru: Loreto, Rio Samiria AMNH 188176 F Peru: Loreto, Rio Samiria, Yanyaquillo No Skull, No mandible AMNH 188173 ? Peru: Loreto, Rio Samiria No skull AMNH 188171 M Peru: Loreto, Rio Samiria, Hamburgo

FMNH Saguinus tripartitus 57620 F Zoo

FMNH Saguinus leucopus 69928 F Colombia: Antioquia, Bellavista

FMNH 29

69929 M Colombia: Antioquia, Bellavista 4

FMNH F Colombia: Antioquia, Bellavista Skull Not Present (Borrowed)

69927 NMNH 292294 F National Zoo

FMNH Saguinus labiatus 38875 M Brazil: Amazonas, Rio Purus FMNH 38874 M Brazil: Amazonas, Rio Purus FMNH 121584 M Zoo FMNH 127394 M Zoo NMNH 398819 F Research Colony NMNH 398823 M Research Colony NMNH 398820 F Research Colony

FMNH Saguinus Imperator 98036 M Peru: Madre de Dios, Altamira FMNH 98035 F Peru: Madre de Dios, Altamira FMNH 124477 F Zoo

FMNH Saguinus fuscicollis 71011 F Colombia: Caqueta, Tres Troncos FMNH 71012 F Colombia: Caqueta, Tres Troncos NMNH 534806 F National Zoo Mandible Broken

FMNH S.f. fuscus 71004 M Colombia: Caqueta, Tres Troncos FMNH 29

S.f. primitivus 122013 F Brazil: Amazonas, Rio Purus

NMNH S.f. leucoginys 461267 M Peru: 59 km. West of Pucallpa NMNH S.f. illigeri 397317 F San Diego Zoo (Institute of Comparative Biology Skull Not Present NMNH 398731 ? Lab Colony - Oak Ridge Associated Universities NMNH S.f. lugonatus 522665 F Lab Colony - Rush Presbyterian St. Lukes

NMNH Saguinus nigricollis 301110 ? National Zoo NMNH San Diego Zoo - Institute of Comparative 397246 M Biology Tappen 213 F Brazil Tappen 190 F Brazil Tappen 189 M Brazil Tappen 188 M Brazil Tappen 187 M Brazil Tappen 184 M Brazil Tappen 183 F Brazil Tappen 171 F Brazil Tappen 124 M Brazil Tappen 127 F Brazil Tappen 126 F Brazil Tappen 125 M Brazil Tappen 128 M Brazil Tappen 144 M Brazil Tappen 143 ? Brazil Tappen 131 F Brazil Tappen 148 M Brazil Tappen 149 F Brazil Tappen 163 M Brazil Tappen 165 F Brazil Tappen 169 M Brazil 29

Tappen 167 M Brazil

Tappen 166 M Brazil

AMNH Callithrix humeralifer 188164 ? Aquired at zoo in Para, Brazil Broken Mandible AMNH 133692 F Brazil: Annapolis Goya No Cranium

FMNH Callithrix argentata 140355 ? Zoo NMNH 399069 M Zoo

Callithrix argentata FMNH melanura 60766 Zoo FMNH 60737 Zoo FMNH 58989 Zoo

FMNH Callithrix jacchus jacchus 20226 M Brazil: Ceara, Jua FMNH 60792 F Zoo FMNH 150725 M Zoo FMNH 60548 F Zoo NMNH 397251 F San Diego Zoo (Institute of Comparative Biology NMNH 397248 M San Diego Zoo (Institute of Comparative Biology NMNH 399037 M Zoo NMNH 399034 M Zoo

Callithrix jacchus AMNH 29

penicilatta 133698 F Brazil: Annapolis Goyaz

FMNH Callithrix jacchus geoffroyi 134473 F Zoo FMNH 134472 ? Zoo FMNH 140916 M Zoo

FMNH Cebuella pygmaea 124560 M Zoo FMNH 137074 F Zoo FMNH 104917 F Zoo FMNH 60799 F Zoo NMNH 337328 F Brazil: Amazonas, near Tabatinga No Collector? 12-Sep-1963 NMNH 337330 F Brazil: Amazonas, near Tabatinga No Collector? 15-Sep-1963 NMNH No Collector? 04-Sep-1963 (Skull 337322 M Brazil: Amazonas, near Tabatinga Bisected) NMNH Brazil: Amazonas, near Tabatinga (Wild Caught- Caught Jan-1963; Died April- 336325 M Died in captivity 4 months later 1963 NMNH 337319 M Brazil: Amazonas, near Tabatinga No Collector? 02-Sep-1963

Leontopithecus FMNH chrysomelas 186914 F Zoo NMNH F Zoo Skull Not Present NMNH M Zoo Skull Not Present

NMNH M Zoo Skull Not Present 29

NMNH ? Zoo Skull Not Present 8

NMNH F Zoo Skull Not Present

Leontopithecus rosalia FMNH rosalia 145563 M Zoo FMNH 180668 M Zoo FMNH 57839 M Zoo FMNH 129350 M Zoo FMNH 57152 F Zoo FMNH 134506 F Zoo FMNH 134505 F Zoo NMNH 269905 F National Zoo NMNH 546317 F National Zoo NMNH 546322 F National Zoo AMNH 235275 ? No Data AMNH 137278 ? No Data, Dealer bought

NMNH Brazil: Between Bana do Bugres and Rio do Allouatta caraya 270355 M Caceres NMNH 270357 F Brazil: 100 miles south of San Luiz do Caceres AMNH 209917 M Bolivia: Dept. Beni, Machupo river mouth 8kgs AMNH 211495 F Bolivia: Dept. Beni, 8 km N. Exaltacion

AMNH

211496 M Bolivia: Dept. Beni, 8 km N. Exaltacion 29

AMNH F Bolivia: Dept. Beni, 8 km. N. Exaltacion 9

211497 AMNH 211499 M Bolivia: Dept. Beni, 8 km N. Exaltacion AMNH 211498 M Bolivia: Dept. Beni, 8 km N. Exaltacion AMNH 211502 F Bolivia: Dept. Beni, 8 km N. Exaltacion AMNH 211501 F Bolivia: Dept. Beni, 8 km N. Exaltacion AMNH 211507 F Bolivia: Dept. Beni, Puerto Caballo AMNH Bolivia: Dept. Beni, Mamare River 12 degrees 211504 M 26' S AMNH 211508 M Bolivia: Dept. Beni, Puerto Caballo AMNH 211512 F Bolivia: Dept. Beni, Puerto Caballo AMNH 211517 ? Bolivia: Dept. Beni, 15 km SW San Joaquin

NMNH Brazil: Rio Grande do Sul, Sao Joao do Monte Allouatta fusca 49619 F Negro Skull Not Present (Borrowed) NMNH Brazil: Rio Grande do Sul, Sao Joao do Monte 49618 F Negro Skull Not Present (Borrowed)

NMNH British Guyana: Rupununi District, 60 miles East Allouatta seniculus 361017 M of Dadanawa NMNH 395068 M British Guyana: Rupununi District AMNH 211531 F Bolivia: Dept. Beni, 5km SE Coimbra Brazil AMNH 211528 M Bolivia: Dept. Beni, 5km SE Coimbra Brazil Broken Zygo AMNH 211527 F Bolivia: Dept. Beni, 5km SE Coimbra Brazil

300

Allouatta seniculus FMNH seniculus 69591 M Colombia: Choco, Unguia FMNH 18869 M Colombia: Guanaca NMNH 123517 F Colombia: Magdalena, Bondo AMNH 23378 F Colombia: Magdalena, Bonda AMNH 99657 F Colombia: AMNH 23342 ? Colombia: Magdalena, Bonda AMNH 23351 ? Colombia: Magdalena, Bonda AMNH 188006 F Peru: Loreto, Rio Samiria Allouatta seniculus AMNH straminea 42316 F Guyana: Kartabo AMNH 42313 M Guyana: Kartabo AMNH 69591 M Venezuela: Latel AMNH 132790 M Venezuela: Paleuque, San Miguel AMNH 30193 M Venezuela: Rio Mateo

Allouatta seniculus FMNH insulans 61857 M Trinidad: Brickfield FMNH 61855 F Trinidad: St. Andrew, Mt. Harris

FMNH Allouatta palliata palliata 57119 M Honduras: Cortes, Lake Ticamaya

FMNH 30

22395 F Honduras: Cortes, San Pedro 1

NMNH 282798 ? El Salvador: Cortes Province Allouatta palliata NMNH (aequatorealis) 543117 M Panama: Barro Colorado Island NMNH 240410 M Panama: Darien, Rio Chununaque near Saltea NMNH 240407 M Panama: Darien, Rio Chununaque Skull Not Present (Borrowed) NMNH 338104 F Panama: Darien, Cerro Mali NMNH 338105 M Panama: Darien, Cerro Mali (4500 ft.) NMNH 338106 M Panama: Darien, Cerro Mali (4500 ft.) NMNH 338109 M Panama: Darien, Cerro Mali (4500 ft.)

AMNH Allouatta belzebul 95758 F Brazil: Rio Tapojoz, Limaal Olalla Bros AMNH 133544 M Annapolis Goyaz AMNH 133879 M Brazil: Para, Fordlandia AMNH 133532 M Brazil: Para, Fordlandia

FMNH Ateles fusciceps fusciceps 93102 M Ecuador: Pichincha, Mindo FMNH Ateles fusciceps robustus 68820 M Colombia: Cordoba, Catival FMNH 68823 M Colombia: Cordoba, Catival FMNH 68822 M Colombia: Cordoba, Catival FMNH 68810 M Colombia: Cordoba, Sucre Las Companas 30

NMNH 338113 F Panama: Darien, Cerro Tacaruna (4100 ft.) NMNH 338111 F Panama: Darien, Cerro Mali (4700 ft.) Skull Not Present NMNH 338112 M Panama: Darien, Cerro Mali (3500 ft.) NMNH 338115 M Panama: Darien, Cerro Tacaruna (4200 ft.) NMNH 338114 F Panama: Darien, Cerro Tacaruna (4200 ft.) NMNH 338116 F Panama: Darien, Cerro Tacaruna (4100 ft.)

NMNH Ateles geoffroyi 276631 F Mexico: Veracruz, San Juan Evangelista NMNH 244863 F Guatemala: Peton, Libertad AMNH Ateles geoffroyi frontatus 28418 F Nicaragua: Matagalpa, Luma No Skull AMNH 28420 M Nicaragua: Lauala No Skull AMNH Ateles geoffroyi vellerosus 172985 ? Mexico: Oaxaca, Tapamatepec No Skull

FMNH Ateles paniscus paniscus 93244 F Suriname: Nickerie, Kayser Gebergte Airstrip FMNH 95498 F Suriname: Nickerie, Wilhemina Mts.

Ateles (sp.) Tappen 155 ? Sucre, Bolivar, Barranquilla, Colombia Tappen 154 ? Sucre, Bolivar, Barranquilla, Colombia Tappen 153 ? Sucre, Bolivar, Barranquilla, Colombia Tappen 152 F Sucre, Bolivar, Barranquilla, Colombia Tappen 151 ? Sucre, Bolivar, Barranquilla, Colombia

Lagothrix lagothricha FMNH 30

3 cana 98050 M Peru: Cuzco, Hacienda Cadena

FMNH 98052 F Peru: Cuzco, Hacienda Cadena FMNH 98054 M Peru: Madre de Dios, Rio Manu FMNH 98055 M Peru: Madre de Dios, Rio Manu AMNH 70404 M Zoo

Lagothrix lagothricha FMNH lagothricha 70591 F Colombia: Putumayo, Rio Mecaya FMNH 70597 M Colombia: Putumayo, Rio Mecaya FMNH 70593 F Colombia: Putumayo, Rio Mecaya NMNH 397774 F National Zoo AMNH 35752 M Zoo, NYZS

Lagothrix lagothricha FMNH lugens 70584 F Colombia: Huila, San Augustin FMNH 70574 M Colombia: Huila, Rio Aguas Claras FMNH 70576 M Colombia: Huila, Rio Aguas Claras NMNH 311217 M National Zoo

Lagothrix lagothricha AMNH poeppigii 188153 F Peru: Loreto, Rio Samiria, yanayaquillo AMNH 188156 F Peru: Loreto, Rio Samiria, yanayaquillo

Brachyteles arachnoides AMNH 260 ? Brazil: Verreaux college partially broken zygo 4

305

Appendix 2