Associations Between Skeletal Fractures and Locomotor Behavior, Habitat Use, and Body Mass in Nonhuman Primates

Associations between Skeletal Fractures and Locomotor Behavior, Habitat Use, and Body Mass in Nonhuman Primates

DISSERTATION

Presented in Partial Fulfillment of the Requirements for the Degree Doctor of Philosophy in the Graduate School of The Ohio State University

Heather Jarrell, B.A., MSc

Graduate Program in Anthropology

The Ohio State University

2011

Dissertation Committee:

W. Scott McGraw, Advisor

Clark Larsen

Jeffrey McKee

Sam Stout

Charlotte Roberts

Heather Jarrell

2011

ABSTRACT

Injuries sustained during falls from heights may be the most frequent cause of long bone trauma among nonhuman primates. Yet the interrelatedness of trauma and positional behaviors is poorly understood. The purpose of this study is to assess how common locomotor behaviors, broad habitat use tendencies, and body mass are associated with skeletal fracture frequencies in primates. Primates exhibiting a higher degree of arboreality should exhibit greater fracture frequencies than more terrestrial primates due to their greater risk of obtaining injuries in falls from heights. Similarly, primates whose locomotor repertoire includes more specialized behaviors should exhibit higher frequencies than those of more generalized quadrupeds. Falls sustained by primates commonly active higher in the canopy and larger primates should be more likely to show severe repercussions (as depicted by higher fracture frequencies) than primates active closer to the ground and smaller primates.

Fractured long bones from primates encompassing twenty-two taxonomic groups housed at The Ohio State University, Cleveland Museum of Natural History, American

Museum of Natural History, National Museum of Natural History, and the Caribbean

Primate Research Center were examined macroscopically and radiographically.

Locomotor and habitat use profiles for each taxonomic group were developed based upon quantitative field observations in the primatological literature.

ii Fracture patterns appear to be most closely associated with locomotor mode, followed by arboreality, vertical distribution, and body mass, although each of these variables are interconnected. Locomotor mode preferences strongly correlate with fracture frequencies. As expected, suspensory primates exhibit the highest fracture frequencies, although leapers have the lowest frequencies. The locations of fractures are significantly correlated with some aspect of every variable examined. When suspensory primates break a bone, it tends to be either the humerus or femur. Small- or medium- sized, arboreal quadrupeds are more likely to fracture their tibia or fibula than another long bone, whereas large and very large quadrupeds tend to fracture any long bone preferentially except for the tibia or fibula. Fracture occurrences in leaping primates tend either to involve the clavicle preferentially or are independent of location. Factors contributing to intraspecific variation in fracture frequencies, including the impact of sex, age, and changing population pressures, may contribute to differential fracture distributions. Combining skeletal samples with behavioral observations from individuals‟ life histories highlights the under-representation of fractures in field studies as well as over-estimates of the degree to which fractures impair mobility.

The fact that fracture frequencies and patterns revealed in this study are associated with locomotor and positional behaviors appears to highlight the importance of risk avoidance in primate evolution. Skeletal trauma may affect reproductive fitness either directly or incidentally. Consequently, primates should be under selective pressure to avoid the risk of obtaining fractures, developing behavioral and anatomical mechanisms to reduce the number and severity of falls from heights. Further analyses of the anatomical distribution of fractures in primates may reveal selective factors shaping

iii locomotor anatomy. Ultimately, the analysis of fractures in primates which have healed under natural conditions may lead to a greater understanding of the origins of medical intervention in humans.

Dedicated to Mom and Dad.

ACKNOWLEDGMENTS

I would like to express my appreciation to all the individuals who have helped make the completion of this research possible, especially the members of my committee:

Drs. Scott McGraw, Clark Larsen, Sam Stout, and Jeff McKee from the Ohio State

University and Dr. Charlotte Roberts from the University of Durham, United Kingdom.

Dr. Paul Sciulli‟s input regarding statistical analyses has been invaluable. Dr. Donna

McCarthy-Beckett was my Graduate Faculty Representative and I thank her for her time and imput. Special thanks go to my advisor, Dr. McGraw, for all of his guidance throughout my tenure at OSU. Thank you for everything.

Financial support was partially provided by the Ohio State University Alumni

Grant for Graduate Research and Scholarship (AGGRS). I would like to thank Dr.

Larsen for use of the NOMAD Portable X-ray system, provided through an equipment purchase via the Larsen Research and Travel Fund. Research at the Laboratory for

Primate Morphology and Genetics was supported by the National Institutes of Health

(grant # P40 RR003640) to the Caribbean Primate Research Center.

I would like to thank all of the institutions which have housed the skeletal collections analyzed in this study. Lyman Jellema (Department of Physical

Anthropology at the Cleveland Museum of Natural History [CMNH]), Darren Lunde and

Eileen Westwig (Department of Mammalogy at the American Museum of Natural

vi History [AMNH]), Linda Gordon (Department of Mammals at the National Museum of

Natural History [USNM]), Dr. Edmondo Kraiselburg (Director of the Caribbean Primate

Research Center [CPRC]), Dr. Donald Dunbar (Director of the Laboratory for Primate

Morphology and Genetics [LPMG]), and Dr. Scott McGraw (OSU) all provided access to their respective collections.

Dr. Christopher Ruff (Johns Hopkins University School of Medicine) and Evan

Garofalo‟s assistance in transporting the NOMAD X-ray system and providing instruction in its use has been much appreciated. Lyman Jellema (CMNH), Eileen

Westwig (AMNH), Dr. Barbara Brown (Department of Ichthyology at the AMNH), and

Jeremy Jacobs (Division of Mammals at the USNM) all provided use of and/or assistance with radiographic equipment and darkroom facilities at their respective institutions.

I am grateful for the efforts of everyone involved in the running and maintenance of all the divisions of the Caribbean Primate Research Center. I am especially thankful both to Dr. Dunbar, for all of the assistance he provided both during and after the application process, and to Dr. Terry Kensler (Lab Manager of the LPMG), for going above and beyond in making sure not only that I had everything I needed at the lab but also that I was fitting in well in Puerto Rico – even gifting me with a birthday cake! I would like to thank Myriam Vi ales, Dr. Bob Kensler, Dr. Jean Turnquist, and Pizarro for their support at the LPMG. I also would like to thank Dr. Janis Gonzalez and Dr.

H ctor P rez for the information they provided at the Sabana Seca Field Station. Thanks go to James Ayala (Colony Manager of the Cayo Santiago Field Station [CSFS]) and Dr.

Adaris Mas-Rivera (Resident Scientist at the CSFS), for allowing my visit to the Cayo

vii Santiago breeding colony. Census Takers Edgar Davila and Giselle Caraballo provided valuable insight into the behaviors of the current and past CSFS colony.

Finally, thanks go to my family and friends, most of all to my parents, J.W.,

Shelly, and Tommy, who took it in turns to placate and berate, empathize and question as the situation called for it, and who believe in me, always.

viii

VITA

2001 ...... B.A. Scholars Anthropology, Northwestern

State University

2003 ...... MSc Human Osteology & Palaeopathology,

University of Bradford, United Kingdom

2000 to 2002 ...... Field Crew and Geophysical Technician,

Louisiana National Guard and National

Forest Surveys

2001 to 2002 ...... Laboratory Supervisor, Cultural Resource

Office, Northwestern State University

2004 to 2009 ...... Graduate Teaching Associate, Department

of Anthropology, The Ohio State University

2009 to 2010 ...... Lecturer, Department of Anthropology, The

Ohio State University

ix PUBLICATION

Jarrell H, Hailey TI. 2002. The Fort Jesup Hospitals: Historical, Geophysical, and Archaeological Investigations. In: Morgan N, Shatwell J, editors. Archaeology, Interpretation, and Management in Cane River National Heritage Area. Natchitoches: Cane River National Heritage Area Commission. p 32-44.

FIELD OF STUDY

Major Field: Anthropology

Minor Field: Anatomy

TABLE OF CONTENTS

ABSTRACT……………………………………………………………………....……………….ii DEDICATION………………..………………...……………………………………………….v ACKNOWLEDGEMENTS…………………………………….……………………………………………………….vi VITA………………………………………..………………..………………….…………………………….ix LIST OF TABLES…………………………………………...…………………………………………….xiv LIST OF FIGURES…………………………………..…………………………………………………….xvi

1 CHAPTER 1: Introduction……………………………………………………………….1

1.1 Project summary……………………………………………………………….1 1.2 Hypotheses……………………………………………………………………...……………….4

2 CHAPTER 2: Research Background……………………………………………………………….11

2.1 Bone and fracture biology……………………………………………………………….11 2.1.1 Biomechanical characteristics of fractures……………………………………………………………….13 2.1.2 Fracture healing……………………………………………………………….19 2.1.3 Nonhuman primates as models of fracture repair……………………………………………………………….28 2.2 Fracture studies……………………………………………………..……………………….30 2.2.1 Previous studies involving fractures in human skeletal assemblages……………………………………………………………….32 2.2.2 Previous studies involving fractures in primate skeletal assemblages………….37 2.3 Field studies of primate positional behavior……………………………………………………………….44 2.3.1 Generalizing and comparing positional behavior……………………………………………………………….45 2.3.2 Limitations to assigning positional behavior classifications………………….…….51 2.3.3 Positional behavior for each representative species……………………………………………………………….56 2.4 Chapter summary……………………………………………………………….120

xi 3 CHAPTER 3: Materials and Methods……………………………………………………………….122

3.1 Inventory of museum samples……………………………………………………………….122 3.2 Macroscopic analyses……………………………………………………………….125 3.3 Radiographic analyses……………………………………………………………….127 3.4 Behavioral observations of Cayo Santiago-derived macaques……………………………………………………………….129 3.5 Development of positional behavior profile……………………………………………………………….131 3.6 Statistical analyses……………………………………………………………….144 3.7 Chapter summary……………………………………………………………….153

4 CHAPTER 4: Results……………………………………………………………….154

4.1 Descriptive data……………………………………………………………….154 4.1.1 Demographic comparisons……………………………………………………………….155 4.1.2 Assessment of fracture healing……………………………………………………………….180 4.1.3 Comparative populations……………………………………………………………….187 4.2 Associations of fracture frequencies with positional behavior……………………………………………………………….189 4.2.1 Fractures and arboreality……………………………………………………………….196 4.2.2 Fractures and height above ground……………………………………………………………….198 4.2.3 Fractures and locomotor mode preferences……………………………………………………………….203 4.2.4 Fractures and body mass……………………………………………………………….208 4.2.5 Fractures and positional behavior, controlling for body mass……………………………………………………………….212 4.2.6 Associations between fractures and positional behavior……………………………………………………………….226 4.3 Impact of intraspecific factors at Cayo Santiago……………………………………………………………….232 4.4 Chapter summary……………………………………………………………….237

5 CHAPTER 5: Discussion……………………………………………………………….238

5.1 Impact of arboreality on fracture frequencies…………………………………….238 5.2 Impact of height above ground on fracture frequencies……………………….241 5.3 Impact of locomotor mode on fracture frequencies……………………………………………………………….243 5.4 Impact of size/body mass on fracture frequencies……………………………………………………………….246 5.5 Impact of intraspecific factors on fracture frequencies……………………………………………………………….248 5.6 Linking behavior and morphology – Cayo Santiago case studies……………………………………………………….253 5.7 Implications for primate evolution…………………………………………….256 5.8 Future research………………………………………………………...……………………….264 5.9 Chapter summary……………………………………………………………….267

xii 6 CHAPTER 6: Conclusions……………………………………………………………….268

REFERENCES………………………………….……………………………………………………….272 APPENDIX A: Scoring criteria for data collection……………………………………295 APPENDIX B: Raw data……………………………………………………………..……303 APPENDIX C: Timing of fracture repair – case studies at Cayo Santiago………………….…315

xiii

LIST OF TABLES

2 CHAPTER 2: Research Background

2.1 Fracture frequencies in comparative populations (full skeleton) …………...…..10041 2.2 Fracture frequencies in comparative populations (long bones only) ………..…..10042 2.3 Comparison of the degree of arboreality in primates………………………...…..10061 2.4 Comparison of the height above ground frequencies in primates………………..10064 2.5 Comparison of locomotor mode frequencies in primates………………………..10068

3 CHAPTER 3: Materials and Methods

3.1 Survey of primate skeletons examined in this investigation……………………..100124 3.2 Comparison of locomotor classifications in primates…………………………....100132

4 CHAPTER 4: Results

4.1 Comparison of fracture frequencies by species…………………………………..100157 4.2 Comparison of fracture frequencies by element……………………………..…..100158 4.3 Comparison of fracture frequencies by sex (by cross %) ……………….….…..100162 4.4 Comparison of fracture frequencies by sex (by individual %) ………………..…..100163 4.5 Chi square statistics for sex classes fracture frequencies (cross %) …………………………….164 4.6 Chi square statistics for sex classes fracture frequencies (individual %) …………………….165 4.7 Statistics for the MCA (Taxa*Element*Type)………………………………….178 4.8 Direction of angulation of distal fractured bone ends…………………………....100184 4.9 Chi square statistics for comparative collections fracture frequencies……...…...100189 4.10 Correlation statistics for fracture patterns versus positional behavior…………...100195 4.11 Correlation matrix eigenvalues, eigenvectors for FXp1*ARB*M…………..…..100214 4.12 Correlation matrix eigenvalues, eigenvectors for FXp2*ARB*M……………....100215 4.13 Correlation matrix eigenvalues, eigenvectors for FXp1*HAGp1*M……….…...100217 4.14 Correlation matrix eigenvalues, eigenvectors for FXp2*HAGp1*M……….…...100218 4.15 Correlation matrix eigenvalues, eigenvectors for FXp2*HAGp3*M……….…...100219 4.16 Correlation matrix eigenvalues, eigenvectors for FXp3*HAGp3*M……….…...100220 4.17 Correlation matrix eigenvalues, eigenvectors for FXp1*LOCp1*M………….....100222

xiv 4.18 Correlation matrix eigenvalues, eigenvectors for FXp3*LOCp1*M………….....100223 4.19 Correlation matrix eigenvalues, eigenvectors for FXp2*LOCp2*M………….....100224 4.20 Correlation matrix eigenvalues, eigenvectors for FXp3*LOCp2*M………….....100225 4.21 Correlation matrix eigenvalues, eigenvectors for F*A*L*H*M………………………….....100228 4.22 Correlation matrix eigenvalues, eigenvectors for A*H*L*M………………………..…..100231 4.23 Sex/age categories of Cayo Santiago fracture frequencies (cross %)…………....100234 4.24 Sex/age categories of Cayo Santiago fracture frequencies (individual %)……....100234 4.25 Comparison of fracture frequencies before and after provisioning…………..…..100236

LIST OF FIGURES

2 CHAPTER 2: Research Background

2.1 Basic forces acting on bone…………………………………………………………………………...15 2.2 Common types of fractures……………………………………………………………………….….17 2.3 Effects of basic forces on characteristic fracture patterns……………………………………………………………………….….19 2.4 Bone modeling by drifts…………………………………………………………………….……..21 2.5 Bone remodelling……………………………………………………………………….…23 2.6 Stages of fracture healing…………………………………………………………………….……..25 2.7 Typical nonhuman primate locomotor behaviors……………………………………………………………………….….47 2.8 The diverse locomotor repertoire of the primates…………………………………………………………………….……52 2.9 Survey of primates examined in this paper……………………………………………………………………….…..57 2.10 Survey of primates examined in this paper, cont…………………………………………………………………….……..58 2.11 Survey of primates examined in this paper, cont…………………………………………………………………….…….59 2.12 Survey of primates examined in this paper, cont…………………………………………………………………….…….60

3 CHAPTER 3: Materials and Methods

3.1 Degree of arboreality profiles………………………………………………………………………….135 3.2 Height above ground profiles………….……………………………………………………………….138 3.3 Height above ground profiles, cont. ………….……………………………………………………………….139 3.4 Locomotor mode profiles ………….……………………………………………………………….140 3.5 Locomotor mode profiles, cont. ……………………………………………………………………….141 3.6 Body mass profiles……………………………………………………………….143 3.7 Height above ground frequencies PCA…………………………………………..100146 3.8 Locomotor mode frequencies PCA…………………………………………..…..100147 3.9 Scatter plot of the height above ground PCA first and second axes……………..100149 3.10 Scatter plot of the locomotor modes PCA first and second axes………….……..100151

4 CHAPTER 4: Results

4.1 Comparison of fracture frequencies by element………………………………………………………………………….159 4.2 Comparison of fracture frequencies by element, cont. ………………………………………………………………………….160 4.3 Fracture distribution by sex………….……………………………………………………………….166

xvi 4.4 Fracture distribution by age………….……………………………………………………………….168 4.5 Fracture distribution by side………………………………………………………………………….169 4.6 Fracture distribution by limb…………..……………………………………………………………….170 4.7 Fracture distribution by bone level…………………………………………………………………….172 4.8 Comparison of fracture frequencies by fracture type………………...…………..100174 4.9 Comparison of fracture frequencies by fracture type, cont. ……………………..100175 4.10 Plot of multiple correspondence analysis…………………………………….…..100177 4.11 Frequency of callus formation……………………………………………..……..100181 4.12 Frequency of sclerosis of bone ends……………………………………………..100181 4.13 Extent of apposition of bone ends………………………………………………..100183 4.14 Proportion of bone shortening………………………………………………..…..100185 4.15 Pan troglodytes humerus with overlap, apposition, and angulation……………………………………….………..100185 4.16 Frequency of fractures with localized periosteal reaction present……………………………………….………..100187 4.17 Element fracture frequencies PCA……………………………………...………..100190 4.18 Scatter plot of the fracture PCA first and second axes…………………………..100193 4.19 Fracture (Prin2) x arboreality correlation………………………………………..100197 4.20 Fracture (Prin1) x height above ground (Prin1) correlation……………………..100199 4.21 Fracture (Prin2) x height above ground (Prin1) correlation……………………..100200 4.22 Fracture (Prin2) x height above ground (Prin3) correlation……………………..100201 4.23 Fracture (Prin3) x height above ground (Prin3) correlation……………………..100202 4.24 Fracture (Prin1) x locomotor mode (Prin1) correlation……………………….....100204 4.25 Fracture (Prin2) x locomotor mode (Prin2) correlation……………………...…..100205 4.26 Fracture (Prin3) x locomotor mode (Prin1) correlation……………………...…..100206 4.27 Fracture (Prin3) x locomotor mode (Prin2) correlation……………………….....100207 4.28 Fracture (Prin2) x body mass (log of average) correlation…………………..…..100209 4.29 Fracture (Prin2) x body mass (sexual dimorphism) correlation……………..…..100210 4.30 Fracture (Prin3) x body mass (log of average) correlation…………………..…..100211 4.31 Fracture (Prin1) x mass x arboreality PCA………………………………..……..100214 4.32 Fracture (Prin2) x mass x arboreality PCA…………………………………..…..100215 4.33 Fracture (Prin1) x mass x height above ground (Prin1) PCA………………….……..100217 4.34 Fracture (Prin2) x mass x height above ground (Prin1) PCA………………….……..100218 4.35 Fracture (Prin2) x mass x height above ground (Prin3) PCA…………………….…..100219 4.36 Fracture (Prin3) x mass x height above ground (Prin3) PCA…………………….…..100220 4.37 Fracture (Prin1) x mass x locomotor mode (Prin1) PCA…………………….…..100222 4.38 Fracture (Prin3) x mass x locomotor mode (Prin1) PCA…………………….…..100223 4.39 Fracture (Prin2) x mass x locomotor mode (Prin2) PCA………………………...100224 4.40 Fracture (Prin3) x mass x locomotor mode (Prin2) PCA…………………….…..100225 4.41 Full PCA (FXp1*A* HAGp1*LOCp1*M)…………………………………...... 227 4.42 Positional behavior PCA (A*HAGp1*LOCp1*M) ……………………………..100231 4.43 Fracture distribution by sex and age at Cayo Santiago…………………………..100235

xvii 5 CHAPTER 5: Discussion

5.1 Severe skeletal injury in primate observed to 'limp a little'……………………..100255

C APPENDIX C: TIMING OF FRACTURE REPAIR

C.1 Photograph of CPRC 3916 fracture……………………………………….……..100316 C.2 Radiographs of CPRC 3916 fracture……………………………………………..100316 C.3 Photograph of CPRC 4188 fracture……………………………….……………..100318 C.4 Radiographs of CPRC 4188 fracture……………………………………………..100319 C.5 Photograph of CPRC 3307 fracture……………………………………….……..100321 C.6 Radiographs of CPRC 3307 fracture…………………………….………..……..100322 C.7 Photograph of CPRC 3372 fracture……………………………………………..100323 C.8 Radiographs of CPRC 3372 fracture……………………………………………..100324 C.9 Photograph of CPRC 3393 fracture……………………………………….……..100325 C.10 Radiographs of CPRC 3393 fracture……………………………………………..100326

xviii

CHAPTER 1: Introduction

1.1 Project summary

The purpose of this study is to assess associations between skeletal fracture frequencies and common locomotor behaviors, habitat use preferences, and average body mass in primates. The impacts on fracture frequencies of four general factors are assessed both independently and combined in a positional behavior profile. First, fracture frequencies should be positively correlated with arboreality due to the greater risk of obtaining injuries in falls from heights. Second, fracture frequencies should be positively correlated with height above ground preferences due to the greater risk of obtaining injuries in longer falls. Third, fracture frequencies should be positively correlated with more specialized locomotor behaviors (e.g., leaping or brachiation) than generalized quadrupedalism due to the greater opportunities for unsuccessful maneuvers to result in injuries. Fourth, fracture frequencies should be positively correlated with increased body mass due to the greater risk for larger primates to obtain injuries in falls than smaller primates.

Long bones (clavicles, humeri, radii, ulnae, femora, tibiae, and fibulae) from 1672 nonhuman primates encompassing twenty-two taxonomic groups were analyzed for the

1 presence of fractures. Primates were housed at The Ohio State University in Ohio,

Cleveland Museum of Natural History in Ohio, American Museum of Natural History in

New York, National Museum of Natural History in Washington, D.C., and the Caribbean

Primate Research Center in Puerto Rico. Each fracture was examined macroscopically and radiographically. Macroscopic examination included descriptions of fracture type, fracture location, extent of healing, overlap, any associated trauma or infection, and available demographic information. Perimortem fractures, often associated with gunshot wounds in wildshot primates, were not included in this study. Radiographic examination included descriptions of callus formation, sclerosis, angulation, apposition, and revised fracture type. Full locomotor and habitat use profiles of each primate taxon were created, based upon quantitative field observations culled from the literature. The profile for each taxon included the following information: degree of arboreality, height above ground frequencies (in 5 meter increments), locomotor mode frequencies (frequency of locomotion categorized as quadrupedalism or bipedalism, climbing, leaping or bridging, and suspension or dropping), and average body mass. All statistical tests were performed using SAS 9.2, including chi square tests, multiple correspondence analysis, Pearson‟s correlations, and principle components analyses.

Most fractures healed fairly well, with minimal deformity and few complications.

Pongo pygmaeus (29.79%) and Procolobus badius (27.69%) exhibited the highest frequencies of fractures. The most commonly fractured element when comparing fracture frequencies of all elements in all taxa is the fibula in Leontopithecus rosalia

(7.04%) and Cebus apella (6.62%). A multiple correspondence analysis of fracture type

2 2 and location for each taxon reveals clustering among the dataset (overall χ 1024 =

9605.94).

Most of the sampled primates do not exhibit long bone fractures; however, the locations of fractures present do appear to be associated with locomotor behaviors, habitat use preferences, and mass. Overall fracture frequencies were only significantly correlated with locomotor mode preferences when examined independently of other factors, although fracture frequencies per element were significantly correlated with some aspect of each positional profile. As expected, suspensory primates exhibited the highest fracture frequencies; in contrast, leapers exhibited the lowest frequencies, probably because the sampled leapers tended to be small-bodied. The results of principle components analyses suggest that fracture patterns are most closely associated with locomotor mode, followed by arboreality, vertical distribution, and body mass, although each of these variables are interconnected. Five clusters are revealed: 1. When suspensory primates break a bone, it tends to be either the humerus or femur. 2.

Small/medium, low travelling height quadrupeds are associated with tibial and fibular fractures. Conversely, 3. large arboreal quadrupeds and 4. terrestrial quadrupeds are likely show a preference for fracturing any long bone except for their tibia or fibula. 5.

Fracture occurrences in small/medium, climbing or leaping, low travelling height primates tend either to involve the clavicle preferentially or are independent of location.

Avoidance of injuries and compensating for loss of movement once injuries occur has played a significant role in primate evolution (Munn, 2006). Arboreal primates face a number of challenges to maintaining their balance on fragile branches (Cant, 1992).

Consequently, primates have adapted to a range of locomotor behaviors to avoid the risk

3 of falling from heights (Pontzer and Wrangham, 2004). Falls resulting in injury are likely to have more severe repercussions in larger primates, as primates with a comparatively larger body mass must dissipate greater amounts of kinetic energy caused by the fall

(Radasch, 1999). Although injuries sustained during falls may be the most frequent cause of long bone trauma among primates (Lovell, 1991; Jurmain, 1997; Carter, et al,

2008), the interrelatedness of trauma and positional behaviors is poorly understood. The primate order offers the most diverse set of locomotor behaviors of all mammals. The fact that primates move in vastly different ways and are exposed to unique dangers involved with such movements, makes them vulnerable to fractures in varying degrees.

This study addresses that issue by examining fracture patterns in primates covering a wide spectrum of positional behaviors, allowing for the synergism of arboreality, height above ground preferences, locomotor mode frequencies, and body mass among primate taxa.

1.2 Hypotheses

The primate order offers the most diverse set of locomotor behaviors of all mammals. Primates have evolved an impressive number of adaptations to meet the demands of locomotion (Fleagle, 1999); however, these same solutions contribute to the development of vulnerabilities that place primates at risk of obtaining fractures. The fact that primates across such a wide size spectrum move in such vastly different ways and

4 are exposed to different dangers involved with them, from arboreal quadrupeds to terrestrial quadrupeds, from leapers to suspensory primates, makes them vulnerable to fractures in varying degrees. The objective of this research is to test the thesis that primate locomotor behaviors, habitat use preferences, and body size affect fracture patterns and healing. Several hypotheses have been formulated to address this thesis.

First, each of the hypotheses below will be tested independently of each other, to assess the impact on fracture frequencies among primates based solely on one factor: arboreality, height above ground, locomotor mode, or body mass. Second, because realistically the impact of body mass on habitat use and locomotor preference cannot be disregarded, as well as the impact of body mass on the intensity of a potential fall, each hypothesis (arboreality, height above ground, locomotor mode) will be tested in combination with body mass. Third, the impact of all examned factors on fracture frequencies will be tested together, in order to assess which factors are most influential to fracture risk.

Degree of arboreality hypothesis: Arboreal primates will have a greater risk of receiving fractures than terrestrial primates.

I predict that fracture frequencies should be positively correlated with arboreality due to the greater risk of obtaining injuries in falls from heights. Because arboreal primates move in the canopy more often and presumably more often face dangers there, it is hypothesized that they will be more likely to fall to the ground, receiving fractures.

Alternatively, terrestrial primates might experience fractures from falls on those

5 occasions when they travel in the canopy, due to being less familiar with the environment. Lovell (1991) has suggested as such, based on fractures in baboons. To examine this hypothesis, I will test for correlations between fracture frequencies and degree of arboreality. Published studies will be used to determine the degree of arboreality for each taxa.

Height above ground hypothesis: Primates ranging at increased heights above the ground (higher in the canopy) will have a greater risk of receiving fractures should they fall than primates which are more often observed close to the ground.

I predict that fracture frequencies should be positively correlated with height from the ground (or canopy level) due to the greater risk of obtaining injuries in longer falls than in shorter falls. The further from the ground one is, the more likely that a fall will result in serious injury. Based on the conservation of energy, height and kinetic energy are positively correlated as an object falls from rest. Consequently, longer falls result in greater impact forces. It is possible that primates commonly occupying extremely high vertical distributions would be more likely to die immediately from their injuries, meaning that no healing would be present in the skeleton. However, Schultz (1956,

1967) classically remarked on the ability of gibbons to fall from extreme heights and survive with remarkably well-healed fractures. To test this hypothesis, I will determine whether a correlation exists between fracture frequencies and height/canopy use. Height above ground frequencies will be determined based upon behavioral data from published sources.

6 Locomotor mode hypothesis: Primates which more commonly practice riskier locomotor modes will have a greater risk of receiving fractures than primates which more often utilize less risky locomotor behaviors.

I predict that fracture frequencies should be positively correlated with more specialized locomotor behaviors (e.g., leaping or brachiation) due to the greater opportunities for unsuccessful maneuvers to result in injuries. It is assumed that leaping and suspensory behaviors involve more risk of falling compared to generalized arboreal quadrupedalism. While primates do have a diverse locomotor repertoire, they often have been grouped into categories based on common locomotor modes for comparative research purposes. For the present study, frequencies with which common locomotor behaviors as described by Hunt (1996) and obtained from published sources for each species will be tested for correlations with fracture frequencies.

Average body mass hypothesis: Larger primates will have a greater risk of receiving fractures than smaller primates independent of positional behaviors.

I predict that fracture frequencies should be positively correlated with increased average body mass due to the greater risk for larger primates to obtain injuries in falls.

Primates with a larger average body mass have more difficulty moving in the canopy and absorb more energy when they do fall to the ground (Fleagle, 1999). The kinetic energy of an object just prior to impact as it falls from rest is dependent upon its mass, the gravitational acceleration of the earth, and the height above the surface of the earth from

7 which it is falling. As mass increases, so does kinetic energy, which in turn increases the impact force. Smaller leaping primates will be able to find more supports able to sustain their leaps; however, they also have greater distances to jump between supports (Fleagle,

1999). To test this hypothesis, fracture frequencies will be tested for correlations with behavioral data on average body mass based on previously published data from Smith and Jungers (1997).

Interdependence of variables hypotheses

In addition to testing whether correlations exist between fracture frequencies and each of the above factors independently of each other (arboreality, height above ground, locomotor mode, and body mass), it also will be determined whether correlations exist between fracture risk and habitat/locomotor profiles when controlling for size. For instance, a large primate falling from a height of 15 meters will have a greater fracture risk than a small primate falling from the same height, due to greater forces impacting the skeleton. Furthermore, the association between fracture frequencies and the entire habitat/locomotor profile of the primates will be assessed through principal component analysis, in order to explain which variables explain the most of the variance seen among primate fracture frequencies.

8 Intraspecific factors hypotheses: the case study of Cayo Santiago

Along with assessing the impact of size and positional behavior on fracture prevalence and healing in primates, factors which may affect frequencies within individual species will be addressed, using the Cayo Santiago macaque population as a case study. This species will be examined because of its large sample size and the impressive demographic data available for each individual. The impact of sex, age, and managed care on fracture prevalence will be addressed.

The null hypothesis is that there will be no appreciable differences in the risk of obtaining fractures between the male and female macaques at Cayo Santiago. This hypothesis will be tested by comparing fracture frequencies between male and female

Macaca mulatta. Additionally, this hypothesis will be tested for all the examined species. Because only long bones are included in the analysis, fractures obtained from violent interactions with conspecifics will not be considered. Although some variation in positional behavior may exist between the sexes in some species, it is believed that sex- dependent differences within species will be negligible compared to the differences in positional behavior between genera.

It is hypothesized that younger macaques will have higher fracture frequencies than older macaques at Cayo Santiago. Adult macaques are less likely to engage in risky locomotor behaviors, being more sedentary and terrestrial than juveniles (Wells and

Turnquist, 2001). Immature bone lags behind in development; younger primates may be more prone to fractures because their bones are weaker than their muscles. However, they are more likely to be protected by conspecifics. This hypothesis is complicated by

9 the fact that fractures to immature bone may heal to imperceptibility (Ulstrup, 2008) and fractures observed in adult skeletons may have occurred prior to adulthood (Bulstrode,

1987). Fractures accumulate over the life of the individual. Consequently, specimens have been selected for special consideration as case studies to determine whether these fractures can be traced back to the time of their occurrence through in vivo behavioral observations.

The null hypothesis is that improvements in managed care at Cayo Santiago have resulted in decreased fracture frequencies within the population over time. With fewer population pressures, primates may be less aggressive, resulting in fewer injuries caused by falls from heights during fights, or by primates pushing rivals out of trees.

Provisioning for and managed care of the macaques at Cayo Santiago has improved over time (Rawlings and Kessler, 1986). Buikstra (1975) examined fractures in a series of skeletal samples derived prior to the availability of regular provisioning and advancements in water collection. A previous study testing the association between linear enamel hypoplasia prevalence and nutritional status at Cayo Santiago indicates that provisioning has reduced enamel defects (Guatelli-Steinberg and Benderlioglu, 2006).

These patterns may be observed based on fracture prevalence in the current study. This hypothesis will be tested by comparing fracture prevalence rates of primates who died in or prior to 1972 based on Buikstra‟s (1975) findings with prevalence rates of primates who were born after 1972.

CHAPTER 2: Research Background

2.1 Bone and fracture biology

Bone is made up of two basic types of tissue: cortical or trabecular tissue.

Cortical tissue (compact bone) constitutes approximately 80% of the body mass of a human (Zoetis et al., 2003) and consists of solid and densely packed osteons with no macroscopic spaces in the bone (Ulstrup, 2008). The shafts of long bones and the outer surface of all bones are made up of compact bone (Swartz, 1983). Trabecular tissue

(cancellous bone) is made up of networks of lattices separated by macroscopic interconnecting spaces occupied by bone marrow (Ulstrup, 2008). Long bone epiphyses and metaphyses, the vertebral centra, and the interior of flat bones all consist of cancellous bone (Swartz, 1983). Both types of tissue share the same developmental processes, cell types, and extracellular protein and mineral components (Swartz, 1983).

Compact and cancellous bones are formed by tissue which exists in both woven and lamellar form. Woven bone is formed quickly and is organized poorly with a haphazard arrangement of collagen and hydroxyapatite crystals. Lamellar bone is formed slowly and is highly organized with strengthening parallel layers (lamellae). Ordinarily,

11 woven bone is not seen in adults although both woven and lamellar tissue is formed during the fracture healing process (Doblaré et al., 2004).

Bone consists of four types of cells: osteoblasts, osteoclasts, osteocytes, and bone lining cells (Ulstrup, 2008). Osteoblasts form bone, whereas osteoclasts resorb bone.

Osteocytes derive from former osteoblasts that are buried in the bone they have secreted.

Bone lining cells are former osteoblasts which remain on the bone surface, ready to be reactivated in response to stimuli (Zoetis et al., 2003).

Osteoblasts create a collagen matrix and secrete calcium-phosphate mineral

(Pearson and Lieberman, 2004). Preosteoblasts (osteoprogenetor cells) located near bone surfaces are created from undifferentiated mesenchymal cells at the periosteum or stomal tissues of bone marrow (Doblaré et al., 2004). The differentiation of mesenchyme into osteoblasts is controlled primarily through core-binding factor-α1 (Cbfα1); the transcription factor in turn is regulated by various growth factors, including bone morphogenetic proteins (Pearson and Lieberman, 2004). After forming bone, osteoblasts become preosteoblasts, osteocytes, bone lining cells, or undergo cell apoptosis (Goodship et al., 1998).

Osteoclasts form when mononuclear cells (monocytes) fuse from hematopoietic marrow. Osteoclasts contain a ruffled surface which adheres to the bone surface. A seal is created, allowing resorption to occur (Pearson and Lieberman, 2004). Osteoclasts secrete acid to demineralize the bone (lowering local pH levels) and enzymes to dissolve its organic matrix (Doblaré et al., 2004; Pearson and Lieberman, 2004).

Osteocytes sit in lacunae within bone (Pearson and Lieberman, 2004). Several processes extend from the osteocytes into tunnels (i.e., canaliculi) which connect to other

12 osteocytes or bone lining cells (Doblaré et al., 2004). They communicate via transmitter proteins at specialized gap junctions (Pearson and Lieberman, 2004). Osteocytes help form a connected cellular network linking osteocytes, cells along the periosteal and endosteal membranes, osteoblasts lining the bone surface, and preosteoblasts within the membrane (Pearson and Lieberman, 2004).

2.1.1 Biomechanical characteristics of fractures

Biomechanics is the interplay between biological systems and the mechanical environment, describing how forces affect the body‟s form and direction of motion

(Draper, 1998; Radasch, 1999). Force (force = mass x acceleration) is referred to as load when applied to bone. Bone has a non-linear relationship between stress and strain. The intensity of any load within a material (stress) determines the amount of deformation that material undergoes (strain). The amount of energy a material such as bone can absorb before it fails (fractures) is a measure of its toughness. Minimal loading may cause little or no change in the shape of the bone and moderate loading may only deform the bone while the load is being applied. The ability of bone to return to its original shape is called elasticity. Plasticity occurs at the yield point of bone, at which point the bone retains a loaded shape after the load has been released. Sufficient loading results in the catastrophic failure of the bone (Draper, 1998; Radasch, 1999).

Different bones, bone types, or bone segments exhibit different degrees of elasticity and plasticity (Draper, 1998; Radasch, 1999). Bone is considered isotropic if it exhibits fairly equal strength and stiffness in all directions; conversely bone is considered

13 anisotropic if it shows greater tensile strength and elasticity in one direction over another

(Amis, 1998). For example, the epiphyses of tibiae are isotropic, whereas the shaft is anisotropic. The ends of the bone are subject to loads in many directions, whereas the shaft receives predominantly axial stresses. Because the osteons that make up the cortical bone of long bones are oriented parallel to the longitudinal axis of the bone, it is stronger in the longitudinal direction than in the transverse direction (Radasch, 1999). Bone is considered to be anisotropic in general, compromising between the need for stiffness to reduce strain and ductility to absorb impact (Doblaré et al., 2004). Cortical bone is stiffer and less likely to deform than cancellous bone, allowing it to tolerate more stress prior to failure although it can tolerate less strain (Radasch, 1999).

When external loads are applied to bone, they generate internal forces, through the actions of muscles, tendons, and ligaments, which act upon bone to prevent or to produce movement (Radasch, 1999). A long bone can experience five types of loading: tension, compression, shear, torsion, and bending (Figure 2.1). Tension, compression, and shear are linear loads, whereas torsion and bending are angular loads. Tension or compression (depending on the direction of the load) is the result of a force being applied along the axis of a bone. Loads directed towards a surface result in compressive stress and strain whereas loads directed away from the surface result in tensile stress and strain.

Shear results from the application of a force to one end of the bone while restraining the other end, producing an opposite but parallel sliding motion of the body planes along the whole length of the bone. Torsion is caused by twisting the bone about its axis. Bending is the result of a moment (the angular equivalent of a force) applied to one end of the bone at a 90 degree angle to its axis in either the sagittal or coronal plane (Draper, 1998).

Figure 2.1 Basic forces acting on bone. From Rogers (1982).

Fractures are cracks or complete breaks in bone caused by the introduction of a load that exceeds bone strength or the repeated activity of loads that accumulate damage in excess of bone‟s repair rate (Adams and Hamblen, 1999). Fractures are designated as either simple (closed) or complex (open). Simple fractures have no communication between the outer skin surface and the fracture site. Complex fractures allow bacteria entry to the body, often resulting in infection and delaying healing (Merbs, 1989). Prior to the advent of antibiotics, infection secondary to a complex fracture may have been fatal (Roberts and Manchester, 1997).

Fractures are characterized by three mechanisms of injury: acute injury or trauma, repeated stress, and secondary to pathology. Most fractures are caused by direct and indirect trauma. A direct trauma injury results in a fracture at the point of impact, whereas an indirect trauma injury results in a break removed from the impact point

(Lovell, 1997). Cracks propagate through repetitive force or sustained stress, inducing fatigue or stress fractures (Merbs, 1989). In spontaneous or pathological fractures, an underlying pathological condition weakens the bone through the loss of the normal mineralized matrix (Radasch, 1999). Bone weakening may be generalized, such as the

15 decrease in bone quantity characterized by osteoporosis or the collagen deficiency seen in osteogenesis imperfect, or localized, such as the lytic lesions caused by metastatic carcinoma or tuberculosis (Roberts and Manchester, 1997).

Fractures often are classified according to the patterns of fracture received (Figure

2.2). Transverse fractures run perpendicularly to the long axis of the bone shaft. In contrast, oblique fractures run diagonally across the long axis (Mann and Murphy, 1990).

Spiral fractures run in an ascending circle around the shaft, beginning as small defects followed by cracks tracing the peak of tensile loading around the bone (Lovell, 1997;

Galloway, 1999). Comminuted fractures involve application of significant force to splinter bone into multiple fracture fragments (Adams and Hamblen, 1999). Young, immature bone often will buckle, bend, or crumple under stress, resulting in a greenstick fracture, named for its appearance (Roberts and Manchester, 1997). Butterfly fractures result from a combination of impacted fractures wedging together the two fractured ends of the bone. Traction and avulsion fractures are caused by violent muscle contractions breaking a portion of bone rather than rupturing the muscle itself (Roberts and

Manchester, 1997).

Figure 2.2 Common types of fractures. A. transverse; B. penetrating, C. comminuted; D. crush; E. oblique; F. spiral; G. greenstick (angular force); H. greenstick (compression); I. impaction; J. avulsion. From Lovell (1997).

Many commonly occurring fractures are named after individuals who described them. A Colles‟ fracture is a distal radius fracture with posterior displacement of the distal fragment. A Smith‟s fracture involves a break of the distal radius with associated medial maleolus ligamentous damage. A Monteggia‟s fracture is a fracture of the ulnar shaft with dislocation of the radial head. A fracture of the lateral condyle of the femur is termed a Stieda‟s fracture. Merbs (1989) provides a review of several such fractures.

The analysis of fractures has shed light on particular activities associated with specific breaks. For instance, the so-called chauffeur‟s fracture, a fracture of the styloid process of the radius caused by a torsional force, is common to individuals who spend much of their time driving vehicles. The grenade-thrower‟s fracture, caused by muscular contraction which fractures the humerus, is associated with throwing heavy objects.

Marching fractures are stress fractures of the metatarsal, calcaneus, or tibia frequently obtained by members of the military although they also are associated with athletes, dancers, nurses, salesmen, and pregnant women (see Merbs, 1989, for a short review). 17 Par interarticularis (or spondylolysis) is the traumatic separation of the neural arch from the vertebral body as a consequence of habitual physical stress (Merbs, 2002). Similarly, the clay-shoveller‟s fracture is the traumatic separation of the tip of the spinous process of the seventh cervical or first thoracic vertebra (Knüsel et al., 1996).

Fracture patterns that occur as a result of external forces are dictated by several factors, including the type of loading applied, the magnitude of the force, and the microstructure of the bone (Radasch, 1999). Different forces or moments acting on bone will result in different strains. Compressive force acting on a bone will strain it by shortening it slightly. However, a bending moment will cause one surface (for instance, the medial surface) to be in tension while the other surface (in this case, the lateral surface) will be in compression. Consequently, the medial stresses are tensile and the lateral stresses are compressive, stretching the lateral border of the bone in tensile strains and squashing the medial border of the bone in compressive strains (Draper, 1998).

Although clinical fractures often occur as a result of several forces acting together, characteristic fracture patterns are associated with the specific primary force(s) required to cause the fracture, as illustrated in Figure 2.3 (Radasch, 1999). Transverse fractures are caused by tension, creating tensile internally generated stresses, and bending, generated by tensile, compressive and possibly shear stresses. Bending loads also may result in butterfly fragments on the compression surface (Radasch, 1999).

However, butterfly fractures also may result from a combination of impacted fractures wedging together the two fractured ends of the bone (Roberts and Manchester, 1997). If bending and compression are combined, the degree of obliquity in butterfly fractures will be accentuated (Radasch, 1999). Compression loading causes compressive and shear

18 stresses to develop within bone, whereas shear loading generates shear stresses.

Compression, shear, and bending loading modes all are anticipated to produce short oblique fractures (Radasch, 1999). Torsion – and the resulting shear, tensile, and compression stresses generated along the longitudinal axis – causes spiral fractures

(Lovell, 1997; Radasch, 1999). Combined forces often result in complex fractures with comminution and numerous fracture lines (Radasch, 1999).

Figure 2.3 Effects of basic forces on characteristic fracture patterns. A. tension results in transverse fractures; B. compression or shear results in oblique fractures; C. torsion results in spiral fractures; D. bending results in transverse or butterfly fractures. Adapted from Radasch (1999).

2.1.2 Fracture healing

Fracture healing is a complex process involving the interaction of several cell types. The removal and deposition of bone, the prime means of microdamage repair and 19 tissue architectural adjustment, are accomplished through processes called modelling and remodelling (Goodship et al., 1998). In both cases, osteoclasts are activated followed by osteoblasts (Doblaré et al., 2004). In modelling, tissue removal and formation occur at different sites concurrently, thereby changing the gross morphology of the bone. In remodelling, tissue removal and formation occur at the same site at different times

(Goodship et al., 1998).

Frost‟s (2003) mechanostat theory states that the mechanostat uses modelling and remodelling thresholds to determine exactly where or when bone needs more or less strength, and responds accordingly. Bone modeling and remodeling stimulus is based on physical deformation of the tissue, via a feedback loop mechanism. When the upper strain threshold is reached, net bone synthesis occurs through modelling; when the lower strain threshold is reached, bone resorption occurs (Frost, 2003). For instance, increased strain through physical activity leads to deposition of bone tissue which reduces strain to the original customary level. Conversely, decreased strain leads to the resorption of bone until the customary strain level is reached. This level varies among taxa and throughout different skeletal locations as well as being dependent upon the particulars of the strain affecting the tissue (Ruff et al., 2006).

Modelling causes bone resorption from one cortex of the bone with bone resorption from the opposite cortex, resulting in a net gain of bone (Figure 2.4). Bone modelling is caused by drifts: formation drifts create osteoblasts to add bone to some surfaces while resorption drifts remove bone from other surfaces via osteoclasts (Frost,

2001). Modelling occurs during growth in children (Rauch and Schoenau, 2001) and during fracture healing to restore the original shape of the bone, if possible, in adults. For

20 instance, drifts can move whole segments of bone to correct a fracture malunion in a subadult. Periosteal drifts on one side of the bone and endosteal drifts on the other side resorb bone from their respective surfaces, while the opposing drifts deposit new bone

(Frost, 2001).

Figure 2.4 Bone modeling. Drifts move the surface of an infant long bone from its original size and shape (solid line) to its new shape (dashed line) during growth (A) and as would occur in fracture healing (B). In (C), formation drifts (F) make and control new osteoblasts to deposit bone and resorption drifts (R) make and control new osteoclasts to remove bone. From Frost (2001).

21 According to Wolff‟s law, changes in bone form or function cause corresponding changes in the bone‟s internal and external architecture (Ulstrup, 2008). Consequently, bone function, in addition to metabolic factors, age, and other variables, contributes to bone remodelling (McKinnis, 1997; Ruff et al., 2006). One of the ways in which functional adaptation (Wolff‟s law) may work in fracture repair is through signaling the beginning of a remodeling cycle during fracture repair. Martin (2000) suggests that osteocytes send an inhibitory signal to osteoblasts, preventing them from forming bone.

When the basic multicellular unit (BMU) (discussed below) is completed during a remodelling cycle, some of the osteoblasts become bone lining cells, still receiving the signal from the osteocytes. If the bone lining cells do not receive the inhibitory signal, they begin a bone remodelling cycle. Diminished loading (disuse) or microdamage affect transmission of the inhibitory signal, consequently activating remodelling by deactivating the inhibitory signal (Martin, 2000).

Remodelling causes erosion and replacement of microscopic cavities of bone, often resulting in a net loss of bone (Frost, 2001). Remodeling replaces immature and old bone in order to maintain its functional capacity (Parfitt, 2002). During fracture healing, osteoclasts resorb damaged bone while woven bone is laid down, increasing bone strength when a sufficient amount of strain surpasses the modelling threshold

(Parfitt, 2003; Frost, 2003). Remodelling is accomplished through the action of basic multicellular units (BMUs) (Frost, 2001). The BMU creates and controls the osteoblasts and osteoclasts following an ARF sequence. The ARF sequence is the process of activation, resorption of bone by osteoclasts, and formation of bone by osteoblasts

(Figure 2.5; Frost, 2001). During remodeling, mineral balance can alter, microdamage

22 can repair, and bone can adapt to the mechanical environment, thus reducing fracture risk. Although remodeling may be stochastic (non-targeted), it also can be targeted towards specific sites, such as in microdamage repair (Burr, 2002). Removal of hyper- mineralized bone may be a focus of non-targeted remodeling (Parfitt, 2002). Changes in bone mass and architecture may be dependent upon signals sent out by the osteocytes when bone degredation limits are reached (Rauch and Schoenau, 2001).

Figure 2.5 Bone remodeling. An activation event (A) causes bone resorption (B) and eventual formation (C). The BMU makes and controls the osteoblasts and osteoclasts involved in remodeling. Adapted from Frost (2001).

Fracture healing mechanisms differ depending on the type of bone affected and treatment provided. Cortical bone fractures heal by callus (or new bone) formation bridging the fracture gap. Unless the fracture gap is wide, cancellous bone heals by direct osteoblastic activity (Dimitriou et al., 2005). Fracture healing also can be affected by nutritional status, the presence of infection, age, and various other factors.

Direct (or primary) fracture healing is rare. Because it necessitates near-complete inter-fragmentary immobility, it is accomplished through application of internal fixation devices (Einhorn, 1998). Secondary osteons remodel the bone across the fracture line

23 (Goodship et al., 1998). This process is performed when osteoclasts are activated, forming a cutting cone of discrete remodelling units (Dimitriou et al., 2005). The cutting cone of osteoclasts resorbs a tunnel of bone across the fracture gap. Immediately behind the osteoclasts, active osteoblasts deposit lamellae forming osteons. The fracture line is obliterated by the osteons. There is little or no callus formation (McKinnis, 1997).

Direct fracture healing is a non-conservative form of treatment unlikely to be found in premodern skeletal populations; obviously this type of healing will not be seen in wild primates.

Indirect (or secondary) fracture healing is undergone when fractures are not treated or during surgical interventions which permit some degree of motion, including the use of a sling or cast, external fixation, and intramedullary fixation. Indirect fracture healing of cortical bone undergoes five stages, combining intramembranous and endochondral ossification (Einhorn, 1998).

In the initial stage, the periosteum (dense fibrous tissue enveloping the cortex) and endosteum (lining the inner aspect of the cortex and medullary cavity) rupture

(Figure 2.6). Blood escaping torn vessels creates a haematoma and a blood clot. Nearby osteocytes die from ischaemia caused by capillary division at the fracture site. However, other cells are sensitized by the injured cells, allowing them to respond to local and systemic healing stimuli (Hendrix, 2002).

Figure 2.6 Stages of fracture healing. Drawings (A, C, E) and photomicrographs (B, D, F) of events following fracture of a long bone diaphysis. A. initial haematoma; B. rat femur 3 days after injury; C. woven bone and cartilage formation; D. rat femur 9 days after injury; E. callus formation and revascularization; F. rat femur 21 days after injury. Adapted from Buckwater et al. (2010) and Einhorn (1998). 25 The second stage is characterized by a buildup of granulation tissue.

Subperiosteal and endosteal cells form a collar of active tissue, which surrounds and connects adjacent bone fragments. The release of local biochemical messengers causes cells to proliferate or regulate the differentiation of the sensitized cells into fibroblasts or new vessels. Macrophages and giant cells within the granulation tissue invade and remove the haemotoma. Osteoclasts resorb nearby dead bone (McKinnis, 2002).

In the third stage, a callus replaces the granulation tissue. Cellular buildup produces osteoblasts which differentiate into the various cell types responsible for fracture union. New bone deposited on either side of the fracture site proceeds towards the gap, eventually uniting. At the site of union, the cells produce cartilage and osteoid matrices, the mineralization of which creates the primary callus (Hendrix, 2002). The callus acts as a natural splint, providing rigidity (Adams and Hamblen, 1999). Small changes in the diameter of the bone will have a large effect on its strength, which explains why periosteal callus formation can stabilize a longbone shaft fracture after only slight deposition of immature bone tissue (Amis, 1998).

The cartilaginous callus is replaced by lamellar mature bone in the fourth stage.

This secondary callus is created via the osteoclast resorption and osteoblast deposition of new bone (McKinnis, 1997). The basic multicellular unit (BMU) is responsible for the new bone formation and replacement of calcified callus (Frost, 2001, 2003). The BMU produces osteoclasts which resorb part of the callus, followed by osteoblasts, which fill the newly created space with new bone. Calcified cartilage is replaced with woven bone which, in turn, is replaced with lamellar bone (Hendrix, 2002).

26 In the final stage, the bone is reshaped to nearly its normal contour. Once bone remodelling is complete, the bone is modelled into roughly its pre-fracture shape.

Excessive bone is resorbed. Skeletal maturation has an adverse effect on modelling

(Hendrix, 2002). Consequently, subadult bone fractures are more likely to return to their prefracture state than fractures in adults. It is possible that modelling occurs in response to local mechanical stress and strain following callus maturation (Hendrix, 2002).

Indirect fracture healing of cancellous bone differs from that of cortical bone.

Cancellous bone fractures heal by means of creeping substitution rather than callus formation (Hendrix, 2002). Through intramembranous ossification, osteoblastic activity occurs directly at the fracture site (Shefelbine et al., 2005). Fracture fragments must be near each other, or haematoma with callus formation will occur (Hendrix, 2002).

Necrotic tissue is resorbed as soft tissue forms in the fracture gap. Isotropic woven bone is laid down by osteoblasts to stabilize the fracture gap. The woven bone then is remodeled into anisotropic trabecular bone. The orientation of the trabeculae is dependent upon loading conditions (Shefelbine et al., 2005).

The time frame for fracture healing involves three overlapping stages: the inflammation, reparative, and remodeling phases. The inflammation phase, occupying approximately 10% of the total healing time, includes the occurrence of the fracture and clot formation in the fracture gap formed by the torn periosteum. The reparative phase, lasting approximately 40% of healing time, includes the formation of granulation tissue, the primary callus, and the ring of cartilage at the margin of the fracture. Lasting about

70% of healing time, the remodeling phase includes the replacement of callus by lamellar bone and the resorption of excess bone formation (Hendrix, 2002).

27 Many factors contribute to the actual amount of time in months or years it takes for these phases to conclude. Metabolic cell function may be influenced by endogenous or exogenous factors. Fractures to younger bone heal faster than fractures in elderly individuals. In children, bone deposition exceeds bone resorption, creating rapid remodeling capabilities. In addition, the thick periosteum maintains reduction and supplies vascular support (Buckwater et al., 2010). Fracture healing time also is dependent upon the degree of local trauma and tissue involvement, the degree of bone loss, and the type of bone involved (e.g., cancellous bone unites rapidly at direct contact points) (Hendrix, 2002). Fracture gap size also is a factor: a large gap size delays healing due to the formation of a smaller, less stiff callus (Gómez-Benito et al., 2005). Other factors include the presence of infection, other pathological conditions, or local malignancies, all of which can impede healing. The degree of immobilization is critical to fracture healing: inadequate immobilization may lead to delayed union or nonunion with a pseudoarthrosis (McKinnis, 1997). Various pharmacologic factors (including hormones, antibiotics, anticoagulants, corticosteroids, and smoking) contribute to fracture healing times, as well as controlled exercise of the affected area (Hendrix, 2002).

2.1.3 Nonhuman primates as models of fracture repair

Molecular regulatory mechanisms driving the five stages of fracture repair are understood only partially. There are three groups of signaling molecules: pro- inflammatory cytokines, growth factors, and angiogenic factors (Dimitriou et al., 2005).

Cytokines regulate endochondral bone formation and remodeling; some cytokines

28 (Interleukin-1, Interleukin-6, and tumour necrosis factor-α) have been shown to help initiate fracture repair (Dimitriou et al., 2005). The transforming growth factor-β (TGF-

β) superfamily is one of a class of proteins which regulates cellular proliferation, osteoblast differentiation, and bone matrix synthesis during fracture healing (Axelrad et al., 2007). Platelets may release TGF-β into the fracture haematoma while osteoblasts synthesize it throughout the healing process (Hendrix, 2002). Bone morphogenic proteins (BMPs) also help regulate bone regeneration subsequent to fracture, during both the graft healing process and angiogenesis (Valdes et al., 2009). Optimal bone regeneration is assisted via angiogenesis, which is the growth of new blood vessels. It has been suggested that angiogenesis is regulated through both a vascular-endothelial growth factor dependent pathway, which mediates specific mitogens during fracture repair, and an angiopoietin dependent pathway, which helps form larger blood vessels and develop branches from existing vessels (Dimitriou et al., 2005).

Nonhuman primates have been used along with other animals as models for human fracture repair when researching clinical applications manipulating signaling molecules. Fibroblast growth factor-2 (FGF-2), a mitogen for mesenchymal cells, has been shown to accelerate fracture healing and prevent nonunion in adult male

Cynomolgus monkeys (Macaca fascicularis) (Kawaguchi et al., 2001). Similarly, human bone morphogenetic protein-2 (rhBMP-2) has been shown to accelerate osteotomy-site healing in adult male baboons (Papio hamadryas) and Cynomolgus monkeys (Macaca fascicularis) by increasing efficiency in regulating the differentiation and proliferation of mesenchymal cells to osteoblasts (Radomsky et al., 1999; Seeherman et al., 2004, 2006).

In their review of the history and applications of rhBMP-2, Valdes and others (2009)

29 identify several other instances in which nonhuman primates have been used as models for fracture repair. However, use of various growth factors in recent human clinical trials have not been as effective as in earlier animal models (Bishop and Einhorn, 2007;

Giannoudis et al., 2007).

Bone quality parameters, such as bone mineral density measurements, can serve as predictors of fracture risk (Grynpas et al., 2000) and comparisons of bone formation rates in humans and rhesus macaques (Macaca mulatta) reveal that cortical bone turnover is slower in macaques than in humans (Burr, 1992). Assessment of bone mineral density in nonhuman primate models for human osteoporosis and osteopenia studies has been explored, using macaques (Macaca nemestrina and M. mulatta) (Cerroni et al., 2000;

Kramer et al., 2002), and baboons (Papio hamadryas anubis and P. h. cynocephalus)

(Havill et al., 2008). However, possible variations in healing amongst nonhuman primate species and genera may affect results adversely.

2.2 Fracture studies

Human and nonhuman primates exhibit a variety of pathological conditions. A multitude of infectious diseases have been reported in both captive and wildshot nonhuman primates, including malaria, yellow fever, yaws, and amoebic dysentery

(Schultz, 1956). Neoplasm appears to be rare in nonhuman primates (Schultz, 1956), possibly reflecting differences in longevity between humans and nonhuman primates.

30 The presence of degenerative joint disease varies within taxa (Schultz, 1956). Dental disease is prevalent throughout the primates, including the presence of abscesses, carious lesions, periodontal disease, enamel hypoplasia, and antemortem tooth loss (Lovell,

1991). Cranial trauma includes vault and facial fractures as well as bite wounds

(DeGusta and Milton, 1998; Jurmain and Kilgore, 2005). It has been reported that postcranial trauma among apes is rather uncommon (Jurmain and Kilgore, 2005).

However, this conclusion is contradicted by other sources (Schultz, 1956; Lovell, 1991).

Not only have all of these conditions also been recorded in humans, but in addition palaeopathological, palaeoepidemiological, and bioarchaeological studies have aimed specifically to document examples of medical intervention based primarily upon osteological evidence. Differentiating between the practice of trepanation in association with cranial trauma (indicative of the treatment of head injuries) and trepanation for ritual reasons or for the obtainment of roundels as fetishes (Bennike, 1985; Brothwell, 1994;

Sankhyan and Weber, 2001) has been attempted. Amputation for therapeutic purposes is explored commonly in the literature (Merbs, 1989; Verano et al., 2000; Redfern, 2010;

Van der Merwe et al., 2010). The treatment of dental disease has been suggested due to the identification of drilled tooth crowns and roots (Bennike, 1985; Larsen, 1997;

Langsjoen, 1998). Fractures have been examined to ascertain whether individuals were provided with medical treatment in the past through reduction and splinting techniques

(Grauer and Roberts, 1996; Judd and Roberts, 1998, 1999; Prokopec and Halman, 1999;

Anderson, 2002; Redfern, 2010).

The determination of fracture frequencies in human or nonhuman primates is limited by several factors. For instance, high levels of taphonomic interference can make

31 the true prevalence of fractures (or any other pathological conditions) within a population difficult or impossible to determine (Grauer and Roberts, 1996). Well remodeled fractures, such as stress fractures and those obtained during growth and development, can heal to imperceptibility (Ulstrup, 2008). It is difficult to distinguish recent antemortem fractures from old breaks which have not healed (Grauer and Roberts, 1996). Museum samples may be obtained by shooting entire groups of primates, meaning that fracture frequencies measured within those groups presumably more accurately reflect frequencies for the entire population than study samples composed of nonhuman primates obtained opportunistically or trapped (Brandwood et al., 1986; but see Buikstra, 1975).

However, the representativeness of museum samples may be subject to sampling bias due to the tendency for museums to acquire non-pathological samples (Brandwood et al.,

1986). Skeletal material from some primates who die from their injuries will not be available because the animal became separated from the group (Lovell, 1991). For instance, only 36% of the bodies of all chimpanzees at Gombe that died during a twenty year period have been seen (Goodall, 1986).

2.2.1 Previous studies involving fractures in human skeletal assemblages

Fractures are one of the most common forms of pathological conditions observed in human skeletal remains (Roberts and Manchester, 1997). There has been a long standing interest in the contributions that fracture analyses can make to the understanding of past lifestyles. Fractures may indicate stress; for instance, a low frequency of fractures suggests a non-stressful lifestyle (Nakai et al., 1999). The analysis of fracture pattern

32 distribution between and within populations may determine gender-differentiated or class-based occupational specialization (Judd, 1994; Cardy, 1997; Judd and Roberts,

1999; Petersson, 1999). Also, fracture patterns can suggest the level of interpersonal or intrapersonal violence exhibited by one or more communities (Stroud and Kemp, 1993;

Liston and Baker, 1996; Robb, 1997; Jurmain, 2001; Jurmain et al., 2009; Meyer et al.,

2009; Steyn et al., 2010, Van der Merwe et al., 2010). Other studies focus on fracture etiology or epidemiology (Lovejoy and Heiple, 1981; Stroud and Kemp, 1993; Neves et al., 1999).

Clinical literature abounds with information concerning the impact of activity on fracture etiology in humans based on biomechanical factors. The vast majority of fractures to the clavicle are the result of a direct blow to the shoulder, either by falling onto the shoulder or by hitting the point of the shoulder (Stanley et al., 1988; Nowak et al., 2000). However, the most common fracture to the medial third of the bone, which is the most common area fractured in clavicles, is from a fall on the outstretched hand

(Craig, 1996). The most common etiologies for isolated proximal humeral fractures include a fall onto an outstretched hand, excessive abductive rotation of the arm, or a direct blow (Bigliani et al., 1996). Humeral shaft fractures are associated with falls onto the outstretched hand, vehicular accidents, some form of direct load to the arm, or extreme muscle contracture (Zuckerman and Koval, 1996). Falls onto the hand usually focus forces into a section located around the radius and the scaphoid (Galloway, 1999).

Direct blows caused by vehicular accidents, fights, or gunshot wounds often are the mechanisms of injury for radius and ulnar shaft fractures (Richards, 2001). Older individuals are at great risk of falling, fracturing the femoral neck (Testi, et al., 1999).

33 Falling on an outstretched arm is also the common etiology of combined fractures of the hip and the neck of the humerus (Mulhall et al., 2002). Tibial and fibular shaft fractures often occur concurrently, either as a result of an angular force, causing transverse or oblique fractures or torsional force, resulting in spiral fractures (Lovell, 1997).

The biomechanical properties of bones can be used to interpret fractures in terms of activity patterns in archaeological populations. Analysis of metacarpal fractures at an historic British cemetery has demonstrated a change in boxing styles over time from bare-knuckle fighting to boxing with gloves (Merb, 1998; Smith and Briskley, 2006).

Long bone fractures (in addition to spondylolysis and subluxation) in late nineteenth century migrant mine workers from Kimberley, South Africa indicate the hazards involved in and the strenuous activities required during performance of their work duties

(Van der Merwe et al., 2010).

Examination of the pattern and types of skeletal trauma has led to the differentiation of the frequency of accidental as opposed to intentionally inflicted injuries in two western Pacific populations (Scott and Buckley, 2010). Parry fractures, in which an individual attempts to ward off a blow to the face, are characterized by isolated transverse fractures of the ulna with midshaft swelling and little to no rotation or apposition (Lovell, 1997; Judd, 2004). However, oblique or spiral ulnar shaft fractures often are caused by falls onto the pronated hand (Judd and Roberts, 1999). Furthermore, isolated ulnar shaft fractures may be caused by an individual falling against a sharp object

(Jurmain, 2001). The high prevalence of fractures involving both the radius and the ulna, the many instances of multiple trauma, and lack of cranio-facial trauma in a Nubian skeletal population at Kulubnarti suggests a high rate of accident-related injuries due to

34 the rugged and forbidding terrain (Kilgore, et al., 1997). Conversely, individuals from

Semma South, Sudanese Nubia, may have practiced interpersonal violence in the form of wrestling and stick fighting or domestic violence, due to the high rate of craniofacial trauma (Alvrus, 1999). A high prevalence of cranial fractures usually is implicated with violence (Standen and Arriaza, 2000; Judd, 2004) whereas a high prevalence of forearm fractures often is felt to indicate accident related etiologies (Grauer and Roberts, 1996;

Kilgore, at al., 1997; Jurmain and Kilgore, 2005). A high prevalence of forearm fractures, probably due to accidents, has been recorded in a skeletal population from the irregular desert and semi-desert landscape at San Pedro de Atacama, in Northern Chili

(Neves et al., 1999).

Analysis of fractures in past human assemblages may suggest the possibility of medical treatment. It is unusual for treatment to be ascertained absolutely, because the materials used during treatment rarely survive taphonomic conditions and conservative splint immobilizations are not permanent, although copper-alloy plates used to splint fractures have been recovered (Knüsel et al., 1995) and I have seen an ulnar fracture treated with lane plates in the Hamann-Todd Collection at the Cleveland Museum of

Natural History. Researchers usually base the possibility of medical treatment on osteological evidence alone. Well healed fractures, including a fractured tibial condyle from a Bronze Age barrow cemetery which healed with minimal deformity (Anderson,

2002) and a medial femur and tibia from a Late Woodland population in Ohio with a lack of pronounced angulation and shortening of the bone (Lovejoy and Heiple, 1981), have been suggested as evidence for treatment. Other studies suggest that healed fractures provide evidence for treatment in the past simply because splinting is an ancient medical

35 technique and such treatment must have been available. For instance, dispite finding that most of the long bone fractures within the Matiegka Pathological Collection comprising medieval sites in Prague healed badly or not at all, Prokopec and Halman (1999) speculate that the few fractures which healed with only angulation and shortening are examples of inadequately treated fractures. Conservatively treated clinical control groups may be used as a model of successful healing when compared to archaeological samples

(Roberts, 1988; Roberts, 1991; Grauer and Roberts, 1996). However, in the Medieval St.

Helen-on-the-Walls collection, Grauer and Roberts (1996) determine that the high level of healed ulnar fractures lacking deformity either is a result of intentional treatment or that the radius acts as a natural splint. Similarly, Roberts (1988) states that successfully healed fractures of the fibula could be due either to treatment or to a natural splint in the form of the tibia. Other long bone fracture studies attempt to provide evidence of possible past medical treatment using anatomical knowledge of the constraints which biology imposes upon the body to suggest cases in which the bone must have been assisted in some way to facilitate healing (Grauer and Roberts, 1996; Cardy 1997;

Redfern, 2010). Cardy (1997) states that two fractured femora in the Medieval Whithorn population were treated because if they were not reduced, the strength of the femoral muscles would have caused the bone ends to overlap, resulting in severe deformity.

Grauer and Roberts (1996) state that the fractures affecting both the radius and the ulna in the medieval St. Helens population probably were treated because the instability caused by such fractures would result in deformity and osteoarthritis if not treated. Redfern

(2010) examined several Iron Age and Roman sites in Dorset for evidence of conservative treatment of fractures using many of the criteria mentioned above, including

36 identifying both stable and unstable fracture types which would not have healed as well had reduction and immobilization not been applied.

2.2.2 Previous studies involving fractures in primate skeletal assemblages

As with humans, fractures are the most frequent type of pathological condition seen in nonhuman primates. Lovell (1991) provides a short review of published accounts in which descriptions are included of one or a few fractures among various ape species and chacma baboons. However, problem-oriented studies concerning fractures and fracture etiology in nonhuman primates are lacking in the clinical and primatological literature. Studies linking fracture frequencies and arboreality (Lovell, 1991; Chapman et al., 2007) or aggression and predation (Schultz, 1939, 1944; DeGusta and Milton, 1998;

Jurmain, 1989; Lovell, 1990a; Chapman and Legge, 2009) have been reported. Schultz

(1944) stated that fracture rates increase over the lifetime of the individual, although

Bulstrode (1987) warned that those rates may be exaggerated because many fractures occurred in juveniles. Assessments of the impact of fractures and other traumatic injuries on reproductive fitness and consequently primate evolution also have been attempted

(Schultz, 1937, 1956; Zihlman et al., 1990; Lovell, 1991). The use of captive nonhuman primates as animal models for fracture repair in biomedical research already has been discussed in this chapter.

Clinically, treatment of long bone fractures tends to be the focus of research.

Intramedullary pinning with external fixation has been applied to transverse tibial-fibular fractures in a Cynomolgus monkey (Macaca fascicularis) who caught its right lower leg

37 in a cage door (Swaim and Martin, 1968). Fractured tibiae are slow-healing bones, possibly due to insufficient haematoma production restricting callus growth (Swaim and

Martin, 1968). A common squirrel monkey (Saimiri sciureis) with an ulnar fracture and associated elbow luxation was treated with external fixation when the elbow would not remain reduced following multiple closed reduction attempts (Wellehan et al., 2004).

Internal fixation with intramedullary pins of four fractures of the distal humerus and 3 fractures of the humeral shaft in rhesus macaques (Macaca mulatta) has been described

(Faulkner, et al., 1976). Intramedullary pinning is the preferred method of fracture immobilization, as nonhuman primates rarely tolerate plaster casts (Mahoney, 2005). A bonnet macaque (Macaca radiata) with caudolateral luxation of the right radius and ulna was treated with closed reduction (Wellehan, et al., 2004). A method of cast application to immobilize the fractured legs and knees of rhesus macaques has been devised (Rohner and Eyring, 1970).

In classic articles, Schultz (1939, 1967) determined that the high level of healed fractures (36%) depicted in 118 wildshot, adult gibbon long bones cast doubts on the validity of assigning treatment to fractures in human assemblages. Nonhuman primate fractures healed with widely varying degrees of success. Although some healed well, with little angulation or deformity, others failed to heal, developed nonunion and pseudoarthrosis, or healed with significant displacement and shortening. The gibbons could not have practiced reduction or immobilization of the affected limbs; consequently, it is doubtful that researchers could posit that humans treated each other‟s wounds solely based upon the presence of a well-healed fracture. It was apparent that most of the breaks did not incapacitate the apes so much that they starved or were captured because

38 the apes under scrutiny were abundant throughout the study area despite low fertility levels. Accordingly, he denied that the many incidences of healed fractures could be due in part to the death of large numbers of gibbons from displaced bone, thereby affecting the fracture frequency rate (Schultz, 1939, 1956, 1967).

Epidemiological information concerning fracture patterns in nonhuman primates is scarce, although some prevalence rates have been reported. Summaries of the fracture frequencies reported for various primate species obtained from previously published accounts are provided here. When comparing fracture frequencies in the literature, it is important to distinguish between those researchers who examined the full skeleton, including crania and vertebrae, (Table 2.1) and those who examined long bones only

(Table 2.2). Furthermore, sometimes it is difficult to determine which formula was used to calculate frequencies, when researchers may list all fractures observed (cross frequencies in Table 2.2) or all individuals who received at least one fracture (individual frequencies in Table 2.2). Whenever possible, all combinations of frequencies available are included.

As far as I have been able to determine, no accounts of fracture prevalence rates have been reported in prosimians prior to this study. According to data collected from the literature, fractures are more prevalent in Old World monkeys than New World monkeys based on comparisons using the entire skeleton of Aotus, Leontopithecus,

Cebus, Macaca, Cercopithecus, Lophocebus, Procolobus, Colobus, and Nasalis in the

Cameroons, Nagana, and elsewhere (Schultz, 1956; Nakai, 2003; Chapman and Legge,

2009). Rhesus macaques (Macaca mulatta) from Cayo Santiago (Buikstra, 1975) are slightly more likely to receive fractures than Japanese macaques (Macaca fuscata

39 fuscata) from Nagano Prefecture, Japan (Nakai, 2003) based on long bone fracture prevalence rates. Yellow baboons (Papio cynocephalus) at the Darajani Primate

Research Station near Kibwezi in Kenya, East Africa have comparatively high fracture patterns (Bramblett, 1967).

40 Table 2.1 Individual fracture frequencies in comparative populations (examining the complete skeleton) SA S N n % Sources Aotus NA A 10 … 20 1 Leontocebus* NA A 56 … 12 1 Cebus NA A 22 … 27 1 Macaca f. fuscata N F 107 57 53.27 2 Macaca f. fuscata N A 88 47 53.41 2 Papio cynocephalus D F 61 39 63.93 3 Papio cynocephalus D A 37 30 81.08 3 Cercopithecus pogonias Cm F 20 6 30.00 4 Cercopithecus cephus Cm F 27 11 40.74 4 Cercopithecus nictitans Cm F 27 12 44.44 4 Cercocebus agilis Cm F 5 4 80.00 4 Cercocebus torquatus Cm F 12 8 66.67 4 Lophocebus albigena Cm F 14 9 64.29 4 Procolobus badius Cm F 28 10 35.71 4 Colobus guereza Cm F 6 1 16.67 4 Nasalis NA A 25 … 28 1 Hylobates NA A 260 … 33 1 Hylobates sp. (pr) A 118 42 35.59 5, 6 Hylobates sp. Ch F 233 65 27.90 7 Hylobates sp. Ch A 233 60 25.75 7 Pongo NA A 68 … 34 1 Pongo pygmaeus (Ca) A 14 4 28.57 8 Gorilla NA A 19 … 21 1 Gorilla g. beringei V F 31 6 19.35 9 Gorilla g. beringei V A 26 6 23.08 9 Gorilla gorilla (WR) F 199 26 13.07 10 Pan sp. NA A 56 … 18 1 Pan t. schweinfurthii G F 11 5 45.45 11 Pan t. schweinfurthii G A 9 5 55.56 11 *partially Leontopithecus , partially Saguinus SA = study area: samples from museums are included in parentheses; NA = no information available; N = Nagano; D = Darajani; Cm = Cameroons; (pr) = private collection; Ch = Chiengmai; (Ca) = Cambridge; V = Virunga; (WR) = Western Reserve; G = Gombe S = subset of population: A = adults; F = full sample N = total number of individuals examined; n = total number of fractures % = frequency (n/N)*100 Sources: 1. Schultz (1956); 2. Nakai (2003); 3. Bramblett (1967); 4. Chapman and Legge (2009); 5. Schultz (1939); 6. Schultz (1967); 7. Schultz (1944); 8. Duckworth (1911); 9. Lovell (1990b); 10. Randall (1944); 11. Jurmain (1989) 41

Table 2.2 Fracture frequencies in comparative populations (examining long bones only) SA S individuals elements frequencies sources N n N n I E C Macaca f. fuscata N F 107 18 1474 25 16.82 1.70 23.36 1 Macaca f. fuscata N A 88 16 … 23 18.18 … 26.14 1 Macaca mulatta CS F 175 26 … … 14.86 … … 2 Macaca mulatta CS A 77 23 … 27 29.87 … 35.06 2 Papio cynocephalus D F 61 … … 20 … … 32.79 3 Papio cynocephalus D A 37 … … 13 … … 35.14 3 Hylobates sp. (pr) A 118 … … 43 … … 36.44 4, 5 Hylobates sp. Ch F 233 … … 63 … … 27.04 6 Pongo pygmaeus (Ca) A 14 4 … 9 28.57 … 64.29 7 Gorilla g. gorilla (P-C) A 62 11 879 13 17.74 1.48 20.97 8, 9 Gorilla g. beringei V F 31 3 … 3 9.68 … 9.68 10 Gorilla g. beringei V A 26 3 … 3 11.54 … 11.54 10 Gorilla gorilla (U) F 29 … 342 6 … 1.75 20.69 11 Gorilla gorilla (WR) F 199 11 … 22 5.53 … 11.06 12 Pan troglodytes (U) F 17 … 231 5 … 2.16 29.41 11 Pan t. troglodytes (P-C) A 92 20 1267 22 21.74 1.74 23.91 8, 9 Pan t. schweinfurthii G F 11 3 … 4 27.27 … 36.36 13 Pan t. schweinfurthii G A 9 3 … 4 33.33 … 44.44 13 Pan t. schweinfurthii K F 11 4 133 4 36.36 3.01 36.36 14 Pan paniscus (P-C) A 15 2 197 2 13.33 1.02 13.33 8, 9 SA = study area: samples from museums are included in parentheses. N = Nagano; CS = Cayo Santiago; D = Darajani; (pr) = private collection; Ch = Chiengmai; (Ca) = Cambridge; (P-C) = Powell-Cotton; V = Virunga; (U) = National Museum of Natural History (Smithsonian Institution); (WR) = Western Reserve; G = Gombe; K = Kibale S = subset of population: A = adults; F = full sample Individuals and Elements: N = total number of individuals or elements examined; n = total number of fractures per individual or element Frequencies: I = individual frequency (In/IN)*100; E = element frequency (En/EN)*100; C = cross frequency (En/IN)*100 Sources: 1. Nakai (2003); 2. Buikstra (1975); 3. Bramblett (1967); 4. Schultz (1939); 5. Schultz (1967); 6. Schultz (1944); 7. Duckworth (1911); 8. Jurmain (1997); 9. Jurmain and Kilgore (2005); 10. Lovell (1990b); 11. Lovell (1990a); 12. Randall (1944); 13. Jurmain (1989); 14. Carter et al. (2008)

Fracture frequencies among the hominoids are more readily available.

Orangutans from the Cambridge collection have the highest frequency of long bone fractures among the apes (Duckworth, 1911). Although Schultz (1939, 1944, 1967) stated that gibbons have high frequencies of long bone fractures, the ranges of rates from 42 various collections are not appreciably different from common chimpanzees housed at

Powell-Cotton (Jurmain, 1997; Jurmain and Kilgore, 2005) and the National Museum of

Natural History (Lovell, 1990a), the Gombe chimpanzees (Jurmain, 1989), and the

Kibale chimpanzees (Carter et al., 2008). Gorillas and bonobos housed at Powell-Cotton

(Jurmain, 1997; Jurmain and Kilgore, 2005) exhibit the lowest long bone frequencies, along with Virunga gorillas (Lovell, 1990b), and gorillas from various museum collections (Randall, 1944; Lovell, 1990a). These ranks shift when comparing the full skeleton, with chimpanzees and gorillas averaging the highest and lowest frequencies, respectively, and orangutans averaging slightly higher frequencies than gibbons (see

Table 1.1 for specifics and references).

Primates differ in the anatomical distribution of fractures. In gibbons and orangutans, the most common long bones to fracture are the humerus and femur (Schultz,

1937, 1939, 1956, 1967). The Kibale chimpanzees most commonly fractured their hands

(Carter et al., 2008). Cayo Santiago macaques (Buikstra, 1975) suffer more from hind limb than fore limb fractures; conversely, Gombe chimpanzees (Jurmain, 1989) and

Chiengmai gibbons (Schultz, 1944) incur more fore limb than hind limb fractures.

Sex differentiation in fracture prevalence has been reported in howler monkeys

(DeGusta and Milton, 1998) gibbons (Schultz, 1937; Schultz, 1944), and gorillas

(Randall, 1944). However, other studies of apes (Lovell, 1990a) and howlers (Crockett and Pope, 1988), rhesus macaques (Buikstra, 1975), yellow baboons (Bramblett, 1967), and other cercopithecines (Chapman and Legge, 2009) have reported no significant differences between male and female frequencies. Male Japanese macaques exhibit more

43 fractures of the trunk, whereas females have more manual and pedal fractures (Nakai,

2003).

2.3 Field studies of primate positional behavior

Examining the behavioral aspects of locomotion through the analysis of habitual locomotor tasks involves an understanding of the features of the primate geographical distribution (Ripley, 1967). The vast majority of primates are distributed geographically in regions located between the Tropics of Cancer and Capricorn. They occupy several diverse habitats, including rain forests, seasonal forests, savannahs, semi-desert scrub biomes, and tropical and temperate woodlands (Nystrom and Ashmore, 2008). Tropical rain forests are typified by prolific rainfall, temperature variations throughout the day that exceed the variations throughout the year, and high humidity. Rain forests typically are structured into the understory, the main canopy, and emergent trees (Cannon and

Leighton, 1994). As a very rough estimate of heights, the understory of tropical rain forests reaches to approximately 10 meters in height, followed by the midlevel 10-25 meters above the ground, and the canopy which soars 25-50 meters above the ground

(Nystrom and Ashmore, 2008). Rainforests may be further divided into several sub- types: they may be humid or dry depending on rainfall amounts, lowland or montane depending on altitude, or primary or secondary depending on the amount of natural or human disturbance. Gallery forests grow along rivers and streams. Seasonal forests

44 exhibit shifts between wet and dry seasons, seasonal temperate shifts, and the inclusion of forests that are semi- to fully deciduous. Savannahs include predominately grass-filled tropical areas with irregular rainfall dispersal. Semi-desert scrub biomes are hot and dry with sparse vegetation. Tropical woodland forests are composed of smaller trees and shrubs whereas temperate woodland forests are composed of needle-leaf and deciduous trees and may experience deep winter snows (Nystrom and Ashmore, 2008).

The physical structure of biomes and biomechanical factors that prohibit certain actions contribute to the choices made by primates when selecting particular substrates during locomotion (Garber, 2007). In the arboreal canopy, terminal branches are thin and tapering, offering weak, unstable support for animals which use them to feed (Sussman,

1991) and to travel from one tree to another (Cant, 1992). Large vertical tree trunks are separated from each other by significant amounts of space (Cant, 1992). Branches are orientated and positioned in zig zag fashion, increasing the amount of energy required to travel from one location to another (Cant, 1992). Terrestrial environments present a more uniform and stable set of substrates with continuous travel pathways than do arboreal environments (Garber, 2007).

2.3.1 Generalizing and comparing positional behavior

It is difficult to develop a standard set of positional behaviors among primate taxa that vary considerably in body mass, limb and body proportions, allometric growth trajectories, and presence or absence of prehensile or non-prehensile tails (Garber, 2007).

Care must be taken in field studies to assure comparability through removal of

45 observational bias and use of standardized terminology regarding positional classifications, such as those proposed by Hunt and colleagues (1996). They caution that positional behaviors with distinct anatomical requirements must be distinguished, and include classifications for several locomotor and postural behaviors. Figure 2.7 illustrates a few of the more common locomotor behaviors described below (Hunt et al.,

1996).

Figure 2.7 Common locomotor behaviors among primates. A. quadrupedal walk, using palmigrady grip on arboreal substrates (symmetrical gait sequence); B. bound (asymmetrical gait sequence); C. bipedal walk, flexed; D. vertical climb, extended elbow; E. descent, rump- first; F. pronograde leap; G. vertical cling and leap; H. brachiation. I. unimanual suspensory drop. Adapted from Hunt et al. (1996).

Most primates walk quadrupedally on horizontally oriented arboreal and terrestrial supports (Garber, 2007). The quadrupedal walk and run are described as locomotion on top of essentially horizontal supports with pronograde torso (Hunt et al.,

1996). Primates lower their center of mass with respect to the substrate during arboreal quadrupedal locomotion by crouching with flexed elbows (Garber, 2007). Terrestrial 47 quadrupedal primates typically have more adducted limbs, more extended elbows, and more equal distribution of vertical reaction forces between fore- and hind limbs (Garber,

2007). Bipedal walking, running, or hopping may occur with hips and knees extended or flexed (Hunt et al., 1996).

Gait may be symmetrical, in which the left fore limb meets the left hind limb and the right fore limb meets the right hind limb; footfalls of each pair of limbs are evenly spaced. Alternatively, gait may be asymmetrical, in which both fore limbs move forward at the same time and both hind limbs move forward at the same time; footfalls of one or both pairs of limbs are unevenly spaced (Hildebrand, 1967; Hunt et al., 1996). Primates are unique among mammals in that they typically use a symmetrical diagonal sequence- diagonal couplet walking gait whereas other placental mammals tend to use a symmetrical lateral gait (Martin, 1990; Garber, 2007). Using terminology developed by

Hildebrand (1967), in a diagonal sequence gait, the sequence consists of movement of the right hind limb followed by the left fore limb, then the left hind limb, and finally the right fore limb. In contrast, the lateral sequence gait consists of the right hind limb being the first to contact the substrate, followed by the right fore limb, then the left hind limb, and finally the left fore limb. Diagonal couplet refers to the predominance of pairs of limbs supporting the body during the sequence of limb movement. In diagonal couplet gaits the footfalls of the fore- and hind limbs on the opposite sides of the body are related in time as a pair, whereas in lateral couplet gaits the footfalls of the fore- and hind limbs on the same sides of the body are related in time as a pair (Hildebrand, 1967). Primates typically distribute more of their weight on their hind limbs than their fore limbs (as is common of cursorial mammals), thereby shifting their center of gravity closer to their

48 hind limbs (Martin, 1990). This hind limb dominance may reduce stress on fore limb joints caused by high ground reaction forces, thereby contributing to greater fore limb joint mobility, an adaptation that is likely linked to the evolution of primate arboreality

(Raichlen et al., 2009). Alternatively, hind limb dominance may alleviate the inherent instability created as a consequence of lateral rolling which theoretically should be observed in animals favoring a diagonal sequence gait (Martin, 1990).

Variation in walking and running also encompasses how the manus and pedes grip and contact supports, including the following contact categories: palmigrady (feet and hands contact supports via the midfoot and the volar region of the palm, respectively), digitigrady (contact via the volar skin over the metacarpal and metatarsal heads and digits), knucklewalking (contact of hands via the dorsal skin over the intermediate phalanges, excluding the hallux; contact of feet via heel-strike plantigrady), fistwalking (contact via the dorsal skin over the proximal phalanges, excluding the hallux), graspwalking (contact in which the hallux and pollex grasp supports and digits align the sides of supports) (Hunt et al., 1996).

Climbing as a term describing locomotor behaviors has been subject to much confusion. For the purpose of this study, climbing involves travel on supports which are angled at greater than 45 degrees and is distinguished from locomotion incorporating any horizontal movement. Climbing may involve ascent (vertical climbing) or descent.

Climbing may be performed with flexed or extended elbows and may include bounding movements, ladder climbing, or bimanual pull-up. Descent may be rump-first, head-first, or sideways (Hunt et al., 1996).

49 Leaping constitutes movement between discontinuous supports in which hind limbs facilitate most of the propulsion. Most anthropoids characteristically perform pronograde leaps. Shorter pronograde leaps typically are used in series to ascend trees, whereas longer leaps typically involve descent, which increases the length of the leap.

More commonly found in prosimians, vertical clinging and leaping involves the use of hind limbs to push off a vertical support from a torso-orthograde clinging posture. VCL maneuvers can be divided into three forms: stretched-out VCL, with the thighs extended at the hip during mid-flight; curled-up VCL, with the thighs flexed at the hip during mid- flight; and limbs-down VCL, with the limbs hanging down during mid-flight. Bridging is a gap crossing maneuver in which the fore limbs assist in locomotion by grasping supports on the other side of the gap and pulling the body across. Another way to cross gaps between trees is to tree sway. This involves using the weight of the body or oscillating the tree, thereby deforming branches, in order to reach the destination tree

(Hunt et al., 1996).

When undergoing suspensory locomotion, the primate grips arboreal supports from underneath them. The torso may be pronograde or othograde. In torso-pronograde maneuvers, the body is roughly parallel to horizontal supports; when the torso is orthograde, the horizontal supports are roughly perpendicular to it. Brachiation constitutes hand over hand orthograde suspensory locomotion, in which fore limbs bear over half the weight of the body and the trunk rotates approximately 180 degrees.

Orthograde clamber (a.k.a., cautious climbing) is similar to brachiation; however, hind limbs also provide support, with all four limbs providing propulsion. Drops involve swinging from on top to underneath a support (Hunt et al., 1996).

50 2.3.2 Limitations to assigning positional behavior classifications

There are many problems associated with assigning a primary mode of locomotion to nonhuman primates and to relating habitual behavior and comparative morphology. From a methodological standpoint, locomotor behaviors represent only 10-

20% of a primate‟s daily activity and often consist of quick behaviors interspersed between long periods of inactivity (Doran, 1992). Both in interspecific and intraspecific comparisons, primates have a diverse locomotor repertoire. For instance, during only four hours of casual observation of the rhesus macaques (Macaca mulatta) at the Cayo

Santiago semi-free range colony, I noted numerous broadly categorized locomotor behaviors, including quadrupedal walking and running in both arboreal and terrestrial space, vertical climbing and descent, pronograde leaping, and bipedality (Figure 2.8).

However, collapsing an entire locomotor repertoire into one or a few activities inevitably results in the conflation of behaviors that are biomechanically distinct (Garber, 2007).

Even within commonly identified dominant locomotor modes, the inclusion of behaviors that exert different forces on the skeleton into a single category becomes a problem

(Walker, 1998). Other factors influencing locomotor patterns include ontogenetic change, habitat use, dominance interactions, predator avoidance, and injury avoidance

(Ripley, 1967).

Figure 2.8 A selection of locomotor modes observed in Cayo Santiago macaques during only four hours of observation, highlighting the diverse locomotor repertoire of the primates. A. CSFS #0B8 walking quadrupedally (symmetrical diagonal sequence-diagonal couplet gait); B. CSFS #0B8 vertical climbing with infant; C. unknown CSFS macaque climbing (head-first descent); D. CSFS #1D5 pronograde leaping.

Despite these concerns, assigning dominant locomotor classifications to primate species for comparative purposes is well-established (Napier and Napier, 1967; Schaffler and Burr, 1984; Anemone, 1990; Swartz, 1990; Demes et al., 1998; Shapiro and Simons,

2002; Ryan and Ketcham, 2005; Bezanson, 2009). Generalized descriptions of locomotor repertoires may be sufficient when undergoing broad-ranging taxonomic assessments (Carlson, 2005), such as in the current study. And skepticism concerning the

52 applicability of comparisons made using disparate studies can be relaxed when assessing behaviorally dissimilar species (Dagosto and Gebo, 1998). But should a primate‟s primary locomotor type be determined based on the behaviors observed as principle survival mechanisms performed under stress (the context of use), as suggested by Napier, or on the behaviors observed most often (the frequency of use), as suggested by Oxnard

(Ripley, 1967)? Although Napier implies that the most skillful form of locomotion is the primary survival mechanism, thereby greatly influencing evolution, the locomotor behaviors used by primates when under stress may be atypical and unusual (Ripley,

1967).

It is important to note as well that comparisons made of observations of primate behavior amongst primate species are complicated by differing data collection protocols.

Sampling decisions include determining whether observations should be made of a particular focal animal (individual or focal sampling) or of all visible members of a group

(group or scan sampling) (Altman, 1974; Fragaszy et al., 1992). Behaviors may be recorded based on the location in which a focal animal is first observed or when it disappears from view; both are recorded by Martin (1973). Fragaszy and colleagues

(1992) compared individual and group sampling of the activity budgets of Cebus olivaceus conducted by Fragaszy and Saimiri oerstedi by Boinski, determining that rankings and means of the variables tested remained consistent across both individual and group sampling methods, although differential visibility in the group sampling did introduce some slight measurement errors. Altmann (1974) preferred focal animal sampling due to its lack of bias, comparatively, and the range of questions that can be addressed with it.

53 Behavioral sampling constitutes collecting data based on the number and frequency with which a given behavior occurs. Ad libitum sampling is considered to be one of the most common forms of behavior recording, consisting of non-systematic observations of behaviors (Altmann, 1974). It is prone to bias based upon differential visibility of some individuals as well as differential conspicuousness of certain behaviors

(Altmann, 1974) although it is recommended when used in combination with other techniques for recording infrequent events in order to maximize the number of cases recorded (Fragaszy et al., 1992). Continuous sampling records all sequences within long time intervals, continuing to record activities after the recording period is over until the activity changes (see Rose, 1977, 1979). Locomotor bout sampling is a type of continuous sampling which records all movement sequences for each locomotor type observed, such as the methodological approaches taken by Fleagle and Mittermeier

(1980), Cant (1987), and Gebo (1987). Bout sampling depicts a measure of the total frequency of the behavior being observed (Wright et al., 2008). It allows for the determination of the distance travelled in each locomotor mode, although other behaviors cannot be sampled independent of locomotor events while sampling is underway (Doran,

1992). Instantaneous sampling and the similar point sampling (see Schön Ybarra, 1984) techniques record behaviors occuring only during pre-set time intervals, such as the approaches used by Garber (1980), Fontaine (1990), Hunt (1991a), and McGraw (1996).

Instantaneous time sampling permits determination of the degree to which locomotor behavior contributes to the entire activity budget and is more easily used in conjunction with the collection of other ecological data, although rare or brief locomotor behaviors

54 (Doran, 1992) or quieter activities performed by more distant individuals (Fragaszy et al.,

1992) may be underrepresented.

In general, it is assumed that results obtained from bout and instantaneous time sampling will be comparable, although the duration of behavior may affect results slightly (Dagosto and Gebo, 1998). Doran (1992) compared instantaneous and bout sampling methods in a study of male Pan troglodytes positional behavior, determining that the two methods yielded similar estimates of behavior, as long as bouts were weighted with information about distance travelled. She suggests employing both methodological approaches simultaneously in order to alleviate the negative aspects of each method. However, in a similar study comparing the techniques in lemurid positional behavior, Dagosto (1994) determined that, although the two methods were comparable under some conditions, they yielded statistically significantly different results in the case of Eulemur rubriventer even when bouts were corrected by distance travelled, suggesting that it is not distance that should be corrected, but rather time duration

(Dagosto and Gebo, 1998). Rose (2000) compared focal instantaneous (interval) and focal continuous sampling methods used to study activity budgets in Cebus capuchinus.

She determined that there were no significant differences in the results obtained, although some estimates of particular activities were inflated during interval sampling. Interval sampling is more time-effective but less stringent in obtaining full records of activities than continuous sampling. However, certain behaviors may be under-represented during difficult sampling conditions when performing continuous sampling (Rose, 2000).

55 2.3.3 Positional behavior for each representative species

Twenty-one primate genera (including one genus with two representative species and two genera which include two or more species pooled into one genus each) are examined in this study (Figures 2.9-2.12). I have attempted to employ the currently accepted species and subspecies taxonomic nomenclature for each species. Despite the relative paucity of studies specifically aimed at documenting quantitative accounts of positional behavior in wild primates (Dagosto and Gebo, 1998), behavioral information concerning locomotor and height preferences is included below for each of the taxonomic groups examined in this study. Published field studies reporting frequency data on the degree of arboreality, height above ground ranges, and common locomotor modes are included. Information concerning the study area and sampling procedures implemented for each field study also is available. Tables 2.3-2.5 present the compilation of all of the field studies described below, adapted to fit the tabular form used for this dissertation.

These data were pooled to create the full positional profiles, a process which is described in more detail in the methods chapter. Acquisition information pertaining to the museum specimens used for this study, although sometimes lacking in details, also is included.

By comparing museum acquisition data with current geographic distributions, more accurate profiles have been attempted, matching skeletal samples with the positional behaviors they were most likely to have used in life while accounting for habitat differences when possible.

Figure 2.9 Survey of primates examined in this study. See Figure 2.12 for caption information.

Figure 2.10 Survey of primates examined in this study, cont. See Figure 2.12 for caption information.

Figure 2.11 Survey of primates examined in this study, cont. See Figure 2.12 for caption information. 59

Figure 2.12 Survey of primates examined in this study, cont. A. Microcebus murinus, photo credit: J. Visser (WPRC Library, 2010). B. Propithecus verreauxi, photo credit: Herbert Gustafson (WPRC Library, 2010). C. Eulemur fulvus, photo credit: David Blank (Myers et al., 2006). D. Galago senegalensis, photo credit: R. A. Barnes (WPRC Library, 2010). E. Otolemur crassicaudatus, photo credit: Anne Barrett Clark (WPRC Library, 2010). F. Aotus lemurinus, photo credit: Luiz Claudio Marigo (WPRC Library, 2010). G. Alouatta seniculus, photo credit: Roy Fontaine (WPRC Library, 2010). H. Saguinus oedipus, photo credit: Richard Frazier (WPRC Library, 2010). I. Leontopithecus rosalia, photo credit: Richard Day (WPRC Library, 2010). J. Cebus apella, photo credit: David Blank (Myers et al., 2006). K. Saimiri boliviensis, photo credit: Rosie Bolen (WPRC Library, 2010). L. Chlorocebus pygerythrus, photo credit: Anne Barrett Clark (WPRC Library, 2010). M. Macaca fascicularis, photo credit: Roy Fontaine (WPRC Library, 2010). N. Macaca mulatta, photo credit: Heather Jarrell. O. Papio anubis, photo credit: Dennis Rasmussen (WPRC Library, 2010). P. Mandrillus sphinx, photo credit: Verena Behringer (WPRC Library, 2010). Q. Procolobus badius, photo credit: Scott McGraw. R. Colobus guereza, photo credit: Júlio César Bicca-Marques (WPRC Library, 2010). S. Hylobates lar, photo credit: Michael Pogany (WPRC Library, 2010). T. Pongo pygmaeus, photo credit: Phil Myers (Myers et al., 2006). U. Pan troglodytes, photo credit: Alain Houle (WPRC Library, 2010). V. Gorilla gorilla, photo credit: Rick Murphy (WPRC Library, 2010). 60 Table 2.3 Comparison of the degree of arboreality in primates A1 S2 Terr3 Arb4 Sources Microcebus murinus 5 A (~9.85) (~90.15) Martin (1973) Propithecus verreauxi A 2 98 Richard (1974) Eulemur fulvus 6 L 32 68 Gebo (1987) Eulemur fulvus A 2 98 Ward & Sussman (1979) Galago senegalensis A 4.59 95.41 Crompton (1983) Otolemur crassicaudatus A 0.02 99.98 Crompton (1983) Aotus lemurinus 7 A A, M 0 100 Thorington et al. (1976) Aotus lemurinus A 0 100 Moynihan (1964) Alouatta seniculus A 0 100 Mittermeier & van Roosmalen (1981) Alouatta seniculus T A 27.7 72.3 Schön Ybarra (1984)

61 Saguinus o. geoffroyi A A 1.8 98.2 Garber & Sussman (1984)

Saguinus m. midas A 0 100 Mittermeier & van Roosmalen (1981) Leontopithecus rosalia 6 A A 1 99 Rosenberger & Stafford (1994) Leontopithecus rosalia A A 2 98 Stafford et al. (1996) Cebus apella A 0 100 Mittermeier & van Roosmalen (1981) Cebus apella A 0 100 Napier & Napier (1967) Saimiri sciureus A 0 100 Mittermeier & van Roosmalen (1981) Chlorocebus pygerythrus R 6.1 93.9 Rose (1979) Chlorocebus pygerythrus L 19.4 80.6 Rose (1979) Chlorocebus pygerythrus L F 10 90 Isbell et al. (1998) Macaca fascicularis A 3 97 Wheatley (1980) Macaca fascicularis A F, H 2 98 Vos et al. (1992) Macaca fascicularis A F, L 0 100 Vos et al. (1992) Macaca mulatta A A 54.80 45.20 Wells and Turnquist (2001) Macaca mulatta A J 44.46 55.5 Wells and Turnquist (2001) Cont.

61 Table 2.3 Comparison of the degree of arboreality in primates, cont. A1 S2 Terr3 Arb4 Sources8 Papio anubis A A 72.2 27.8 Hunt (1992) Papio anubis F A 61.1 38.9 Hunt (1992) Papio anubis A 98.2 1.8 Rose (1977) Papio anubis A 72.1 27.9 Dunbar & Dunbar (1974) Papio sp. A < 70 > 30 Napier and Napier (1967) Mandrillus sphinx A 80 20 Norris (1988) Mandrillus sphinx F 77 23 Norris (1988) Mandrillus sphinx A M 100 0 Jouventin (1975) Mandrillus sphinx 6 A M 100 0 Chang et al. (1999) Mandrillus sphinx 6 A F 75 25 Chang et al. (1999) Procolobus b. badius L F 0.3 99.7 McGraw (1998a)

62 Procolobus b. badius T F 0 100 McGraw (1998a) Procolobus b. badius Fo F 0.2 99.8 McGraw (1998a) Colobus g. caudatus A 0 100 Mittermeier & Fleagle (1976) Colobus guereza A A 2 98 Gebo & Chapman (1995) Colobus guereza R 0.3 99.7 Rose (1979) Colobus guereza L 4.4 95.6 Rose (1979) Hylobates agilis A 0 100 Cannon & Leighton (1994) Hylobates hoolock A 0 100 Islam & Feeroz (1992) Hylobates lar A (~0.5) (~99.5) Vereecke et al. (2006) Pongo pygmaeus T 10 90 Rodman (1984)

Cont. 62 Table 2.3 Comparison of the degree of arboreality in primates, cont. A1 S2 Terr3 Arb4 Sources8 Gorilla g. beringei A M 97.68 2.32 Doran (1996) Gorilla g. beringei A F 91.85 8.15 Doran (1996) Gorilla g. gorilla A A < 80 > 20 Remis (1998) Gorilla g. gorilla L M 97.97 2.03 cited in Carlson (2005) Gorilla g. gorilla L F 90.87 9.13 cited in Carlson (2005) Pan t. verus L A 84 16 Doran (1993b) Pan t. verus A A, M 56.5 43.5 Doran (1993b) Pan t. verus A A, F 38.7 61.3 Doran (1993b) Pan t. verus L M 85.30 14.70 cited in Carlson (2005) Pan t. verus L F 81.80 18.20 cited in Carlson (2005) Pan troglodytes (Gombe) A A 52.8 47.2 Hunt (1992) Pan troglodytes (Gombe) F A 31.0 69.0 Hunt (1992)

Pan troglodytes (Gombe) T > 70 < 30 Wrangham (cited in Rodman, 1984) Pan troglodytes (Mahale) A A 39.3 60.7 Hunt (1992) Pan troglodytes (Mahale) F A 43.2 56.8 Hunt (1992) Pan t. schweinfurthii L M 91.80 8.20 cited in Carlson (2005) Pan t. schweinfurthii L F 87.98 12.02 cited in Carlson (2005) 1. A = activity: T, travel; F, feeding; Fo = foraging; R = resting; L, all locomotion; A, all activities (locomotor and postural) 2. S = subset of population examined: M = males; F = females; A = adults; J = juveniles; H = high ranking; L = low ranking 3. Terr = frequency of terrestriality 4. Arb = frequency of arboreality 5. determined based on frequency in 0-0.5 m height increment 6. observations from captive animals 7. observation includes release of one captive specimen into the wild Cont. 63 Table 2.4 Comparison of the percent of time spent at heights above the ground A1 S2 0-5 m 6-10 m 11-15 m 16-20 m 21-25 m 25+ m Sources Microcebus murinus A 96.97 3.03 0 0 0 0 Martin (1973) Propithecus diadema A A, W 9.73 42.05 28.68 11.98 7.58 0.00 Dagosto (1995) Propithecus diadema A A, D 19.12 39.90 11.40 10.65 16.88 1.43 Dagosto (1995) Propithecus diadema F A, W 16.95 45.78 19.53 9.73 8.05 0.00 Dagosto (1995) Propithecus diadema F A, D 18.60 20.70 17.17 19.05 21.63 2.83 Dagosto (1995) Eulemur f. rufus 3 (Antserunanomby) A 0.44 2.21 10.95 71.03 15.38 0.00 Ward & Sussman (1979) Eulemur f. rufus 3 (Tongobato) A 1.58 3.80 8.00 70.39 16.23 0.00 Ward & Sussman (1979) Eulemur f. rufus 3 (Antserunanomby) T 0.00 0.00 2.60 87.84 9.56 0.00 Ward & Sussman (1979) Eulemur f. rufus 3 (Tongobato) T 0.95 3.69 5.92 82.94 6.50 0.00 Ward & Sussman (1979) Eulemur f. rufus 3 (Antserunanomby) F 0.00 2.58 15.60 59.66 22.16 0.00 Ward & Sussman (1979) Eulemur f. rufus 3 (Tongobato) F 2.17 11.40 5.01 44.66 36.76 0.00 Ward & Sussman (1979) Eulemur f. rufus 3 (Antserunanomby) L 2.61 0.60 18.14 66.16 12.48 0.00 Ward & Sussman (1979)

64 Eulemur f. rufus 3 (Tongobato) L 6.02 1.27 4.14 78.64 9.93 0.00 Ward & Sussman (1979) Eulemur f. rufus (Talatakely) A A, W 8.90 53.80 25.47 8.73 3.10 0.00 Dagosto (1995) Eulemur f. rufus (Talatakely) A A, D 2.64 40.60 28.70 28.02 0.00 0.00 Dagosto (1995) Eulemur f. rufus (Talatakely) F A, W 13.17 53.97 22.33 8.20 2.37 0.00 Dagosto (1995) Eulemur f. rufus (Talatakely) F A, D 8.43 48.00 27.18 16.40 0.00 0.00 Dagosto (1995) Eulemur f. rufus (Vatoharanana) A 4.8 2.7 16.8 26.2 39.7 9.7 Dagosto & Yamashito (1998) Galago senegalensis 4 A A 84.9 15.1 0.00 0.00 0.00 0.00 Crompton (1983) Galago senegalensis 4 A I 68.5 31.6 0.00 0.00 0.00 0.00 Crompton (1983) Otolemur crassicaudatus 4 A A 24.4 70.8 4.80 0.00 0.00 0.00 Crompton (1983) Otolemur crassicaudatus 4 A I 45.5 51.5 2.90 0.00 0.00 0.00 Crompton (1983) Aotus spp. A 11 89 0 0 0 0 Warner (2002) Aotus trivurgatus A 28 72 0 Wright (1985, 1994)

Cont. 64 Table 2.4 Comparison of the percent of time spent at heights above the ground, cont. A1 S2 0-5 m 6-10 m 11-15 m 16-20 m 21-25 m 25+ m Sources Alouatta seniculus 5 A 0.0 9.4 9.4 40.0 41.2 Mittermeier & van Roosmalen (1981) Alouatta seniculus 3 A 7 9 35 49 Fleagle & Mittermeier (1980) Alouatta seniculus T A, D 2.1 95.8 Youlatos (1998b) Alouatta seniculus T A, W 0.6 98.7 Youlatos (1998b) Alouatta seniculus F A, D 3.1 95.2 Youlatos (1998b) Alouatta seniculus F A, W 4.9 95.1 Youlatos (1998b) Saguinus o. geoffroyi 6 T A 9.3 36.9 53.7 Garber & Sussman (1984) Saguinus m. midas 5 A 1.0 29.6 28.6 32.7 8.2 Mittermeier & van Roosmalen (1981) Saguinus midas 3 A 25 27 30 18 Fleagle & Mittermeier (1980) Saguinus tripartitus A 75.4 23.2 1.4 Youlatos (1999) Saguinus fascicollis A 3 31 38 18 10 0 Warner (2002) Leontopithecus rosalia 3 A A 7 52 41 0 0 0 Stafford et al. (1996) Cebus a. apella A A 5.4 22.9 36.3 35.4 Youlatos (1998a)

65 Cebus a. apella 5 A 2.4 36.6 21.1 27.6 12.3 Mittermeier & van Roosmalen (1981)

Cebus apella A 0 8 46 29 9 8 Warner (2002) Cebus apella 3 A 26 30 32 12 Fleagle & Mittermeier (1980) Cebus albifrons A 46.8 51.1 2.1 Youlatos (1999) Saimiri sciureus A 18 37 27 18 0 0 Warner (2002) Saimiri sciureus A 63.6 36.4 0 Youlatos (1999) Saimiri sciureus 5 A 8.0 61.4 12.5 12.5 5.6 Mittermeier & van Roosmalen (1981) Saimiri sciureus 3 A 55 18 16 11 Fleagle & Mittermeier (1980) Chlorocebus pygerythrus 7 L 48.5 17.0 10.2 7.0 11.1 6.2 Rose (1979) Chlorocebus pygerythrus 7 R 52.4 23.6 9.8 5.3 6.7 2.2 Rose (1979) Macaca fascicularis A F, H 31 44 19 6 0 Vos et al. (1992) Macaca fascicularis A F, L 13 32 45 9 1 Vos et al. (1992) Macaca fascicularis A A low low med med high med Cannon & Leighton (1994) Macaca fascicularis A 1 3 26 41 24 5 Rodman (1978) Macaca mulatta 8 A A 86.49 13.51 0 0 0 0 Wells & Turnquist (2001) Macaca mulatta 8 A J 70.59 29.41 0 0 0 0 Wells & Turnquist (2001) Cont. 65 Table 2.4 Comparison of the percent of time spent at heights above the ground, cont. A1 S2 0-5 m 6-10 m 11-15 m 16-20 m 21-25 m 25+ m Sources Papio hamadryas 9 T 100 0 0 0 0 0 Dunbar & Dunbar (1974) Papio hamadryas 9 T 100 0 0 0 0 0 Hall (1962) Mandrillus sphinx A 66.8 13 8 11 1.2 0 Hoshino (1985) Mandrillus sphinx A high low Norris (1988) Mandrillus sphinx 3 A M high never never never never never Jouventin (1975) Mandrillus sphinx 3 A F, J high high med med never never Jouventin (1975) Mandrillus sphinx 3 A high high never never never never Sabater Pí (1972) Mandrillus sphinx 3 A high high low low low low Harrison (1988) Procolobus b. badius L F, Di 0.3 15 84.5 McGraw (1996) Procolobus b. badius L F, U 0.54 19.9 79.5 McGraw (1996) Colobus guereza 7 L 25.8 24.8 21.6 15.6 8.4 3.8 Rose (1979) Colobus guereza 7 R 15.0 19.6 21.9 17.8 11.4 4.3 Rose (1979)

66 Colobus guereza A A 2 37 61 Gebo & Chapman (1995)

Colobus guereza L A 2 40 58 Gebo & Chapman (1995) Colobus guereza A A, M 1 37 62 Gebo & Chapman (1995) Colobus guereza A A, F 3 37 60 Gebo & Chapman (1995) Hylobates agilis T 0 3 35 62 Gittins (1983) Hylobates agilis F 0 5 54 41 Gittins (1983) Hylobates agilis R 0 0 30 70 Gittins (1983) Hylobates agilis Fo 0 10 42 48 Gittins (1983) Hylobates agilis A A never never never med high high Cannon & Leighton (1994) Hylobates albibarbis A A, M 2 9 52 30 6 1 Cheyne (2010) Hylobates albibarbis A A, F 0 5 45 40 9 1 Cheyne (2010) Hylobates muelleri A 0 0 10 22 37 31 Rodman (1978) Pongo pygmaeus 3 L A, F 38 40 18 3 <1 Cant (1987) Pongo p. abelii L 66 34 Thorpe & Crompton (2005) Pongo p. abelii T 72.5 27.5 Thorpe & Crompton (2005) Pongo p. abelii F 48.5 51.5 Thorpe & Crompton (2005) Pongo pygmaeus A 8 7 7 24 36 18 Rodman (1978) Cont. 66 Table 2.4 Comparison of the percent of time spent at heights above the ground, cont. A1 S2 0-5 m 6-10 m 11-15 m 16-20 m 21-25 m 25+ m Sources Gorilla g. gorilla 10 A A, F 2 8 24 32 34 Remis (1995) Gorilla g. gorilla 10 (group males) A A, M 2 1 19 42 36 Remis (1995) Gorilla g. gorilla 10 (lone males) A A, M 1 1 21 57 20 Remis (1995) Pan t. verus 11 A A, M 61.8 7.8 8.0 21.7 Doran (1993b) Pan t. verus 11 A A, F 48.0 9.3 9.7 31.0 Doran (1993b) Pan t. verus 11 T A, M 94 2 2 2 Doran (1993b) Pan t. verus 11 T A, F 79 8 5 7 Doran (1993b) Pan t. verus 11 F A, M 58 7 8 26 Doran (1993b) Pan t. verus 11 F A, F 48 5 12 34 Doran (1993b) Pan t. verus 11 R A, M 62 14 9 15 Doran (1993b) Pan t. verus 11 R A, F 42 17 20 21 Doran (1993b) 1. A = activity: T, travel; F, feeding; R = resting; Fo = forage; L, all locomotion; A, all locomotor and postural activities. 2. S = subset of population examined: M = males; F = females; A = adults; J = juveniles; I = infants; W = wet season; D = dry season; H = high

67 ranking; L = low ranking; Di = disturbed; U = undisturbed

3. data based on canopy levels. See text for details on this and all subsequent notes. 4. adjusted from author's categories: 0-5.4 m (= 0-5 m), 5.5-9.8 m (= 6-10 m), and 9.9-12.0+ m (= 11-15 m) 5. adjusted from author's categories: 0-3 m (= 0-5 m), 3-15 m (= 6-15 m), 15-20 m (= 16-20 m), etc. 6. data based on tree quadrats 7. adjusted from author's categories: 0-4 m (= 0-5 m), 5-12 m (= 6-10 m), 13-16 m (= 11-15 m), 17-20 m (= 16-20 m), 21-24 m (= 21-25), and 25-28 m (= 25+) 8. data based on vegetation types; adjusted from vegetation 3-13 m tall (= 6-10 m) 9. based on progression in trees and on rocks (heights of sleeping cliffs are not mentioned) 10. adjusted from author's categories: 1-9 m (= 0-10 m), 10-14 m (= 11-15 m), 15-19 m (= 16-20 m), 20-24 m (= 21-25), and 25-30+ m (= 25+) 11. adjusted from author's categories: 0-7 m (= 0-10 m), 7-13 m (= 11-15 m), 13-20 m (= 16-20 m), and >20m (= 21-25+)

67 Table 2.5 Comparison of the frequency with which common locomotor modes are observed in primates 1 A2 S3 Q4 Bi5 C6 Br7 L8 D9 S10 Sources15 Microcebus murinus 11 T 29 <1 24 3 38 … 5 1 Microcebus murinus 12 A high (esp W , H) med high 2, 3 Propithecus verreauxi 11 T 6 3 30 0 46 … 15 1 Propithecus verreauxi A 1 … 18 … P 29 V 53 … … 4 Eulemur fulvus 11 T 39 <1 17 1 34 … 9 1 Eulemur fulvus 11 T Ar 16 0.1 26 … 44 … 13 1 Eulemur fulvus 11 T T 86 1 0 … 13 … 0 1 Eulemur f. rufus A A, W 25.8 … 8.5 … 62.7 … … 5 Eulemur f. rufus A A, D 18.9 … 7.1 … 73.3 … … 5 Eulemur f. rufus T A, W 19.6 … 10.2 … 68.4 … … 5 Eulemur f. rufus T A, D 16.2 … 3.9 … 73.4 … … 5

68 Eulemur f. rufus F A, W 33.5 … 14.7 … 44.1 … … 5 Eulemur f. rufus F A, D 23.1 … 5.6 … 69.5 … … 5 Galago senegalensis A A 19.8 H 2.9 V 16.8, D 3.1 0.4 54.1 … … 6 Galago senegalensis A I 23.3 H 4.8 V 24.5, D 0.0 0.6 45.3 … … 6 Galago senegalensis 11 T 5 2 26 <1 63 … 3 1 Otolemur crassicaudatus A A 40.4 H 0.0 V 29.4, D 0.8 6.2 22.4 … … 6 Otolemur crassicaudatus A I 37.5 H 0.0 V 38.1, D 0.4 3 20.0 … … 6 Aotus lemurinus 12 A high (~45) never (0) med (~35) … med (~20) … never (0) 7, 8 Alouatta seniculus T 80 … 16 … P 4 … … 9 Alouatta seniculus F 59 … 41 … 0 … … 9 Saguinus o. geoffroyi A A 37.8 … 42.3 … 19.9 … … 10 Saguinus m. midas T 76 … 0 … 24 … … 9 Saguinus m, midas F 87 … 2 … 12 … … 9

Cont. 68 Table 2.5 Comparison of the frequency with which common locomotor modes are observed in primates 1 , cont. A2 S3 Q4 Bi5 C6 Br7 L8 D9 S10 Sources15 Leontopithecus rosalia 11 A A W 14, B 30 … V 12 … 34 … 9 11 Leontopithecus rosalia A A W 13, B 14, S 12 … 20 1 38 … 2 12 Cebus a. apella T 84 … 5 … P 10 … … 9 Cebus a. apella F 88 … 8 … P 4 … … 9 Cebus a. apella T A W 31.8, S 10.1 2.1 V 11.4, D, 7.7 13.3 19.7 3.9 … 13 Cebus a. apella F A W 24.2, S 16.7 3.0 V 17.4, D 22.0 3.1 11.3 2.3 … 13 Cebus apella A W 46, B 7, S 3 … 9 9 22 4 … 14 Cebus apella T W 46, B 6, S 2 … 6 7 27 4 … 14 Cebus apella F W 45, B 8, S 3 … 11 11 17 4 … 14 Saimiri boliviensis A 73.6 0.5 4.3 1.0 19.8 0.8 0.3 15 Saimiri sciureus T 55 … 42 … 3 … … 9 … … … … 69 Saimiri sciuereus F 87 11 2 9

Chlorocebus pygerythrus A 48.9 … V 15.2, D 14.3 … 9.6 … … 16 Chlorocebus pygerythrus A F 68.93 … 29.17 … 1.90 … … 17 Macaca fascicularis T M W 65.2, S 16.7 0.0 V 4.9, D 0.5 … 10.8 0.7 C 1.2 18 Macaca fascicularis F M W 74.0, S 13.5 0.0 V 7.7, D 1.1 … 3.6 0.0 C 0.2 18 Macaca fascicularis T A W 59.8, S 15.0 … V 12.0, B 6.0 0.9 P 6.4 … … 19 Macaca fascicularis G A W 10.5, S 1.3 … V 2.6, B 1.3 48.7 P 35.5 … … 19 Macaca mulatta A A 75 2 V 12, B 0 … 11 0 … 20 Macaca mulatta A J 48 1 V 28, B 3 … 17 3 … 20 Papio anubis A A W 98.6, S 0.0 W 0.0 0.7 0.0 P 0.5 … 0.0 21 Papio anubis A A, Ar W 68.3, S 0.0 W 0.0 21.3 0.0 P 10.4 … 0.0 21 Papio anubis 13 A W 96.8 … 3.2 … 183 (no.) … … 22 Mandrillus sphinx 12 A W high (~90) … low (~4.5) (~1) low (~4.5) … … 23

Cont. 69 Table 2.5 Comparison of the frequency with which common locomotor modes are observed in primates 1 , cont. A2 S3 Q4 Bi5 C6 Br7 L8 D9 S10 Sources15 Procolobus b. badius A F 61.3 … 17 … 17.8 … A 3.9 24 Procolobus b. badius T F 64.1 … 12.2 … 20.8 … A 2.9 24 Procolobus b. badius Fo F 58.4 … 21.6 … 15 … A 5 24 Procolobus b. badius A F, Di 61.7 … 16.7 … 18.4 … A 3.3 25 Procolobus b. badius A F, U 60.5 … 17.6 … 16.9 … A 4.9 25 Procolobus b. badius T F, U 64.9 … 12 … 19.4 … A 3.7 26 Procolobus b. badius Fo F, U 55.3 … 24.5 … 14 … A 6.2 26 Procolobus b. badius T F, Di 63.6 … 12.3 … 21.6 … A 2.5 26 Procolobus b. badius Fo F, Di 60.4 … 19.8 … 15.6 … A 4.2 26 Colobus g. caudatus A B high low V low B med … P high med A low 27 Colobus g. kikuyensis A 42.08 4.51 V 8.11, D 9.52 … 34.49 … 1.29 28, 29

70 Colobus guereza A 29.9 … V 20.9, D 15.6 … 19.6 … … 16

Colobus guereza T A 39 0 V 11, B 5 0 44 … <1 30 Colobus guereza F A 43 <1 V 18, B 4 0 33 … 1 30 Hylobates agilis T 7 … 14 … 6 … 74 31 Hylobates agilis T S 4.0 W 12.0, H 14.7 5.3 0.0 P 16.0 … B 48.0 19 Hylobates agilis G S 0.0 W 4.8, H 0.0 0.0 4.8 P 33.3 … B 57.0 19 Hylobates hoolock A <1 4 16 … … … B 80 32 Hylobates albibarbis A A S 11 … 2 … 17 … B 70 33 Hylobates lar A 0.0 5.2 34.1 … 9.5 … B 51.2 34 Pongo p. abelii 14 A 18 7 V 16, D 9 3 P 0 2 B 15, C 20 35 Pongo p. abelii A M 22 5 23 3 0 3 39 35 Pongo p. abelii A A, F 16 8 25 4 1 2 41 35 Pongo p. abelii A J 18 7 27 5 1 4 38 35 Pongo p. abelii 14 T 15 7 V 14, D 8 4 P 0 2 B 16, C 23 35 Pongo p. abelii 14 F 24 8 V 21, D 12 0 P 0 2 B 12, C 14 35 Cont. 70 Table 2.5 Comparison of the frequency with which common locomotor modes are observed in primates 1 , cont. A2 S3 Q4 Bi5 C6 Br7 L8 D9 S10 Sources15 Gorilla g. beringei A A, M 94.30 4.22 0.63 0.21 0.00 36 Gorilla g. beringei A A, F 90.02 6.31 2.65 0.20 0.20 36 Gorilla g. beringei A A, M, Ar 45.45 18.18 27.27 9.09 0.00 36 Gorilla g. beringei A A, F, Ar 52.50 7.50 32.50 2.50 2.50 36 G. g. gorilla (lone males) A A, M, Ar W 22, S 17 0 54 … … … 0 37 G. g. gorilla (group males) A A, M, Ar W 21.5, S 23.7 4.2 42.1 … … … 7.9 37 G. g. gorilla A A, F, Ar W 23.2, S 24.0 2.6 40.0 … … … 4.2 37 Pan troglodytes (Mahale) A A 92.53 0.57 5.17 … 0.00 … 1.72 38 Pan troglodytes (Gombe) A A 94.41 0.56 5.03 … 0.00 … 0.00 38 Pan troglodytes (combined) A A W 93.4, S 0.3 W 0.4 4.9 0.3 P 0.1 … 0.5 21 Pan troglodytes (combined) A A, Ar W 36.7, S 2.3 W 6.7 48.9 2.4 P 0.4 … 5.9 21 Pan t. schweinfurthii A A, M 93.85 0.26 4.27 0.26 0.60 36

71 Pan t. schweinfurthii A A, F 91.49 0.28 5.96 1.23 0.95 36

Pan t. verus A A, M 86.6 1.2 11.1 0.0 1.1 39 Pan t. verus A A, F 85.6 1.2 10.9 0.6 1.4 39 Pan t. verus A A, M 86.61 1.23 8.33 1.37 1.09 36 Pan t. verus A A, F 85.63 1.16 9.29 1.89 1.45 36

Cont. 71 Table 2.5 Comparison of the frequency with which common locomotor modes are observed in primates 1 , cont. A2 S3 Q4 Bi5 C6 Br7 L8 D9 S10 Sources15 Pan t. verus T A, M 89.3 0.2 9.6 0.2 0.8 39 Pan t. verus T A, F 85.7 0.0 12.6 0.2 1.5 39 Pan t. verus F A, M 81.1 5.4 9.0 0.0 4.5 39 Pan t. verus F A, F 85.5 4.6 5.3 0.7 3.9 39 Pan t. verus A A, M, Ar 11.6 5.8 76.7 0.0 5.8 39, 40 Pan t. verus A A, F, Ar 30.3 0.8 59.8 1.6 7.4 39, 40 1. terminology based on descriptions in Hunt et al. (1996) 2. A = activity: F, feeding; Fo = Forage; T, travel; G, gap crossing; A, all 3. S = subset of population examined: M = males; F = females; A = adults; J = juveniles; I = infants; W = wet season; D = dry season; Ar = arboreal; T = terrestrial; Di = disturbed; U = undisturbed 4. Q = % quadrupedalism: (arboreal & terrestrial) W, walk/run; B, bound; S, scramble (= pronograde clamber) 5. Bi = % bipedalism: (arboreal & terrestrial) W, walk/run; H, hop (= step) 6. C = % climbing: V, vertical climb; B, vertical bound (= pulse climb, hop, shinny); D, vertical descent

72 7. Br = % bridging

8. L = % leaping: P, pronograde leap; V, vertical cling and leap 9. D = % drop 10. S = % suspension: A, arm-swing; B, brachiate; C, orthograde clamber (= cautious climb) 11. observations from captive animals 12. estimate of frequencies based on qualitative accounts. See text for specifics. 13. leaping data is not included as a frequency with the other locomotor modes but rather as the number of instances observed throughout the day 14. Thorpe & Crompton (2006) also include tree sway (6%, all; 7%, travel; 1%, feed) and pronograde suspension (4%, all; 3%, travel; 5%, feed) 15. Sources = 1. Gebo (1987); 2. Martin (1972); 3. Petter (1962); 4. Lawler (2006); 5. Dagosto (1995); 6. Crompton (1983); 7. Moynihan (1964); 8. Wright (1981); 9. Fleagle & Mittermeier (1980); 10. Garber and Sussman (1984); 11. Rosenberger & Stafford (1994); 12. Stafford et al. (1996); 13. Youlatos (1998a); 14. Wright (2007); 15. Fontaine (1990); 16. Rose (1979); 17. Isbell et al. (1998); 18. Cant (1988); 19. Cannon & Leighton (1994); 20. Wells & Turnquist (2001); 21. Hunt (1991b); 22. Rose (1977); 23. Sabater Pí (1972); 24. McGraw (1998a); 25. McGraw (1996); 26. McGraw (1998b); 27. Mittermeier & Fleagle (1976); 28. Morbeck (1977); 29. Morbeck (1979); 30. Gebo & Chapman (1995); 31. Gittins (1983); 32. Islam & Feeroz (1992); 33. Cheyne (2010); 34. Fleagle (1980); 35. Thorpe & Crompton (2006); 36. cited in Carlson (2005); 37. Remis (1998); 38. Hunt (1992); 39. Doran (1993b); 40. Doran (1993a)

72 Microcebus murinus

The grey or lesser mouse lemur (Microcebus murinus) is a nocturnal and arboreal

Malagasy primate of the family Cheirogaleidae (Campbell et al., 2007). Mouse lemurs are small (Rose, 1973), females averaging 0.063 kilograms and males averaging 0.059 kilograms (Smith and Jungers, 1997). They are found mainly in closed canopy forests and less commonly in gallery forests and populated rural areas (Burton, 1995). They have been found to be highly flexible in habitat usage compared to other cheirogalids

(Schwab and Granzhorn, 2004) although they nearly always occupy the fine branch niche, even in dry forest areas (Martin, 1972). They travel along branches of all sizes among dense foliage (Napier and Napier, 1967; Burton, 1995). As branch runners they possess short arms and legs relative to their trunk, and long tails (Campbell et al., 2007).

The M. murinus used in the current study were acquired in Amboasary in central

Madagascar. They are solitary, foraging alone at night, sleeping together in tree hole nests which they also use as offspring rearing sites (Rendigs et al., 2003).

Martin (1973) reported on M. murinus in the Mandena forestry reserve of the Fort

Dauphin area in southeastern Madagascar. The heights (in 0.5 meter increments) at which individual Microcebus were active in the Mandena study area were based on initial sightings and points at which the animals disappeared from view. Microcebus were first sighted at heights ranging from 0-5 meters from the ground 96.97% of the time, with the remaining 3.03% sighted at heights of 5-10 meters. They were most commonly observed in the 2-4 meter range (Martin, 1973). Lahann‟s (2008) study of trapped and radio- collared M. murinus at Mandena supports Martin‟s findings. Lahann observed focal

73 animals mainly in the understory and lower canopy at a mean height of 3.0 meters (± 1.8 meters). Sleeping sites were located at a mean height of 4.1 meters (± 1.5 meters).

However, trees in the endemic forest reaching heights greater than 15 meters are sparse.

Martin (1973) cautions that the height at which the animals are most active depends upon the presence of fine branches and dense foliage, and therefore varies from 0-10 meters in secondary forest and pathside vegetation to 15-30 meters in dense primary forests, although they are far more commonly found in secondary forest. Although the degree of arboreality is not provided, it is reported that they spend 90.15% of their time at heights above 0.5 meters and that proportion was used for the arboreality profile for this study.

They do descend to ground level to cross pathways, especially if arboreal pathways would require leaps of greater than 3 meters. They also forage for beetles terrestrially

(Martin, 1973).

The locomotor repertoire of M. murinus is extremely versatile (Martin, 1972).

They most often are described as active arboreal quadrupedalists with considerable leaping capabilities (Napier and Napier, 1967; Walker, 1974; Anemone, 1990; Kimura,

2002). Gebo (1987) observed locomotor patterns among various prosimians housed at the Duke Primate Center. Although frequencies of locomotor bouts were obtained using captive animals, Gebo states that results were comparable to studies based on wild populations. As generalists, M. murinus were observed to leap with the greatest frequency (38% of bouts), although quadrupedalism (29%) and climbing (24%) also were observed quite frequently. Martin (1972) observed the positional behavior of M. murinus, apparently via ad libitum sampling, at five locations throughout Madagascar, with the bulk of observations coming from the aforementioned Mandena study area.

74 Petter (1962) also described the positional behavior of M. murinus via ad libitum sampling at five different habitats zones throughout Madagascar: the east (including study areas in the littoral forests of P rinet Nature Reserve), Tsaratanana plateau, the west (Ankarafantsika and Ampijoroa national parks), Sambirano (Nose-b and Nosy-

Komba forests), and south of Sambirano. Although frequency data are not provided, their descriptions appear to be essentially in accord with the quantitative observations provided by Gebo‟s (1987) captive study. M. murinus are predominantly arboreal, progressing quadrupedally along supports of all inclinations, including bridging small gaps (Martin, 1972). They also utilize jerky, scurrying movements when travelling quadrupedally along branches (Petter, 1962). When terrestrial, they walk and run quadrupedally, but also hop on all four limbs, largely by thrusting with their hind legs

(Petter, 1962; Martin, 1973). This hopping movement has been observed in captive primates as well (Gebo, 1987). Leaps of distances up to 3 meters have been reported, in which the animal lands on all fours (Martin, 1972).

Given that Microcebus typically is classified as quadrupedal, it is possible that M. murinus in the wild might leap less and walk, run, and hop quadrupedally more than in seen in the captive setting described by Gebo (1987). However, M. murinus does exceed the rest of the cheirogalids in leaping proclivities based upon morphometric separations as indicators of morphological adaptations towards leaping (Oxnard, et al., 1981).

Biomechanical analyses further demonstrate the importance of leaping in their repertoire, with hind limb muscle typologies consistent with extensive leaping abilities, yet not to the extent of those seen in dedicated leapers, such as galagos (Legreneur, et al., 2010).

75 Consequently, Gebo‟s (1987) results were used to develop the locomotor mode profile for Microcebus.

Propithecus verreauxi

Verreaux‟s sifaka (Propithecus verreauxi) is a primarily arboreal, diurnal lemur and member of the family Indriidae. They are medium sized primates, averaging 2.95 kilograms in females and 3.25 kilograms in males (Smith and Jungers, 1997). They frequent the trunks and larger branches of dry forested regions throughout the west, south, and southwest of Madagascar (Richard, 1974; Campbell et al., 2007). They flourish in disturbed and secondary growth habitats (Burton, 1995). The P. verreaxi used in the current study were acquired in Amboasary in central Madagascar. Sifaka social groups consist of family groups of 3 to 15 individuals (Burton, 1995).

Four subspecies of Propithecus verreaxi in northwestern and southern

Madagascar were observed to be approximately 98% arboreal (Richard, 1974).

Individual animals were subjects for daily 12-hour observation periods. They fed at almost tree levels (Richard, 1974). A related species, the diademed sifaka (Propithecus diadema), has been shown to vary little in average height above ground observed between wet and dry seasons (Dagosto, 1995). Marked adult sifakas were studied at

Talatakely in the Ranomafana National Park, a forested area in eastern Madagascar, using bout sampling. They were active most often at 6-10 meters from the ground when comparing bouts overall in both wet and dry seasons as well as feeding bouts in the wet

76 season. Feeding during the dry season was also quite active at 6-10 meters, but a slightly higher frequency was exhibited at the 21-25 meter range (Dagosto, 1995).

Sifakas are vertical clingers and leapers (Napier and Napier, 1967; Anemone,

1990). Orthograde leaping from vertical support to vertical support accounts for more than half of their locomotor behavior (Terranova, 1995). During leaps, the position of their fore limbs varies from being held at their sides to above their heads (Walker, 1974) whereas their femora are extended at the hip at mid-flight (i.e., stretched-out vertical cling leap) (Hunt et al., 1996). They hop bipedally when they travel at ground level because their hind limbs are so long (Campbell et al., 2007). Bipedal locomotion also occurs on larger horizontal arboreal substrates (Walker, 1974). Their feeding posture is suspensory (Campbell et al., 2007) as well as upright (Walker, 1974). Lawler (2006) recorded Propithecus verreaxi verreaxi at the Beza Mahafaly Special Reserve vertical leaping 53% of the time and pronograde leaping a further 29% based on locomotor bout sampling. A study of captive prosimians at the Duke Primate Center also revealed that almost half of all locomotor bouts recorded for Propithecus verreaxi constituted vertical clinging and leaping (Gebo, 1987). Neither differences in the structural makeup among various forests (Richard, 1974) nor seasonal variations (Dagosto, 1995) appear to influence the types of locomotor modes commonly employed.

Eulemur fulvus

The diurnal brown lemur (Eulemur fulvus) is a member of the family Lemuridae.

Medium sized primates (Rose, 1973), females average 2.25 kilograms and males average

77 2.18 kilograms (Smith and Jungers, 1997). They occupy all major forest zones, preferring to utilize fine terminal branches horizontal to the ground (Ward and Sussman,

1979; Napier and Napier, 1967). E. fulvus is the most geographically widespread of the true lemurs (Campbell et al., 2007). The Eulemur fulvus sample examined in this study were acquired from the plateau of Ambatondradama in central Madagascar. They live in large multimale-multifemale social groups (Burton, 1995).

E. fulvus is highly arboreal. Burton (1995) states that they are exclusively arboreal. Similarly, Ward and Sussman (1979) reports that they spend less than 2% of their time on the ground. Ward and Sussman‟s findings are based on observations of two populations of Eulemur fulvus rufus at Antiserananomby and Tongobato. In Gebo‟s

(1987) study of prosimian locomotion in captive settings, Eulemur fulvus was observed to progress terrestrially within 0.43 hectare outdoor enclosures with ease, travelling terrestrially 32% of the time. Although determinations of the average ground height at which Eulemur fulvus is active were not recorded at Antiserananomby and Tongobato, it was observed spending over 70% of its time in the continuous canopy, including group travel from site to site (Ward and Sussman, 1979). Adult E. fulvus at Talatakely in the

Ranomafana National Park were observed to be active most often in the 6-10 meter range using bout sampling (53.8% in the wet season and 40.6% in the dry season) (Dagosto,

1995). However, at Vatoharanana, a forest 4 kilometers south of Talatakely with significantly more larger and taller trees, E. fulvus was reported by Dagosto and

Yamashita (1998) to be most active at 21-25 meters (39.7%), followed by 16-20 meters

(26.2%) using instantaneous time sampling.

78 Napier and Napier (1967) classify true lemurs as quadrupedal primates with some similarities to vertical clinging and leaping. Walker (1974) states Lemuridae locomotor behavior largely consists of active to slow arboreal quadrupedal locomotion on upper support surfaces. They generally are considered quadrupedal (Ward and Sussman, 1979;

Campbell et al., 2007). Their leaping ability varies and they are not very agile on small branches (Napier and Napier, 1967). Terranova (1995) notes that they leap less than 50% of the time. The tail is used actively, swung side to side, or arched over the back

(Walker, 1974). Captive E. fulvus have been observed to use quadrupedal locomotion

39% of the time, with leaping behaviors occurring a close second at 34% (Gebo, 1987).

Adult E. fulvus at Talatakely have been reported to leap 62.7% in the wet season and

73.3% in the dry season (Dagosto, 1995).

Galago senegalensis

The Senegal lesser bushbaby (Galago senegalensis) is a nocturnal lorisiform of the family Galagidae. Lesser bushbabies are small (Rose, 1973), females and males averaging 0.199 and 0.227 kilograms, respectively (Smith and Jungers, 1997). They are commonly found in open woodlands of Africa south of the Sahara, but can sometimes inhabit closed forests (Nash et al., 1989). Bushbabies (or galagos) nest in sleeping groups that vary in size seasonally, although they tend to forage individually (Burton,

1995). The practice of urine washing has been shown to assist in enhancing grip during locomotion (Campbell et al., 2007). G. senegalensis also has enhanced depth perception

79 and visual acuity, to assist in gauging leaps (Charles-Dominique, 1977). They prefer to exhibit vertical postures and use high-angled supports (Crompton, 1983).

Crompton (1983, 1984) studied the positional behavior of G. senegalensis at

Mosdene in the northern Transvaal of South Africa using a mixture of bout and instantaneous sampling techniques. They are more terrestrial than O. crassicaudatus

(Crompton, 1983), frequently crossing open ground or foraging for arthropods

(Crompton, 1984). G. senegalensis tends to occupy lower forest levels (Burton, 1995) but can be found at all strata (Campbell et al., 2007). The mean height above the ground at which G. senegalensis was observed at Mosdene was 2.97 meters based on initial support used, although there were few trees in that habitat reaching heights of greater than 10 meters (Crompton, 1984). Infants are more active at greater heights (Crompton,

1983).

Bushbabies are vertical clingers and leapers (VCL) (Napier and Napier, 1967).

Unlike pottos and lorises, bushbabies cross gaps by hopping and leaping, facilitated by the presence of long tails and elongated tarsal bones (Campbell et al., 2007). G. senegalensis is considered the most specialized and frequent of leapers among the

Galagidae (Oxnard et al., 1981; Anemone, 1990). They can leap distances over six times their own body length excluding their tail (Legreneur et al., 2010). They have been observed to leap more than 50% of travel time (Terranova, 1995). Indeed, in a study of captive primates at the Duke Primate Center, leaping was the most common locomotor activity observed in G. senegalensis at 63% (Gebo, 1987). At Mosdene, they were observed to leap in 49.7% of all bouts (Crompton, 1983). During the middle of leaps, their limbs are positioned in front of their bodies, termed curled-up vertical cling leap

80 (Hunt et al., 1996). They also maneuver on branches by quadupedal running, climbing, and jumping (Campbell et al., 2007). Walking and climbing are more common in infants than adults at Mosdene, while leaping, both in frequency and distance travelled, was less often practiced (Crompton, 1983). Nevertheless, high leaping frequencies in G. senegalensis remain constant despite seasonal and habitat variations (Crompton, 1984).

Otolemur crassicaudatus

The thick-tailed greater bushbaby (Otolemur crassicaudatus) is a nocturnal lorisiform of the family Galagidae. They are approximately six times the size of G. senegalensis (Crompton, 1984) and the largest of the bushbabies (Nash et al, 1989).

Females average 1.11 kilograms and males average 1.19 kilograms (Smith and Jungers,

1997). They are found in open forest as well as woodland savannah habitats (Burton,

1995). O. crassicaudatus came from Mozambique and Rhodesia in the current study. As with the lesser bushbabies, urine washing enhances grip during locomotion (Campbell et al., 2007). Living within a noyau social group, O. crassicaudatus are solitary foragers, nesting in sleeping groups that vary in size from one to six individuals (Burton, 1995).

Crompton (1983, 1984) studied the positional behavior of O. crassicaudatus at

Wallacedale in the northern Transvaal of South Africa using a mixture of bout and instantaneous sampling techniques. They rarely reach ground-level (Crompton, 1983,

1984). They are found from mid to high canopy (Campbell et al., 2007). They averaged heights of 6.46 meters above the ground at Wallacedale based on initial support used, in a habitat in which no trees grew higher than 12 meters. Unlike G. senegalensis, infants are

81 more active at lesser heights than adults, possibly due to greater curiosity and lower timidity (Crompton, 1983).

Although Napier and Napier (1967) consider all bushbabies to be vertical clingers and leapers (VCL), O. crassicaudatus leaps with little frequency (Burton, 1995). They are still considered VCL prosimians (Anemone, 1990) although these „infrequent leapers‟ have been observed to practice leaping behaviors during less than 50% of travel time

(Terranova, 1995) and leap the least of all the galagines (Oxnard, et al., 1981). At

Wallacedale, they leaped only 21.2% of the time, preferring qradrupedal progression at

38.95% (Crompton, 1983). They are unable to land hindfeet first when leaping (Nash et al., 1989). Otolemur is more monkey-like in locomotion than other bushbabies, using broad horizontal supports to maneuver quadrupedally (Campbell et al., 2007). They also exhibit behaviors commensurate with slow climbing quadrupedalism (Walker, 1974).

Walking and climbing are more frequent in infants than adults at Wallacedale, but the overall differences in locomotor patterns are small (Crompton, 1983).

Aotus lemurinus

The grey bellied owl monkey or night monkey (Aotus lemurinus) is a medium- sized, arboreal cebid in the family Aotidae (Rose, 1973). Females average 0.874 kilograms and males average 0.918 kilograms (Smith and Jungers, 1997). They occur in tropical rainforests, mixed deciduous forests, and old secondary forests (Fernández-

Duque, et al., 2010), tending to prefer areas of dense canopy (Kinzey, 1997). They are distributed throughout Central and South America, from Panama to Argentina, excluding

82 the Guianian Shield in northeastern South America (Wright, 1994). The Aotus lemurinus examined herein are from Columbia. The only nocturnal anthropoid, owl monkeys have only a single cone type in their orbits and thus lack color vision (Xu et al., 2004). It is suspected that they wait until diurnal predators, including hawks and eagles, are asleep to perform activities, yet balance their timing of nocturnal activity patterns with moments of greatest luminosity, since they may have difficulty moving in complete darkness (Wright,

1989). Observations of Aotus azarai activity patterns in Argentina and Paraguay indicate that owl monkeys are most active at dawn and dusk, and that nocturnal activities are higher during nights with full moons (Fernández-Duque, et al., 2010). Owl monkeys live in family groups of a monogamous adult pair and their offspring (Kinzey, 1997).

Aggressive interactions between social groups have been reported to result in injuries to the face and fore limb in both sexes (Campbell et al., 2007).

Aotus is considered to be completely arboreal. Thorington and colleagues (1976) tracked the movements of a formerly-captive young male A. trivurgatus released into the wild at Barro Colorado Island, Panama. It was fitted with a radio transmitter and occasionally spotted visually. During the day, it was located 10 to 15 meters above the ground; at night, it occasionally dropped as close to the ground as 3 meters (Thorington et al., 1976). Wild Aotus sp. (probably A. trivurgatus) observed ad libitum at Barro

Colorado Island by Moynihan (1964) also never were seen to travel lower than 3 meters above the ground. Aotus trivurgatus in the Manu National Park, a rainforest in Peru, and

La Golondrina Ranch, a tropical dry forest in Paraguay, have been observed using instantaneous sampling to prefer the high canopy, spending 72% of the time at heights of

10 meters or higher (Wright 1985, 1994). Social behaviors, such as traveling, feeding,

83 playing, intergroup fighting, and calling all are performed high in the canopy (Wright

1989). They consistently sleep in the same few trees and have been observed at the

Cocha Cashu study site in the Manu National Park to disappear into the vines of sleep trees at approximately 18 meters above the ground (Wright, 1985). However, it has been suggested that they prefer dense canopy, whether or not it is high or low canopy (Kinzey,

1997). Indeed, Warner (2002) observed Aotus spp. during the daytime at the Bahuaja

Lodge Research Station in southeastern Peru; they determined, probably based on first sightings, that the owl monkeys at that location preferred the lower understory of the disturbed forest. Contrary to Wright‟s (1985, 1994) findings, Warner (2002) reported that Aotus was never spotted more than 10 meters above the ground and was encountered the majority of the time at 5-9 meters above the ground (89%).

Napier and Napier (1967) classify Aotus as arboreal quadrupeds, running, walking, and leaping using their tails for balance (Thorington et al., 1976). As the only nocturnal anthropoid, field studies addressing locomotor behaviors have proven difficult to implement (Fernández-Duque, et al., 2010). Apparently, no quantitative study of the positional behavior of any species of Aotus has been published. However, an estimate of the frequency with which Aotus practice common locomotor behaviors has been made based on a compilation of anecdotal reports. For instance, of the suspensory behaviors, brachiation, armswinging, and suspension by the arms alone have not been observed by

Wright (1981), although captive A. t. griseimembra have been spotted suspending from their hind limbs. Bipedalism also has never been observed (Wright, 1981). Moynihan

(1964) states that, although they run quadrupedally along branches less frequently than

Cebus, Saimiri, or Saguinus, they bound quickly through trees. They are considered

84 powerful leapers, crossing gaps of one to five meters (Wright, 1981), although longer leaps are rare (Thorington et al., 1976). Although Aotus resemble marmosets and tamarins in a number of characteristics (Moynihan, 1964), Aotus rely more on their hands for climbing, rather than their legs for springing, than the callitrichids (Wright, 1981). It is important to note that caution should be taken when relying upon qualitative accounts of locomotor activity, due to the possibility that researchers may tend to stress more dramatic behaviors, thereby underestimating the frequency of more common behaviors

(Garber, 1980).

Alouatta seniculus

Red howler monkeys (Alouatta seniculus) are large-bodied New World monkeys of the family Atelidae (Rose, 1973), averaging 5.21 and 6.69 kilograms in females and males, respectively (Smith and Jungers, 1997). Their habitat includes low rain forests, mountain savannah forests, pine forests, swamps, gallery forests, forest patches, secondary growth and liane forests although they rely heavily on the high forest (Fleagle and Mittermeier, 1980; Mittermeier and van Roosmalen, 1981; Burton, 1995). The

Alouatta seniculus sample was aquired in Columbia, Bolivia, and Trinidad. Howlers typically live in social groups averaging between 3 and 13 individuals, with 2 or 3 adult females in multimale groups (Burton, 1995). They are not commonly physically aggressive, preferring to defend their territory by howling and shaking branches (Napier and Napier, 1967). However, aggression within groups during breeding is intense

(Campbell et al., 2007).

85 Alouatta seniculus in the Raleigh-vallen-Voltzberg Nature Reserve in Central

Surinam were reported by Mittermeier and van Roosmalen (1981) to be completely arboreal. However, Schön Ybarra (1984) reported that adult Alouatta seniculus in Hato

Masaguaral in Venezuela travel along the ground 27.7% of the time, based on observations using point sampling techniques. Schön Ybarra suggests that when provided with the opportunity or inducement to do so, Alouatta will travel terrestrially.

Mittermeier collected data during 1976-1977, stratifying the forest in the Voltzberg study into the shrub layer (0-3 meters), understory (3-15 meters), lower canopy (15-20 meters) middle canopy (20-25 meters), upper canopy (25-30 meters), and emergents (+30 meters)

(Mittermeier and van Roosmalen, 1981). Alouatta was seen most often in the middle and upper canopy based on first sightings (40% in the middle canopy and 28.2% in the upper canopy). They never were observed to enter the shrub layer. In a separate study, during which Fleagle collected data in the Voltzberg study area during 1978, Fleagle and

Mittermeier (1980) also observed that Alouatta prefer to live in the upper and middle canopy based on first sightings among canopy layers. They often move along the tops of branches (Burton, 1995). Youlatos (1998b) compared adult Alouatta seniculus positional behavior in the wet and dry seasons at the Station des Nouragues in French Guiana using focal animal instantaneous sampling. Locomotion overwhelmingly occurred in the main canopy (15 to 30 meters) during travel and feeding in both the wet and dry seasons (95.1-

98.7%). Gebo (1992) reported distinctions in canopy usage based on sex in Allouatta palliata in Costa Rico; females preferred the lower canopy.

Although Napier and Napier (1967) classified the locomotor behavior of Alouatta as New World semibrachiation sub-type of quadrupedalism, the term is no longer in use.

86 Howler monkeys do not use tail-arm suspensory locomotion, in which their prehensile tail assists in brachiation (Garber, 2007). They avoid leaping (Napier and Napier, 1967);

Fleagle and Mittermeier (1980) record leaps in only 4% of travel time. They also avoid swinging by their arms from terminal branches, or traveling on the ground (Napier and

Napier, 1967). Instead, they cross discontinuous supports via cautious pronograde bridging, where at least one extremity maintains contact with a support throughout the locomotor bout (Hunt et al., 1996; Youlatos and Gasc, 2001). Indeed, Alouatta locomote using cautious above-ground quadrupedal walking and running, mixed with climbing and bridging (Youlatos and Gasc, 2001; Garber, 2007). When walking, the heels of their feet contact the supports after their midfeet (Hunt et al., 1996). They use their prehensile tail to support the entire body, for intermittent grasping, for assistance in inverted quadrupedal walking, or to assist head-first descent down vertical supports (Hunt et al.,

1996; Youlatos and Gasc, 2001; Campbell et al., 2007). Commonly, they grip supports using schizodactyl graspwalking, in which digits are aligned on the sides of supports and grasping occurs between the second and third digits (Hunt et al., 1996). Alouatta in the

Voltzberg study area locomote most often by slow quadrupedalism over relatively large branches (80% of bouts observed during travel and 59% of bouts observed during feeding) (Fleagle and Mittermeier, 1980). A further sixteen percent of travel bouts and forty-one percent of feeding bouts involve climbing along smaller branches (Fleagle and

Mittermeier, 1980). Allouatta palliata in Costa Rica were observed to travel along arboreal supports quadrupedally 47% of the time; they also spent time climbing (37%) and bridging (10%) (Gebo, 1992).

87 Saguinus oedipus

Cotton-top tamarins (Saguinus oedipus) are small-bodied (Rose, 1973) New

World monkeys of the family Callitrichidae. Females average 0.404 kilograms; males average 0.418 kilograms (Smith and Jungers, 1997). Marmosets and tamarins possess claw-like nails called tegulae to obtain a secure grip on vertical and near vertical large- branch supports and tree trunks (Garber, 1984). They reside in secondary growth areas with a tangled understory (Burton, 1995) in high and low rain forests, mountain savannah forests, pine forests, and liane forests (Mittermeier and van Roosmalen 1981). The S. oedipus sample used here came from the North Coastal region of Columbia. Their social behavior consists of family groups of two adults, an older juvenile, and an infant (Napier and Napier, 1967). Females are more aggressive than males (Napier and Napier, 1967).

Saguinus oedipus in Panama are largely arboreal, only coming down to the ground 1.8% of the time (Garber and Sussman, 1984) although Saguinus midas midas in the Raleigh-vallen-Voltzberg Nature Reserve in Surinam were reported by Mittermeier and van Roosmalen (1981) to be completely arboreal. The forest was stratified into the shrub layer (0-3 m), understory (3-15 m), lower canopy (15-20 m) middle canopy (20-25 m), upper canopy (25-30 m), and emergents (+30 m), with S. midas seen most often in the middle canopy (32.2%) and understory (29.6%) based on first sightings (Mittermeier and van Roosmalen, 1981). Fleagle‟s separate collection of data in Voltzberg corroborates this, with Saguinus midas preferring the middle canopy (Fleagle and

Mittermeier, 1980). Both Saguinus tripartitus in Ecuador (Youlatos, 1999) and S. fascicollis in southeastern Peru (Warner, 2002) preferred the understory.

88 Cotton-top tamarins are classified by Napier and Napier (1967) as arboreal quadrupeds. They are agile climbers, using their tails for balance (Napier and Napier,

1967). However, unlike squirrels, which travel through the canopy by climbing up and down tree trunks, Saguinus prefer to execute long acrobatic leaps from terminal branches

(Garber, 1980). Saguinus oedipus geoffroyi at the Rodman Naval Fuel Farm in Panama have been observed practicing several locomotor behaviors during feeding and foraging, including quadrupedal progression (37.8%), climbing requiring prehension (42.3%), and jumping (19.9%) (Garber and Sussman, 1984). Data were collected using instantaneous focal animal time sampling and the vertical location of animals were determined by dividing trees into nine quadrats. Jumping (47%) and quadrupedalism (34%) were the most frequently recorded locomotor behaviors in the upper and outermost regions of the canopy, where the majority of locomotor activities occurred (Garber and Sussman, 1984).

Garber (1991) states that the various species of Saguinus employ similar patterns of positional behavior despite exhibiting a range of body weights; quadrupedal progression accounts for approximately half of their locomotor repertoire. However, Fleagle and

Mittermeier (1980) found that S. midas spent less time leaping and more time quadrupedal than Garber suggested.

Leontopithecus rosalia

The golden lion tamarin (Leontopithecus rosalia) is an arboreal New World monkey of the family Callitrichidae. They are small (Rose, 1973), females averaging

0.598 kilograms and males averaging 0.620 kilograms (Smith and Jungers, 1997). They

89 occupy mountainous tropical rain forests, preferring to travel along small branches in the middle and upper canopy (Napier and Napier, 1967). The golden lion tamarins are found only in Southeast Brazil. They live in small groups of 2 to 12 individuals (Burton, 1995).

There is little aggression between males (Burton, 1995). As with other callitrichids, golden lion tamarins possess claw-like nails termed tegulae.

Stafford and colleagues (1996) studied a group of wild adult L. rosalia at the Po o das Antas Biological Reserve near Rio de Janeiro by using a modified focal animal sampling method similar to bout sampling. L. rosalia at the study site were found to be

98% arboreal. When foraging for invertebrates among leaf litter, they were positioned at heights of 2 meters or less. Consequently, categories used to relate height from ground included heights below two meters, the subcanopy (between the canopy and two meters from the ground), and the canopy (with interlocking branches in a continuous environment). Slightly over half (52%) of all activities occurred in the subcanopy

(Stafford et al., 1996).

Leontopithecus are quadrupedal (Napier and Napier, 1967), using an asymmetrical gait when walking, running, and bounding. In a study of captive adult L. rosalia at the Conservation Research Center in Virginia using the modified bout sampling, half of all locomotor bouts consisted of arboreal quadrupedal walking (12%) and transaxial bounding (38%) (Rosenberger and Stafford, 1994). During transaxial bounding, limbs contact supports in equal proportions, the back is relatively unflexed, and hind limbs advance ahead of the fore limbs to meet the substrate (Rosenberger and

Stafford, 1994). Although care should be taken when interpreting locomotor behavior based on captive samples, the authors note that they would not have been able to identify

90 transaxial bounding in wild L. rosalia if they had not first identified in the more controlled captive settings (Stafford et al., 1996). However, captive L. rosalia are more quadrupedal than wild groups, who use quadrupedalism (including walking, bounding, and quadrumanous climbing) and leaping (including leaping and bounding-leaping) with equal frequency (38% each).

Cebus apella

Tufted or brown capuchins (Cebus apella) are medium-bodied New World monkeys of the family Cebidae. Medium sized primates (Rose, 1973), female tufted capuchins average 2.52 kilograms whereas the larger males average 3.65 kilograms

(Smith and Jungers, 1997). Their habitat includes high and low rain forests, mountain savannah forests, pine forests, and liane forests (Mittermeier and van Roosmalen 1981).

They range throughout all types of humid forest, mainly below 500 meters (Burton,

1995). The museum specimens of Cebus apella I examined are from Peru and Bolivia in the tropical Andes. Social groups range from 10 to 35 individuals (Burton, 1995).

Although tufted capuchins form dominance hierarchies, aggression within kin groups is rare (Burton, 1995).

Cebus apella apella in the Raleigh-vallen-Voltzberg Nature Reserve in Central

Surinam were reported to be completely arboreal (Mittermeier and van Roosmalen,

1981). Napier and Napier (1967) also assert that they are completely arboreal, descending to the ground only to drink. The forest was stratified into the shrub layer (0-

3 m), understory (3-15 m), lower canopy (15-20 m) middle canopy (20-25 m), upper

91 canopy (25-30 m), and emergents (+30 m), with Cebus seen most often in the understory

(36.6%) as well as the lower (21.1%) and middle canopy (27.6%) based on instantaneous focal animal sample (Mittermeier and van Roosmalen 1981). It was never seen in the emergent layer (Mittermeier and van Roosmalen 1981). In Fleagle and Mittermeier‟s

(1980) study, C. apella was found to prefer the lower canopy, while remaining active in the middle canopy and understory with slightly less frequency. C. apella in the Bahuaja

Lodge Research Station, Peru, were observed based on the location of the first animal observed within each layer (Warner, 2002). Categories included the shrub layer (0-4 m), lower understory (5-9 m), upper understory (10-14 m), lower canopy (15-19 m), middle canopy (20-24 m), upper canopy (25-29 m), or emergents (+30 m) (Warner, 2002).

Forty-six percent were first observed in the upper understory (Warner, 2002). At the

Station des Nourages in French Guiana, adult C. apella apella prefer the middle (36.3%) and high (35.4%) forest layers (using focal animal instantaneous sampling) (Youlatos,

1998a). Just over half the time (51.5%), C. albifrons in Yasuni National Park in Ecuador were first observed via focal animal instantaneous sampling in the main canopy

(Youlatos, 1999). In short, Cebus apella seem to prefer slightly heights of 16-25 meters.

During travel, Cebus apella in Raleigh-vallen-Voltzberg Nature Reserve are primarily quadrupedal, based on 84% of bouts observed by Fleagle and Mittermeier

(1980). They also have been observed to leap (10%) and climb (5%) when travelling.

During feeding and foraging, 88% of bouts are quadrupedal, 4% involve leaping, and 8% involve climbing (Fleagle and Mittermeier, 1980). Members of the Cebus genus are active and agile quadrupeds, using semi-prehensile tails as temporary anchors to assist in locomotion (Napier and Napier, 1967). The tail grasps supports during torso-pronograde

92 suspensory locomotion, such as inverted quadrupedal walking (Hunt et al., 1996). They occasionally practice bipedalism (Napier and Napier, 1967). Most locomotor bouts recorded for C. apella at Iwokrama Rainforest Reserve in Guyana involve quadrupedal walking (40%) and leaping (22%) (Wright, 2007). They leap slightly more during travel

(27%) and walk slightly more during foraging (45%) Wright, 2007). Adult C. apella apella at the Station des Nourages most frequently walk quadrupedally when travelling

(31.8%) and foraging (24.2%); other frequent behaviors include leaping when travelling

(19.7%) and ascending (17.4%), descending (22.0%), and scrambling (16.7%) when foraging (Youlatos, 1998a).

Saimiri boliviensis

The Bolivian squirrel monkey (Saimiri boliviensis) is a medium-bodied (Rose,

1973) New World monkey of the family Cebidae. Females average 0.711 kilograms and males average 0.911 kilograms (Smith and Jungers, 1997). They occupy a variety of forest types, including gallery, primary, secondary, remnant, mountain savannah, pine, liane, and dry forests (Mittermeier and van Roosmalen 1981; Burton, 1995), although they prefer tropical lowland rainforests (Campbell et al., 2007). The S. boliviensis sample was acquired in Beni, Bolivia. They live in large groups, known on occasion to exceed five hundred individuals (Napier and Napier, 1967). Agonistic behavior in the form of open conflict may occur in order to maintain dominance hierarchies (Burton, 1995).

Saimiri sciureus in the Raleigh-vallen-Voltzberg Nature Reserve in Surinam were reported by Mittermeier and van Roosmalen (1981) to be completely arboreal. Saimiri

93 was seen most often in the understory in both the Mittermeier and van Roosmalen (1981) study at 61.4% and Fleagle and Mittermeier (1980) study at 55%. Saimiri sciureus in the

Bahuaja Lodge Research Station, Peru, were most often first sighted in the lower understory (37%), but they were seen throughout the shrub layer, understory, and lower canopy (Warner, 2002). Saimiri sciureus focal animals in Ecuador were first observed in the understory most of the time (63.6%) and never observed in the emergents (Youlatos,

1999).

According to Napier and Napier (1967), squirrel monkeys are arboreal quadrupeds, often using their tails for balance. Compared to Cebus, the other member of the Cebidae family examined in this study, Saimiri have longer hind than fore limbs, which may be an adaptation to the more frequent leaping characterized by Saimiri

(Campbell et al., 2007). While exploiting the fine branches of the canopy, squirrel monkeys tend to use greater limb excursions rather than aerial phases using their entire body (Young, 2009). This compliant walking is characteristic of arboreal locomotion

(Young, 2009). In a study at the Monkey Jungle, Fontaine (1990) used instantaneous sampling to determine that the most common locomotor behaviors utilized by S. boliviensis peruviensis involved symmetrical quadrupedal cursorial locomotion (61.09% of all quadrupedal locomotion) and slow quadrupedal walking (58.41% of all quadrupedal locomotion). Quadrupedal locomotion constitutes 73.58% of all locomotion; other behaviors observed with less frequency include galloping (5.03%), pronograde leaping (19.83%), pronograde bridging (0.98%), unassisted bipedalism

(0.50%), and quadrupedal climbing (2.07%). They most often take off for leaps from a slow quadrupedal position, take off for drops from a hind limb suspensory position and

94 land from leaps or drops into a quadrupedal pronograde position (Fontaine, 1990). When feeding, Saimiri sciureus in the Voltzberg Nature Reserve preferred quadrupedal movements (87%); however, when travelling, they spent similar amounts of time climbing (42%) and walking, running, and bounding quadrupedally (55%) (Fleagle and

Mittermeier, 1980).

Chlorocebus pygerythrus

Vervet monkeys (Chlorocebus pygerythrus) are Old World monkeys of the family

Cercopithecidae and the subfamily Cercopithecinae. Vervets are large (Rose, 1973), females averaging 2.98 kilograms and males averaging 4.26 kilograms (Smith and

Jungers, 1997). There is some dispute over the taxonomy of the cercopithecines. For the purpose of this research, the updated classification of Chlorocebus pygerythrus is used.

Taxonomic variation includes Cercopithecus aethiops, Chlorocebus aethiops, and

Cercopithecus pygerythrus. Vervets range throughout a diversity of habitats, primarily dwelling in the closed savannah woodlands (Campbell et al., 2007) but also including rainforests, secondary forests, and montane forests (Napier and Napier, 1967). Ch.

Pygerythrus resides in southern and central Africa (Burton, 1995). The C. pygerythrus used in the present study were acquired from various parts of Africa, including Kenya,

Tanzania, Mozambique, Botswana, and South Africa. Vervets live in permanent multimale-multifemale social groups which vary in size from 5 to 75 individuals (Anapol et al., 2005; Burton, 1995). Competition is strong amongst males (Burton, 1995).

95 Vervets typically are considered semi-terrestrial primates (Anapol et al., 2005), although they are not as terrestrial of some other species of Cercopithecines (McGraw,

2002). Rose (1979) studied Chlorocebus pygerythrus in a riparian acacia forest in the

Rift Valley using continuous sampling. They rested terrestrially 6.15% of the time and engaged in locomotor activities terrestrially 19.4% of the time, during which they usually walked while foraging for food. Focal animal instantaneous sampling was used when determining that Chlorocebus pygerythrus at Segera Ranch on the Laikipia Plateau in north-central Kenya are 10% terrrestrial (Isbell et al., 1998). Rose (1979) determined that vervets spent approximately half of their resting (52.4%) and locomotor (48.5%) times at heights within 4 meters of the ground if not actually on the ground.

Vervets are quadrupedal – climbing, jumping, and running on the ground (Napier and Napier, 1967). They are capable of considerable downward jumps (Napier and

Napier, 1967). Vervets in the Rift Valley spend almost half (48.9%) of their locomotor time walking (Rose, 1979). They climb 29.5% and leap 9.6% of their locomotor time

(Rose, 1979). Vervets in Segera are roughly similar to those in the Rift Valley in the rank ordering of the percentage of time spent in locomotor activities: quadrupedalism at

68.93%, climbing at 29.17%, and leaping at 1.90% (Isbell et al., 1998).

Macaca fascicularis

Crab-eating or long tailed macaques (Macaca fascicularis) are Old World monkeys of the family Cercopithecidae and the subfamily Cercopithecinae. They are large, averaging 3.59 (females) and 5.36 (males) kilograms (Smith and Jungers, 1997).

96 They live in primary, riverine, or coastal forests near water sources in Southeast Asia

(Rodman, 1991). The M. fascicularis examined here were collected opportunistically by

Dan Farslowe from the Republic of Palau, an island nation located approximately 500 miles east of the Philippines, and given to Dr. Scott McGraw. The long tail functions most importantly as a rudder during leaping, although it also is used as a brace while climbing or progressing along narrow limbs, as a balance on limbs, or as a counterbalance while sitting (Rodman, 1979). They live in hierarchical social groups of

2 to 100 individuals although the average troop size is 30 (Burton, 1995).

M. fascicularis are highly arboreal (Rodman, 1991) although they have been known to range to ground level (Campbell et al., 2007). Wheatley (1980) observed them on the ground less than 3% of the time near the Hilmi Oesman Memorial Research

Station in the Kutai Nature Reserve, Indonesia. However, without an observer present, that frequency could increase to as much as 10%. Terrestriality, measured in minutes animals spent on the ground observed through continuous sampling, increased over time, as the animals became more habituated to the observer, up to 5% terrestriality (Wheatley,

1980). Based on the results of instantaneous point samples, M. fascicularis mother-infant dyads in Denung Leuser National Park, Indonesia were found to vary in arboreality and typical height from ground categories depending on dominance rank (Vos et al., 1992).

High ranking mothers were 98% arboreal whereas lower ranking mothers were completely arboreal. Lower ranking mothers also stayed higher in the canopy, spending

45% of the time 11-15 meters high, than higher ranking mothers, who averaged 44% of the time in the 6-10 meter high forest level (Vos et al., 1992). Macaques from Gunung

Palung National Park in Borneo, Indonesia were observed to travel 55% of the time in

97 main canopy and to avoid the understory, spending only 2% of travel time there (Cannon and Leighton, 1994). Data were obtained via a modified form of bout sampling measuring locomotor segments. They preferred to travel along structures situated at heights 21 to 24 meters above the ground (Cannon and Leighton, 1994). M. fascicularis in the Kutai Nature Reserve in Indonesia most often were first contacted in the 15-20 meter range (at 41%) and on average were first contacted 17 meters above the ground

(Rodman, 1978).

The most common locomotion for M. fascicularis in Borneo, observed 59.8% of all time travelling, is arboreal quadrupedal walking (Cannon and Leighton, 1994). They have been observed frequently crossing gaps between trees either by bridging (48.7%) in the case of narrow gaps or by pronograde leaping (35.5%) across wider gaps. Cannon and Leighton (1994) also observed them infrequently scrambling (15% of travel time; 1% of gap crossings), climbing (12% of travel time; 3% of gap crossings), and hopping (6% of travel time; 1% of gap crossings). Adult male M. fascicularis from Gunung Leuser

National Park in Sumatra, Indonesia were observed using focal animal locomotor bout sampling (Cant, 1988). They spent comparable amounts of time in arboreal quadrupedal locomotion (65.2% of time spent travelling, 64.7% of foraging time, and 74.0% of feeding time). Less frequently, their locomotor repertoire included other modes, such as vertical climbing and descent, pronograde and vertical clambering, pronograde leaping, and dropping (Cant, 1988). Over 70% of locomotion was across continuous substrates, possibly to reduce the risk of falling from less stable smaller branches by travelling along multiple substrates, especially since travel and foraging was most often along substrates with a diameter of less than 4 cm (Cant, 1988).

Macaca mulatta

The rhesus macaque (Macaca mulatta) is an Old World Monkey of the family

Cercopithecidae and the subfamily Cercopithecinae. Large primates (Rose, 1973), females average 8.8 kilograms and males average 11.0 kilograms (Smith and Jungers,

1997). Macaques may live in tropical rain forests, monsoon forests, mangrove swamps, montane forests, temperate forests, and grasslands (Napier and Napier, 1967). They also live in urban habitats such as temples, parks, and roadways (Burton, 1995). Macaques live in varyingly sized social groups of between 20 and 100s of individuals, with well- defined dominance hierarchies both between and within groups (Napier and Napier,

1967; Burton, 1995). Aggression is common, especially among males, which may lead to fights resulting in wounds to the face and body (Burton, 1995).

The rhesus macaques examined in the present study are from the Cayo Santiago semi-free range breeding colony. Cayo Santiago is a 15.2 hectare island located one kilometer off the southeastern coast of Peru at coordinates 18° 09´ N 65° 44´ W

(Rawlings and Kessler, 1986). It consists of two hills, Big Cay and Small Cay, bounded on the southern and eastern sides by steep cliffs sloping down to an isthmus connecting the Cays. Much of the topography consists of a combination of rocky terrain, open ground, and a mangrove swamp. Vegetation substrate types include 3-13 meter tall trees with large horizontal surfaces and arboreal pathways (e.g., Pisonia fragans, Avicennia germmains, Rhizophora mangle, Taguncularia racemosa), 5-8 meter tall trees with smaller more sporatic branches that feature more obstructions to rapid travel (e.g.,

99 Citharexaylum fructicoslum, Tabebulie heterophlla), dense scrub (e.g., Crepodendrum aculeatum, Sida acuta), and palm trees (i.e., Cocos nucifera). (Wells and Turnquist,

2001) A free-range population of rhesus macaques (Macca mulatta) used for biomedical and behavioral research has been housed there since C. R. Carpenter shipped the original stock of 409 macaques from India in 1938 (Rawlings and Kessler, 1986).

M. mulatta is considered one of the most terrestrial species of macaques (Napier and Napier, 1967) although they do seek heights at times to travel, to protect themselves, and to feed (Wells and Turnquist, 2001). Wells and Turnquist (2001) examined the positional behavior and habitat preferences of the Cayo Santiago rhesus macaques using bout sampling. Adults were reported to be 45.2% arboreal while juveniles were slightly more so at 55.5%. Although height above ground information was not obtained, trees at

Cayo Santiago do not reach higher than 13 meters. Adults spend 36.3% of their activities in various types of vegetation (not rocks or the ground) and 37.22% of that vegetation time in substrates which range from 3-13 meters high. Therefore, 13.51% of all arboreal activity in adults occurs at heights of 3-13 meters. Juveniles spend 29.41% (59.37% of

49.54%) of their arboreal time in 3-13 meter vegetation. These are admittedly approximate estimations of height. Adults spend more than half of their arboreal time in branch debris, while juveniles are more diverse in their substrate use (Wells and

Turnquist, 2001).

According to Napier and Napier (1967), macaques are primarily quadrupedal.

Adults at Cayo Santiago are largely sedentary (Wells and Turnquist, 2001). Seventy-five percent of their locomotor bouts involve quadrupedal movements. Younger infants employ a variety of locomotor modes whereas older infants typically locomote in

100 manners similar to adults. Juveniles are more agile and active, leaping and climbing more often than adults (Wells and Turnquist, 2001).

Papio spp.

Savannah baboons (genus Papio) are large Old World monkeys and members of the family Cercopithecidae and the subfamily Cercopithecinae. On average, females and males have body masses of 9.9 and 16.9 kilograms, respectively (Smith and Jungers,

1997). Discrepancies exist in taxonomic classification among the species of Papio, in part based on geographical overlap during which interbreeding occurs (Campbell et al.,

2007). For instance, some scholars include P. anubis as subspecies of P. hamadryas

(Burton, 1995). Due to inconsistencies in museum archival recording and to bolster sample size available for analysis, all hamadryas baboon (Papio hamadryas) and olive or anubis baboon (P. anubis) specimens were conflated under Papio spp. for the purpose of this research. Papio anubis and Papio hamadryas were acquired from the Congo,

Ethiopia, the Cameroons, although about half of the specimens examined were P. anubis from Kenya.

Baboons live in a variety of habitats, including the sub-desert, savannah, forest- savannah mosaic, rainforests, and less frequently living in cliffs (Napier and Napier,

1967). P. hamadryas prefer subdesert steppes, grass plains, and meadows (Burton,

1995). P. anubis prefer forests (Hunt, 1991b). Baboon populations vary considerably in social behavior and have dominance hierarchies (Napier and Napier, 1967). Aggregation

101 sizes range from 7-550 hamadryas baboons in daytime parties and 25-800 hamadryas in sleeping cliffs (Zinner et al., 2001).

Most baboons spend at least 30% of the day in trees, although P. hamadryas are more terrestrial (Napier and Napier, 1967). Hunt (1992) observed positional behaviors among adult P. anubis in the Mahale Mountain and Gombe Stream National Parks, in

Tanzania using instantaneous scan sampling. They were recorded to be terrestrial 72.2% of the time, spending 61.1% of all feeding time and 82.0% of all non-feeding time on the ground. However, P. anubis in the Rift Valley of Kenya were observed via continuous sampling to be 98.2% terrestrial (Rose, 1977). Seven troops of P. anubis (N = 140) in the

Bole Valley, Ethiopia were studied by Dunbar and Dunbar (1974) using instantaneous scan sampling. Of the animals sampled, 27.9% were recorded in trees or bushes during activity counts. Because almost all actual progression takes place terrestrially (see next paragraph for clarification), establishing height from ground frequencies was deemed unnecessary (Dunbar and Dunbar, 1974). Essentially, all progression occurs in the 0-5 meter range.

According to Napier and Napier (1967), baboons are predominantly quadrupedal.

Hunt (1991b) recorded that adult P. anubis in Mahale and Gombe were overwhelmingly quadrupedal walking at 97%, followed by quadrupedal running at 1.6%, climbing at

0.7%, and leaping/hopping at 0.5%. Rose (1977) found that P. anubis were comparably quadrupedal in the Rift Valley at 96.8%, although the only other locomotor category included was climbing at 3.2%. They were observed to leap up 82 and leap down 101 times throughout the daylong observation period; however leaping frequencies were not incorporated into the percentage incidence of positional activities (including locomotor

102 and postural activities). The majority of walking was associated with feeding, with the rest allotted to travel (Rose, 1977). Running, bipedal walking, climbing up and down, leaping, and suspension all were observed yet uncommon activities. Hall (1962) reported that arboreal progression, excluding such arboreal activities as leaping from one branch to another and climbing up and down a tree, never has been observed in the P. ursinius occupying the Cape of Good Hope Nature Reserve and in southwestern Africa.

However, they do spend considerable time climbing near-vertical cliff faces with slopes consistently greater than 70° (Hamilton, 1982). Baboon climbing abilities are considered quite remarkable (Hamilton, 1982).

Mandrillus sphinx

Mandrills (Mandrillus sphinx) are large (Rose, 1973) Old World monkeys, members of the family Cercopithecidae and the subfamily Cercopithecinae. The most sexually dimorphic of all primate species, male mandrills (averaging 31.6 kilograms) are approximately 3.4 times the size of females (Smith and Jungers, 1997; Leigh et al.,

2008). Mandrills live mainly in closed semi-deciduous forests in western central Africa

(Campbell et al., 2007; White et al., 2010). The M. sphinx sample was obtained in Bafia,

Cameroon and Bafuka, Democratic Republic of the Congo. They group together in extremely large permanent social groups of approximately 200-750 mandrills, called hordes, making the best use of space within their home range through intensive use of gallery forests and isolated forest fragments with high botanical diversity (White et al.,

2010). Dominance hierarchies are present (Napier and Napier, 1967).

103 Locomotor data on mandrills are scant, due to difficulties locating and following hordes in densely forested areas (Harrison, 1988; White et al., 2010). They are considered predominantly terrestrial (Harrison, 1988) although they are less so than

Papio (Lahm, 1986). Provisioned semi-free range M. sphinx in a natural enclosed forest in Gabon were found to be 80% terrestrial based on the mean of pooled focal animal scan sampling data (Norris, 1988). At least 70% of the troop was on the ground at all times of the day except near nightfall, when 58% were terrestrial. They are believed to be representative of wild mandrills (Norris, 1988). Similar frequencies of arboreality have been recorded in captive mandrills in Atlanta, USA, based on modified point sampling techniques (Chang et al., 1999). Males were determined to be 100% terrestrial and females 75% terrestrial. Males are also completely terrestrial in Gabon (Jouventin,

1975). Wild solitary mandrills in Rio Muni, Equatorial Guinea tended to be more arboreal than mandrill groups (Sabater Pí, 1972)

Mandrills in Gabon (Jouventin, 1975) and Rio Muni, Equatorial Guinea (Sabater

Pí, 1972) predominantly were active either on the ground or in lower levels of vegetation.

Habitat utilization was stratified in Gabon in that adult males remained at ground level while females and juveniles traversed the undergrowth and middle forest layer

(Jouventin, 1975). However, while Harrison (1988) also noted that mandrills in Gabon, presumably through ad libitum sampling, preferred to travel and forage at ground level or in the understory, they were observed to feed and sleep at all canopy levels, including the high canopy. Based on first sighting values, 66.8% of all activities by mandrills in the

R serve de Faune de Campo, Cameroon take place in the 0-5 meter range (Hoshino,

104 1985). Norris (1988) states that mandrills in Gabon, when arboreal, usually are positioned within 10 meters of the ground.

According to Napier and Napier (1967), mandrills are predominantly quadrupedal. Quantitative data on the locomotor repertoire of M. sphinx at Rio Muni is unavailable; however, a qualitative description is provided (Sabater Pí, 1972). Mandrills spend the majority of their time walking slowly along the ground, foraging. Younger animals run and chase each other. Arboreal progression is also slow. They have been spotted climbing a tree while simultaneously eating fruit; they also climb to hide from predators. They are capable of arboreal leaps spanning 2 meters and terrestrial jumps covering 5 meters (Sabater Pí, 1972). Mandrills have been observed reducing gaps between tree branches by grasping the target branch with one or both fore limbs and pulling the foliage towards them (Charles-Dominique, 1977).

Procolobus badius badius

The Western red colobus (Procolobus badius badius) is an Old World monkey of the family Cercopithecidae and the subfamily Colobinae. They are large (Rose, 1973), females averaging 8.21 kilograms and males averaging 8.36 kilograms (Smith and

Jungers, 1997). The various subspecies of red colobus inhabit tree and shrub savannah, swamps, primary and secondary forests, montane forests, and gallery forests (Burton,

1995; Campbell et al., 2007). The red colobus monkey skeletons used in this study were collected by Dr. Scott McGraw in the Ta Forest, C te d‟Ivoire. In general, red colobines live in multimale, multifemale groups of 25-50 individuals (Campbell et al., 2007),

105 although groups from 5 to 100 have been suggested (Butron, 1995). Predators include humans, chimpanzees, eagles, and leopards (Campbell et al., 2007).

Habitat use among red colobines is influenced by the presence of other species.

Red colobines are more likely to occupy a higher stratum when they are sympatric with black and white colobines (Campbell et al., 2007). They associate with guenons

(Cercopithecus diana) as an antipredation strategy against ground predators at Ta , resulting in red colobines more often observed below the closed canopy and on the ground (Bshary and No , 1997). This polyspecific association is further augmented when

P. badius and C. diana are in the presence of the sooty mangaby (Cercocebus atys)

(McGraw and Bshary, 2002).

The locomotor behavior and habitat preferences of Procolobus badius badius at

Taï were obtained through instantaneous time point sampling (McGraw, 1996, 1998a,

1998b). Females were chosen as focal animals because there were more adult females in the population. When travelling, red colobus monkeys are completely arboreal; they only rarely come to the ground when foraging (0.2%) and overall when locomoting (0.3%)

(McGraw, 1998a). They are most often active at heights of 21-30 meters in both disturbed (42.3%) and undisturbed (47.8%) forests (McGraw, 1996).

P. badius most often walk quadrupedally in both undisturbed (53.6%) and disturbed (52.8%) forests (McGraw, 1996). Quadrupedalism is the predominant locomotor mode during travelling (64.1%) and foraging (58.4%) when combining the data from both forest types (McGraw, 1998a). They climb (17.6%) slightly more than they leap (16.9%) in undisturbed forests, whereas the reverse rank is observed in disturbed forests, where they leap (18.4%) slightly more than they climb (16.7%)

106 (McGraw, 1996). There is no significant difference when comparing locomotor behaviors between the disturbed and undisturbed forests, either when travelling or foraging (McGraw, 1998b).

Colobus guereza

The Guereza black and white colobus (Colobus guereza) is an Old World monkey of the family Cercopithecidae and the subfamily Colobinae. They are large (Rose, 1973), females averaging 9.2 kilograms and males averaging 13.5 kilograms (Smith and Jungers,

1997). They inhabit lowland rain, gallery, and montane forests (Campbell et al., 2007) in

East Africa, Ethiopia, the Sudan, Zaire, Gabon, Nigeria, Tanzania, and the southern

Cameroons (Mittermeier and Fleagle, 1976). C. guereza in this study were acquired from

Africa, Zaire, and Uganda. They can thrive in fragmented and secondary forests (Napier and Napier, 1967). Guereza colobines live in single or multimale groups with multiple females and offspring (Campbell et al., 2007). Groups range in size from 10 to 15 members (Burton, 1995). They are highly territorial, with males especially exhibiting agonistic behavior through vocal and physical displays (Napier and Napier, 1967). Such aggressive behavior is more prominent in groups with more than one male than in single male groups (Campbell et al., 2007). Females rarely behave aggressively (Campbell et al., 2007).

Guerezas seldom travel on ground level (Napier and Napier, 1967). Continuous sampling of adult focal animals in the Kanyawara study area in the Kibale forest,

Uganda, revealed that Colobus guereza are 98% arboreal (Gebo and Chapman, 1995).

107 Rose (1979) studied Colobus guereza in a riparian acacia forest in the Rift Valley using continuous sampling. Guerezas spent only 0.3% of the day resting on the ground and

4.4% of the day engaged in locomotor activities terrestrially. They mainly come to the ground either to pass between tree clumps or to play (Rose, 1979).

Although they prefer the middle and upper canopy (Napier and Napier, 1967;

Mittermeier and Fleagle, 1976), black and white colobines are more likely to occupy a lower stratum than red colobines when they are sympatric and they descend to ground level to cross forest gaps or feed on terrestrial vegetation (Campbell et al., 2007). Rose

(1979) determined that guerezas spent over half (50.6%) of their locomotor time at heights of less than 12 meters and over half (55.4%) their resting time at heights greater than 12 meters. Although their time spent in various locomotor activities was fairly evenly distributed vertically, they were most commonly observed in the 13-16 (21.6%) and 1-4 (21.4%) meter ranges (Rose, 1979). Guereza colobus monkeys at Kibale are more commonly found above 16 meters (Gebo and Chapman, 1995). Males were slightly more likely than females to be active above this height, at 62% and 60%, respectively.

This frequency declined slightly in the combined sample (58%) when they were engaged in locomotor activities (Gebo and Chapman, 1995).

In the past, C. guereza were classified as quadrupedal monkeys practicing Old

World Semibrachiation due to their below branch arm swinging (Napier and Napier,

1967). However, Mittermeier and Fleagle (1976) repudiate these claims, stating that the semibrachiation category does not exist. Based on qualitative observations of a group of

Colobus guereza caudatus in Arusha National Park in Tanzania, they determined that black and white colobus monkeys are primarily arboreal quadrupeds and pronograde

108 leapers. The most common types of quadrupedal locomotion in their repertoire include asymmetrical gait bounding and galloping (Mittermeier and Fleagle, 1976). They commonly use a plantigrade gait (Napier and Napier, 1967). C. guereza leap more frequently than other members of its genus (Nakatsukasa, 1994). Pronograde leaping, especially with a qradrupedal stance on stable substrates upon takeoff, is quite common

(Mittermeier and Fleagle, 1976). Rapid vertical drops of 15 to 30 meters are not unheard of (Mittermeier and Fleagle, 1976) although typically their leaps are horizontal rather than the vertical dropping seen in some other colobines (Nakatsukasa, 1994). When leaping, they brake flights by grabbing branches with both hands and with assistance from their tails (Napier and Napier, 1967). Although landings are usually hind limb-first or with all limbs landing simultaneously on long descents, fore limb-first landings of all distances have been recorded (Mittermeier and Fleagle, 1976). They never were observed brachiating and only rarely were seen arm swinging (Mittermeier and Fleagle,

1976). Guerezas in the Rift Valley divide their locomotor activities into 29.9% walking and running quadrupedally, 36.5% climbing, and 19.6% leaping (Rose, 1979). When travelling, Colobus guereza in Kibale leap (44%) more often than they walk quadrupedally (39%); the opposite case is found when foraging, during which quadrupedalism (43%) is more common than leaping (33%) (Gebo and Chapman, 1995).

Using a combination of focal animal, time scan, and ad libitum sampling, Morbeck

(1977, 1979) observed that Colobus guereza kikuyensis in a remnant montane forest near

Limuru, Kenya, spent 42.08% of the time locomoting quadrupedally and 34.49% of the time leaping.

109 Hylobates spp.

Gibbons (Hylobates) are lesser apes of the family Hylobatidae. In order to bolster sample sizes, several species of gibbon have been examined for this study, including the agile or black-handed gibbon (H. agilis), the Bornean white-bearded gibbon (H. albibarbis), the black crested gibbon (H. concolor), the hoolock gibbon (H. hoolock), the

Kloss‟ or Mentawai gibbon (H. klossii), the lar or white-handed gibbon (H. lar), the moloch or silvery gibbon (H. moloch), and the Müller‟s Bornean or grey gibbon (H. muerelli). Because almost half of the gibbon samples examined are classified as

Hylobates lar, the behavioral data gathered for the gibbon focuses on that species whenever possible, although Hylobates agilis is apparently a popular study species and has been included as well, when required, to complete the locomotor behavior profile.

Gittins (1983) states that the agile and lar gibbons (both of which feature prominently in my analyses) employ similar forms of locomotion, differing from the larger siamangs in their added mobility during feeding. As all gibbons were pooled for this study, they consequently were acquired from a number of sources, including Thailand, Sumatra,

India, Borneo, Myanmar, and Java. The most common species in this study was H. lar from Chiang Mai province in Thailand. Although among the smallest of the apes, H. lar are large primates, females averaging 5.34 kilograms and males averaging 5.90 kilograms

(Smith and Jungers, 1997).

Gibbons are found in the tropical rain, semi-deciduous, lowland peat swamp, and montane forests of Southeast Asia, preferably in the closed canopy (Napier and Napier,

1967; Quinten et al., 2010). The white handed gibbon (H. lar) social group most often

110 consists of an adult pair and their offspring, although an additional older male may be part of the group as well (Napier and Napier, 1967). Solitary animals also are found

(Napier and Napier, 1967). Conflict increases between juveniles and adults as the former mature, until they leave the social group (Burton, 1995).

Although gibbons are mostly active high in the canopy, during feeding they may ascend to the highest crowns of trees or descend to the ground level (Napier and Napier,

1967; Campbell et al., 2007). Terrestrial movement does occasionally occur when crossing roads or gaps in fragmented forests (Verecke et al., 2006). H. hoolock in

Lawachara and Chunati, Bangladesh, are completely arboreal based on observations taken using instantaneous scan sampling (Islam and Feeroz, 1992). H. agilis in Gunung

Palung are also completely arboreal (Cannon and Leighton, 1994). Captive H. lar at the

Wild Animal Park in Planckendael, Belgium, have been videotaped using bipedal, tripedal, and quadrupedal gaits on the ground (Vereecke et al., 2006). Paired adult H. albibarbis in Sabangau Catchment, Central Kalimantan, Indonesia, prefer to use the 11-

15 meter canopy height even more than it is available in the forest (Cheyne, 2010).

Using focal instantaneous sampling techniques, it has been determined that there is no significant difference in canopy height use in H. albibarbis between males and females

(Cheyne, 2010).

Cannon and Leighton (1994) observed that 32% of all travel by H. agilis in

Gunung Palung National Park in Borneo, Indonesia occurred in the emergent layer of the crown. Data were obtained via a modified form of bout sampling measuring locomotor segments. Hylobates in general are rarely observed in the understory (Cant, 1992) and H. agilis have been observed completely avoiding the understory and lower canopy (Cannon

111 and Leighton, 1994). They travel most frequently at heights 21 to 24 meters and 37 to 40 meters above the ground, while neglecting structures situated at heights 13 to 16 meters high (Cannon and Leighton, 1994). Using instantaneous time scan sampling, Gittins

(1983) reported that Sungai Dal H. agilis spent 62% of the time travelling in the emergent and upper canopy, at heights above 25 meters. They sang at the highest tops of the trees, rested and slept high in the canopy, travelled mostly in the upper canopy, foraged in the upper and middle canopy, and fed in the middle canopy (Gittins, 1983). Hylobates agilis at Sungai Dal, West Malaysia only came within 15 meters of the ground occasionally to travel, forage, or feed; never to sleep, rest, sing, or dispute (Gittins, 1983). H. muelleri also prefer heights, spending 37% of the time at 21-25 meters and 31% of the time above

25 meters (Rodman, 1978).

Gibbons are brachiators (Napier and Napier, 1967). H. lar have been observed brachiating during 51.2% of all locomotor activities (Fleagle, 1980); similarly, H. agilis brachiates 48% of the time when travelling along supports and 57% of travel time spent crossing gaps in the canopy (Cannon and Leighton, 1994). H. agilis at Sungai Dal brachiate 73% of the time (Gittins, 1983). H. albibarbis also are predominantly brachiators (70%) who sometimes leap (17%), scramble (11%), and climb (2%) (Cheyne,

2010). Gibbons typically brachiate into leaps, taking off from horizontally inclined takeoff branches (Cant, 1992). Downwardly directed leaps of up to 15 meters have been recorded (Napier and Napier, 1967). Among H. agilis in Borneo, the most common locomotor mode observed is brachiation (48% of all locomotion while travelling), followed by leaping (at 16%), stepping (15%), bipedal walking (12%), climbing (5%), and scrambling (4%) (Cannon and Leighton, 1994). After bridging (49%) when gap

112 crossing, leaping is the most common locomotor mode observed among H. agilis (36%); leaping is often used to cross wider gaps than those crossed during brachiation (Cannon and Leighton, 1994). Ninety percent of their arboreal locomotion is achieved through arm swinging. (Napier and Napier, 1967). When gibbons exploit resources at the periphery of the tree crown, they use fore limb suspensory behavior to downwardly displace branches, thereby expanding access to food resources (Garber, 2007). They also run bipedally through the trees and, on the rare occasions in which they reach the forest floor, on the ground (Campbell et al., 2007). H. hoolock in Lawachara and

Chunati, Bangladesh, brachiate 80% of the time, climb 16%, walk bipedally 4%, and walk quadrupedally less than 1% of the time (Islam and Feeroz, 1992).

Pongo pygmaeus

Orangutans (Pongo pygmaeus) are arboreal apes of the family Hominidae. They are the largest arboreal mammal; females average 35.8 kilograms and males average 78.5 kilograms (Smith and Jungers, 1997). They are found in the tropical primary rainforests of Borneo (P. pygmeaus) and Sumatra (P. abelii) from swamp forests to more elevated montane forests (Burton, 1995). Pongo pygmaeus skeletons sampled in this study were acquired near several rivers in Borneo. Group composition of orangutans is commonly noyau, consisting of solitary adult males, lone females with offspring, or solitary subadults (Burton, 1995).

They are the most arboreal of the great apes, only rarely seen on the ground

(Thorpe and Crompton, 2006). Although adult males may descend to the ground to travel

113 long distances, orangutans in the Kutai Nature Reserve, Indonesia travel arboreally over

90% of the time (Rodman, 1984). They inhabit all levels of the canopy, feeding among smaller branches and sleeping in nests in the closed canopy (Napier and Napier, 1967).

The majority of locomotor bouts sampled in two adult female P. pygmaeus at the

Mentoko site in Kutai National Park, Kalimantan Timur, Borneo, occurred in the lower main canopy (40%) and understory (38%) (Cant, 1987). P. pygmaeus in Borneo spend

36% of their time at heights from 21-25 meters (Rodman, 1978). In Thorpe and

Crompton‟s (2005) observation of Pongo pygmaeus abelii at the Ketambe Research

Station in Gunung Leuser National Park, Sumatra, Indonesia, using focal instantaneous sampling, the forest was vertically divided into frequencies of time spent above or below

20 meters. When travelling, 72.5 % of travel occurred below 20 meters. When feeding,

48.5% of feeding activities occurred below 20 meters. Adult females tended to travel lower in the canopy; they are four times as likely to travel at heights below 20 meters when compared to males or juveniles (Thorpe and Crompton, 2005).

Napier and Napier (1967) classify Pongo as modified brachiators, although brachiation generally is used only over short distances (Tuttle and Cortright, 1988). They make use of a diverse locomotor repertoire, as expected in large-bodied primates dealing with the difficulties of traversing the spatial discontinuities and fragile supports of the canopy (Thorpe and Crompton, 2006). They are typically considered cautious quadrumanus climbers, grasping supports with both hands and feet (Tuttle and Cortright,

1988; Campbell et al., 2007). Orangutans rarely leap or jump (Napier and Napier, 1967), preferring to employ tree sway or gap bridging (Tuttle and Cortright, 1988; Hunt et al.,

1996). The female orangutans at Mentoko clambered over half of their locomotor time

114 (Cant, 1987). The most commonly occurring locomotor mode among the Ketambe orangutans is torso-orthograde suspensory locomotion (encompassing 35% of all modes encountered), including brachiation and fore limb swing (15%) and orthograde clamber and transfer (20%) (Thorpe and Crompton, 2006). The contact category for their terrestrial gait is fist-walking (Burton, 1995; Hunt et al., 1996) although they have been known to use palmigrade and modified palmigrade postures as well (Tuttle and Cortright,

1988). Orangutans in Ketambe employ tripedal and quadrupedal walking 8% of the time

(Thorpe and Crompton, 2006). Orangutans use hand assisted bipedal locomotion and tree sway along compliant branches to maximize stability in the fine branch niche and reduce the energetic cost of gap crossing (Thorpe et al., 2007, 2009). The Ketambe orangutans walk bipedally 7% of the time and tree sway 4% of the time (Thorpe and Crompton,

2006). Frequencies of the type of locomotor modes used do not vary significantly among age-sex categories, although adult females select more solid and secure supports than males or juveniles (Thorpe et al., 2009).

Gorilla gorilla

Gorillas (Gorilla gorilla) are very large-bodied apes of the family Hominidae.

Weighing approximately 170.4 kilograms, males can grow significantly larger than females, which only weigh approximately 71.5 kilograms (Smith and Jungers, 1997).

They live in lowland and montane rain forests with open canopies, occupying a variety of habitats, depending on the subspecies (Burton, 1995). The gorillas examined in the current study were acquired wildshot from Abong Mbang and Ebolowa, Cameroon and

115 consequently are likely western lowland gorillas (G. g. gorilla). They live in groups of 2 to 35 individuals, typically consisting of a breeding silverback male, several females, and offspring (Burton, 1995). Western lowland gorillas (Gorilla gorilla gorilla) are more arboreal and frugivorous than mountain gorillas (Gorilla gorilla beringei) (Remis, 1998).

They are highly terrestrial, spending 90% of the day on the ground; females and juveniles spend more time in trees than males (Napier and Napier, 1967). Remis studied the positional behavior of western lowland gorillas (G. g. gorilla) at Bai Hokou, Central

African Republic, using instantaneous sampling (Remis 1995, 1998). Because the gorillas were never fully habituated, her data were biased towards arboreal sightings.

Consequently, she could not obtain a specific degree of arboreality, although the gorillas probably are at least 20% arboreal. It has been recorded that female G. g. gorilla engage in arboreal locomotion 9.13% of the time and males spend 2.03% of all locomotion on the ground (Carlson, 2005). Mountain gorillas (Gorilla gorilla beringei) at Karisoke,

Rwanda, (data obtained via instantaneous sampling) are more terrestrial, with females only 9% arboreal and males only 2% arboreal (Doran, 1996). Western lowland gorillas typically spend the majority of their time at heights above 16 meters (Remis, 1995).

During the wet season, they most often were located at heights of 20-24 meters: 32% of the females‟ time, 42% for group males, and 57% for lone males. Activity patterns were significantly different at those heights, with group males typically feeding and lone males typically resting. During the dry season, the 15-19 height range was most frequently used by both group males (98%) and females (42%) (Remis, 1995).

Napier and Napier (1967) classify gorillas as modified brachiators with a quadrupedal gait on the ground whereas Rose (1973) classifies them as knuckle-walking

116 terrestrial quadrupeds. Their common terrestrial gait is knuckle-walking (Burton, 1995).

Gorillas tend to travel arboreally between feeding sites within trees or climb into or out of food trees, descending to the ground to knucklewalk between trees (Remis, 1998). G. g. beringei have been observed be quadrupedal most frequently, whether examining the frequency of quadrupedalism as a proportion of all locomotor behaviors (female: 90.02%; male: 94.30%) or as a proportion of only arboreal locomotor behaviors (female: 52.50%; male: 45.45%) (Carlson, 2005). When examining arboreal locomotion, G. g. gorilla primarily walk quadrupedally (female: 23.2%; group male: 21.5%; lone male: 22%), scramble (female: 24.0%; group male: 23.7%; lone male: 17%), and climb (female:

40.0%; group male: 42.1%; lone male: 54%) (Remis, 1998).

Pan troglodytes

The common chimpanzee (Pan troglodytes) is an African great ape of the family

Hominidae. They are very large primates, females averaging 45.8 kilograms and males averaging 59.7 kilograms (Smith and Jungers, 1997). They live in a variety of forest types, including tropical rain forests, savannah mosaics, deciduous woodlands, montane forests, secondary forests, low-lands, and riverine forests (Napier and Napier, 1967;

Burton, 1995). The common chimpanzees examined in the current study were acquired wildshot from Abong Mbang and Ebolowa, Cameroon and consequently are likely members of the central chimpanzee subspecies (P. t. troglodytes). They sleep in nests in the trees (Napier and Napier, 1967). They show a considerable amount of variation in social behavior marked by fission-fusion social grouping (Burton, 1995). Fluctuations in

117 male coalitions and the nature of the fission-fusion system may require frequent bouts of aggression in order to establish and maintain rank (Campbell et al., 2007). Male territorial interactions both between and within groups are highly aggressive and may result in death (Burton, 1995).

Much of what is known about the locomotor behavior and habitat preferences of chimpanzees comes from two major sources. Doran studied adult P. troglodytes verus in

Taï National Park, C te d‟Ivoire, a lowland evergreen rainforest area. The habitat preferences of P. t. verus at Taï were obtained using a combination of focal animal instantaneous sampling and continuous locomotor bout sampling (Doran, 1993b). Hunt studied adult P. troglodytes in Mahale National Park in Tanzania, a closed forest with extensive vine tangles, and Gombe National Park in Tanzania, an open woodland semi- deciduous forest, using focal animal instantaneous sampling. Mahale receives greater yearly rainfall amounts. Wrangham also studied P. troglodytes at Gombe.

Common chimpanzees are arboreal throughout most of the day light hours

(Napier and Napier, 1967; Burton, 1995). Mahale and Gombe chimpanzees spent 39.3% and 52.8% of a 24 timespan on the ground, respectively (Hunt, 1992). Males were more terrestrial than females at Taï (56.5% and 38.7%, respectively) (Doran, 199b).

Chimpanzees at Mahale (56.8%) and Gombe (69.0%) are slightly more arboreal when feeding (Hunt, 1992). However, Wrangham‟s study of adult male chimpanzees at

Gombe combined with his compilation of other‟s observations of adult females at Gombe determined that chimpanzees travel terrestrially more than 70% of the time, even in closed canopy forests (as cited by Rodman, 1984). Indeed, 84% of all locomotion practiced by P. t. verus in Taï was terrestrial (Doran, 1993b). Frequencies of terrestrial

118 locomotion among male and female adult chimpanzees at all of the above-mentioned locations have been reported to range from 81.80 to 91.80%, with males tending to spend slightly more time involved in terrestrial behaviors (Carlson, 2005).

Among adult P. t. verus at Taï, sex-specific differences in vertical distribution do exist (Doran, 1993b). Females tend to spend greater amounts of time than males at above ground heights, especially heights above 20 meters (31.0% in females and 21.7% in males). Specifically, they spend significantly more resting time above ground compared to males. However, males and females both spend the most time at heights below 11 meters (61.8% and 48.0%, respectively). Males spend 94% of their traveling time below

11 meters (Doran, 1993b).

Napier and Napier (1967) classified Pan as modified brachiators in trees. Rose

(1973) classifies them as knuckle-walking terrestrial quadrupeds on the ground.

Knuckle-walking quadrupedalism accounts for approximately 86% of all Pan troglodytes locomotor behavior (Doran, 1993b). Quadrupedalism constitutes 92.53% of all locomotor behavior at Mahale and 94.41% at Gombe (Hunt, 1992). Doran (1993b) observed P. t. verus practicing several types of arboreal and terrestrial quadrupedalism at

Taï (86.6% of all locomotor time in males and 85.6% in females), including knuckle- walking, modified knuckle-walking, and palmigrade quadrupedalism. Other behaviors include quadrumanous climbing (11.1% in males and 10.9% in females), suspensory behaviors (1.1% in males and 1.4% in females), bipedalism (1.2% in males and 1.2% in females), and leaping (0% in males and 0.6% in females) (Doran, 1993b). Quadrupedal walking accounts for 93.4% of all locomotor behavior when Mahale and Gombe P. troglodytes data are combined, with scrambling (0.3%), bipedal walking (0.4%),

119 climbing (4.9%), bridging (0.3%), pronograde leaping (0.1%), and suspensory behaviors

(0.5%) also present (Hunt, 1991b). Males (93.85%) are slightly more quadrupedal than females (91.49%) (Carlson, 2005). Most arboreal travel involves ascending into or descending from feeding and resting trees rather than arboreal travel between sites

(Doran, 1993a). At Mahale and Gombe combined, almost half of all arboreal travel among P. troglodytes involves climbing (48.9%), with quadrupedal walking (36.7%), scrambling (2.3%), bipedal walking (6.7%), bridging (2.4%), pronograde leaping (0.4%), and suspensory behaviors (5.9%) also present (Hunt, 1991b). When comparing only time spent in arboreal locomotion, quadrumanous climbing constituted the most common type of locomotion in both males and females at Taï – 60.2% and 52.4%, respectively (Doran,

1993b). These frequencies vary only slightly between males and females and between the activities of travelling and feeding at Taï (Doran, 1993b; Carlson, 2005). Common chimpanzees have been observed brachiating over short distances (Ziegler, 1964). When practicing bipedalism in trees, they do so usually at least 15 meters above ground

(Stanford, 2006). They also crutch-walk during steep descents, which consists of a type of terrestrial quadrupedal asymmetrical gait walk (Hunt et al., 1996).

2.4 Chapter summary

Biomechanically, a fracture occurs when one or more mechanical loads produce stresses which exceed the ability of bone to resist deformation. Fracture healing is a

120 complex process during which several types of cells coordinate to regenerate and restore the original tissue. Although many studies have reported fracture patterns and frequencies in human skeletal assemblages in order to address the etiology, epidemiology, and treatment of trauma on individual, population, and sociocultural levels, evaluations of fractures in nonhuman primates are rare. A review of the published accounts of the locomotor repertoire and habitat use preferences of each species examined in this study is provided.

121

CHAPTER 3: Materials and Methods

3.1 Inventory of museum samples

The skeletal material studied in this investigation was chosen based on the availability of large sample sizes for statistical analyses and good bone preservation for ease in macroscopic assessment of trauma. Captive specimens, zoo or circus animals, and research primates were excluded from this study to ensure that any associations between locomotor tendencies and fracture prevalence pertained only to the behaviors of primates in the wild. This also ensured that no measures were taken to treat the injury during the life of the affected animal. Although most museum specimens consisted of wildshot individuals, the Procolobus badius specimens were collected opportunistically and all Macaca mulatta were collected upon their natural deaths. The presence of trauma may render a primate more liable to capture or being shot for a museum due to the primate‟s reduced mobility, thereby overestimating the presence of trauma in that population (Randall, 1944). Alternatively, an injured primate may be less liable to end up in a museum series due to its increased alertness and decreased visibility (Schultz,

1944). Consequently, although this study assumes that the samples included here are representative of natural populations, sample bias may be present.

122 In total, 1672 primates from 22 species encompassing 10 primate families were analyzed. They include the grey mouse lemur (Cheirogaleidae: Microcebus murinus),

Verreaux‟s shifaka (Indriidae: Propithecus verreauxi), the brown lemur (Lemuridae:

Eulemus fulvus), the lesser bushbaby (Galagidae: Galago senegalensis), the thick-tailed bushbaby (Galagidae: Otolemur crasssicaudatus), the grey bellied owl monkey (Aotidae:

Aotus lemurinus), the red howler monkey (Atelidae: Alouatta seniculus), the cotton-top tamarin (Callitrichidae: Saguinus oedipus), the golden lion tamarin (Callitrichidae:

Leontopithecus rosalia), the tufted capuchin (Cebidae: Cebus apella), the squirrel monkey (Cebidae: Saimiri boliviensis), the vervet (Cercopithecidae: Chlorocebus pygerythrus), the crab-eating macaque (Cercopithecidae: Macaca fascicularis), the rhesus macaque (Cercopithecidae: Macaca mulatta), baboons (Cercopithecidae: Papio spp.), the mandrill (Cercopithecidae: Mandrillus sphinx), the guereza colobus (Cercopithecidae:

Colobus guereza), the Western red colobus (Cercopithecidae: Procolobus badius), gibbons (Hylobatidae: Hylobates spp.), the orangutan (Hominidae: Pongo pygmaeus), the gorilla (Hominidae: and Gorilla gorilla), and the common chimpanzee (Hominidae: Pan troglodytes). Table 3.1 lists the number of each species examined as well as the institution from which it came. The specimens currently are housed at the Ohio State

University in Columbus, Ohio; Cleveland Museum of Natural History (CMNH) in

Cleveland, Ohio; American Museum of Natural History (AMNH) in New York, New

York; National Museum of Natural History (USNM) in Washington, D.C.; and the

Carribbean Primate Research Center (CPRC) in San Juan, Puerto Rico. The majority of the primate specimens in the collections at the AMNH, the CMNH, and the USNM were wild shot, whereas the macaques at the CPRC were collected following natural deaths

123 and the specimens at OSU were obtained opportunistically. Records are kept by the museums for most specimens, listing sex, acquisition information, and other demographic information where available.

Table 3.1 Survey of primate skeletons examined for this investigation 1 CMNH AMNH USNM CPRC OSU Total Microcebus murinus 1 21 … … … 22 Propithecus verreauxi … 10 … … … 10 Eulemur fulvus 2 21 6 … … 29 Galago senegalensis … 21 13 … … 34 Otolemur crassicaudatus … … 34 … … 34 Aotus lemurinus … … 85 … … 85 Alouatta seniculus … 63 7 … … 70 Saguinus oedipus 2 … 69 … … 71 Leontopithecus rosalia … 4 34 … … 38 Cebus apella … 92 … … … 92 Saimiri boliviensis … 83 … … … 83 Chlorocebus pygerythrus 4 13 39 … … 56 Macaca fascicularis 2 … … … 36 38 Macaca mulatta … … … 484 … 484 Papio spp. 2 9 17 38 … … 64 Mandrillus sphinx … 18 … … … 18 Procolobus badius … … … … 65 65 Colobus guereza 1 14 39 … … 54 Hylobates spp. 3 38 19 34 … … 91 Pongo pygmaeus 11 13 23 … … 47 Gorilla gorilla 105 … … … … 105 Pan troglodytes 82 … … … … 82 Total: 257 409 421 484 101 1672 1. CMNH = Cleveland Museum of Natural History, Cleveland, OH AMNH = American Museum of Natural History, New York, NY USNM = National Museum of Natural History, Washington, DC CPRC = Carribbean Primate Research Center, San Juan, PR OSU = collection at The Ohio State University, Columbus, OH 2. Papio spp. includes P. anubis (N=34), P. hamadryas (N=30) 3. Hylobates spp. includes H. agilis (N=4), H. albibarbis (N=5), H. concolor (N=2), H. hoolock (N=15), H. klossii (N=8), H. lar (N=43), H. moloch (N=2), H. muelleri (N=12)

124

The Caribbean Primate Research Center (CPRC) is composed of several units.

Select yearlings are relocated annually from the Cayo Santiago field research site (CSFS) to the Sabana Seca Field Station (SSFS) where they may be used for biomedical research purposes along with SSFS-born specific pathogen free animals. Any primate removed to the SSFS will never be reintroduced to the Cayo Santiago population. Monkeys who die at Cayo Santiago are collected, macerated at Sabana Seca, and catalogued and stored at the Laboratory for Primate Morphology and Genetics (LPMG) located in the University of Puerto Rico‟s Medical Sciences campus. Sex, date of birth, age at death, matrilineal associations, and other details are available for every skeleton.

3.2 Macroscopic analyses

Macroscopic examination consisted of a revised version of methods developed for humans by Grauer and Roberts (1996) and nonhuman primates by Lovell (1990a, 1997).

Appendices A and B include the scoring criteria used during data collection and raw data used in these analyses. Long bones (clavicles, humeri, radii, ulnae, femora, tibiae, and fibulae) from each individual were examined for evidence of fractures. Each bone was identified as complete (greater than 90% of the bone present), partial (50-90% of the bone present), fragmentary (less than 50% of the bone present), or absent. Only complete bones were used in this study. Sex, acquisition information, and other available

125 demographic data were recorded for comparative purposes. All fractures were sketched and photographed. Many of the wildshot primates, especially the hominoids, exhibited perimortem fractures which I inferred were sustained incidentally with the bullets that killed them (Randall, 1944). Such fractures were not included in this study. Fractures either exhibited some signs of healing or were not counted.

For each fracture, the type of break (e.g., transverse, oblique, spiral, comminuted, greenstick, partial, avulsion, impacted, or other types) and region of the bone affected

(e.g., diaphysis, head, intercondylar, or other regions) were recorded. The location of the break (e.g., proximal, middle, or distal third of bone) and the side of the body (e.g., left or right) affected also was included. The degree of healing was recorded. If localized periosteal reaction (periostitis or osteomyelitis), callus formation, degenerative joint disease, or any associated trauma (such as gunshot or bite wounds) were present, they were included as well. Localized non-specific infection was used in this study as an indicator of a compound fracture, in which direct contact is made between the bone and the surface of the skin (Grauer and Roberts, 1996). Non-localized periosteal reaction was assumed to be unrelated to the fracture. Individuals with multiple fractures were noted.

Measurements taken of both the affected bone and the unaffected contralateral bone help to quantify bone shortening. Measurements were taken with digital calipers or osteometric boards, depending on the size of the long bone. In order to compare the degree of bone shortening present among primates with such vast differences in body size, the percent difference between right and left elements, based on the longer element, was used.

126

3.3 Radiographic analyses

Radiographs provide a clearer picture of the type of fracture present as well as the extent of healing exhibited by an individual than examination by macroscopic analysis alone. Fractures were radiographed in antero-posterior and medio-lateral views. The extent of callus formation, presence of sclerosis, and revised estimate of the type of trauma observed were recorded. Callus formation and sclerosis assist with the determination of fracture healing. Revising the techniques illustrated by Grauer and

Roberts (1996) for human skeletal samples, the degree of apposition, alignment, and overlap were determined. Apposition is the degree to which fractured bone ends are apposed, expressed as the percentage of surface area united by the two bone fragments

(Lovell, 1997). Apposition was recorded as complete, partial, or absent. Complete apposition (100%) indicates that both bone ends have unified with 100% of their surface area (Lovell, 1997). Absent apposition indicates that 0% of the original fractured bone ends have healed together. Nonunion fractures were not included in this assessment.

Alignment is determined by the direction of displacement of the distal bone fragment compared to the proximal fragment (Lovell, 1997). Alignment was recorded as anterior, posterior, medial, or lateral; clavicular fractures were recorded separately as anterior – clavicle, posterior – clavicle, superior – clavicle, inferior – clavicle. If there was no angulation, it was noted. In the case of nonunion fractures, the label not applicable was used.

127 Radiographs were taken using equipment available on site at the Cleveland

Museum of Natural History, the American Museum of Natural History, and the National

Museum of Natural History. An Aribex NOMAD CE Examiner Portable Dental X-Ray

System, owned by the Ohio State University Department of Anthropology, was used to obtain radiographs at the National Museum of Natural History, the Ohio State University, and the Laboratory for Primate Morphology and Genetics. The NOMAD portable x-ray system operates at a fixed 60 kV operating voltage and 2.3 mA current. Typical exposure time for use in this study was 0.8 – 0.11 seconds. At the Cleveland Museum of Natural

History, courtesy of the Department of Physical Anthropology, a Series 43855A Cabinet

X-ray System by Hewlett-Packard was used. Varying operating levels were required based on the size and density of the bone: voltage ranged from 30-60 kVp, exposure time from 20-40 seconds, and amperage was fixed at 3.0 mA. Films were developed using the

Mini-Medical Series X-Ray Automatic Film Processor (AFP Imaging) on Faxitron

Kodak Portal Pack for Localization Imaging film. At the American Museum of Natural

History, courtesy of the Department of Ichthyology, the Faxitron Series 43807N X-ray

System (Hewlett-Packard) was used with operating levels ranging from 50-135 seconds at 90 kVp. Plain films were developed using standard darkroom procedures on Kodak T

MAT G/RA film. In addition to the NOMAD portable x-ray, two other radiographic systems were used at the National Museum of Natural History (USNM), courtesy of the

Division of Fishes. One x-ray was the Kevex PXS5-724EA MicroFocus (Thermo

Scientific) portable X-ray source mounted above a PaxScan 4030 (Varian Medical

Systems) digital imaging panel with Varian Image Viewing and Acquisition (VIVA) software. It was operated at 68.9 kV and 0.098 mA with a fixed time. The other x-ray

128 system was used for one bone too long to be radiographed by either the NOMAD or the

Kevex systems. It was a Picker Corporation 805-D X-ray machine. Ninety kilovolts were applied at 5 mA for 30 seconds. The film was developed using routine darkroom development procedures on Kodak film.

3.4 Behavioral observations of Cayo Santiago-derived macaques

The macaques at Cayo Santiago are unique in that they have well-documented birth and death dates and, in many cases, behavioral observations obtained from census takers during the lifetime of the animal. Births, deaths, injuries, illnesses, and missing macaques generally are recorded within two days of their occurrence. Recording of injuries consists mainly of a note in daily census logs that an animal was wounded or has been observed limping. Rarely is any other information provided. Information specifically relating to fractures is extremely rare.

Census information was obtained through the Cayo Santiago administrative compound at Punta Santiago in Humacao. It is protocol that only employees are allowed to search the personal field notes kept at Punta Santiago. Therefore, I provided a list of

37 macaques that I had determined had fractures based on my initial findings at the

LPMG. Edgar Davila (Chief Census Taker) and Giselle Caraballo (Assistant Census

Taker) compiled copies of census data on injuries observed in 17 of those animals. I then examined the copies to ascertain whether any of the injuries mentioned in the records

129 potentially could be associated with the fractures I had observed in their skeletons. Only five Cayo Santiago-derived macaques include accompanying observations of injuries they received during their lifetimes. I have included these observations in Appendix C.

Census data consists of wound checksheets and written personal field notes.

Wound checksheets are standardized forms with columns to record the ID tattoo of the affected animal, the date the wound was noticed, the type of wound sustained, the size of the wound (where applicable), and any additional comments. Pictures of a macaque face, an outline of the left side of a macaque body, and an outline of the right side of the body are provided so that the census taker can sketch in the location of the wound. The type of wound may include abrasions, bites, punctures, slashes, inflammation, broken limbs, limps, or other observations. The length, breadth, and deepness of slashes and the diameter of bites are included in the size column. All census data provided was originally recorded by Edgar Davila.

Although the sample size of fractures with accompanying behavioral observations is exceedingly small, it provides an opportunity to assess fracture healing in wild primates on a case by case basis without harming live animals. The age of the fracture was determined by subtracting the date in which the injury was observed from the date of the death of the individual. Both dates are accurate to within two or three days.

It is important to note that it is possible that the injury observed in the census records may not have occurred at the same time as the fracture. The causes of the injuries were not recorded in the census data. Edgar Davila and Giselle Caraballo were not able to recall any specific information about how affected individuals behaved around the rest of their troop or were treated by others subsequent to their injuries.

130 3.5 Development of positional behavior profiles

Locomotor behavior and habitat use profiles were developed for each taxonomic group based upon the results of published accounts. These profiles include frequencies of arboreality and heights above ground as well as the frequency of use of common locomotor modes. The average body mass of representative taxa also was obtained.

Creating locomotor and habitat use profiles allow for a more accurate assessment of primate behavior than simply assigning one primary locomotor mode or canopy level to each species. Although assigning broad locomotor characterizations to representative species is well established in studies which relate the adaptive role of limb morphology to primate locomotor behavior (Cartmill and Milton, 1977; Swartz, 1990; Terranova, 1995;

Demes, et al., 1998; Kimura, 2002; Schmidt, 2005a), more complex approaches are rare and face many challenges (Crompton et al., 1987; Dagosto and Gebo, 1998). Table 3.2 provides a list of what primary locomotor modes have been determined for each taxonomic group by other researchers. Although there is some variability in the terminology used for these determinations, the broad classifications tend to remain consistent. However, some categories, such as the term semibrachiation (Napier and

Napier, 1967; Rose, 1973) have been disputed and are no longer in use (Mittermeier and

Fleagle, 1976). They also favor comparably with the locomotor categories determined to have the largest frequencies in the profiles created for this study, with a few exceptions described below. It is felt that the general agreement amongst researchers bolsters the validity of using these profiles in this study.

131 Table 3.2 Comparison of locomotor classifications in primates Napier and Napier (1967) Martin (1990) Fleagle (1999) Kimura (2002) Microcebus murinus AQ AQ Q (some L)* AQ* Propithecus verreauxi VCL VCL VCL* VCL* Eulemur fulvus AQ AQ Q / L* VCL Galago senegalensis VCL VCL VCL* VCL* Otolemur crassicaudatus VCL … Q (some L)* VCL* Aotus lemurinus AQ AQ Q (some L) AQ Alouatta seniculus Q (NWSB) AQ (NWS) AQ (slow)* AQ* Saguinus oedipus AQ AQ (clawed) AQ* AQ* Leontopithecus rosalia AQ AQ (clawed) AQ* AQ* Cebus apella AQ AQ AQ* AQ* Saimiri boliviensis AQ AQ Q (frequent L) AQ Chlorocebus pygerythrus AQ AQ AQ / TQ* TQ / AQ*

132 Macaca fascicularis TQ TQ (D) or AQ AQ* AQ* Macaca mulatta TQ TQ (D) or AQ Q* TQ / AQ

Papio spp. TQ TQ (D) TQ* TQ* Mandrillus sphinx TQ TQ (D) TQ* TQ* Procolobus badius Q (OWSB) AQ (OWS) AQ AQ / AS* Colobus guereza Q (OWSB) AQ (OWS) AQ (bounding)* AQ / AS* Hylobates spp. BR (true) AS (BR) BR* BR* Pongo pygmaeus BR (modified) AS (QM) QM* KFQ / AS* Gorilla gorilla BR (modified) TQ (KW) / AS (QM) KW* KFQ / AS* Pan troglodytes BR (modified) TQ (KW) / AS (QM) KW / AQ / S* KFQ / AS* Locomotor classifications by genus except when noted by (*), which is by species. Q = quadrupedalism, AQ = arboreal (or branch running) quadrupedalism, TQ = terrestrial (or ground running) quadrupedalism, D = digitigrady, KW = knuckle-walking, KFQ = knuckle or fist quadrupedalism, QM = quadrumanous climbing, L = leaping, VCL = vertical clinging and leaping, S = suspensory, NWS = New World suspensory, OWS = Old World suspensory, AS = arm-swing, BR = brachiation, NWSB = New World semibrachiation, OWSB = Old World semi-brachiation. 132 Determinations of positional repertoires used here comprise data derived from research conducted by numerous authors. Research was conducted at different times in different habitats using multiple, possibly not wholly compatible, sampling procedures.

However, it is not the intention of this study to establish detailed comparative syntheses of primate locomotion but rather to characterize aspects of locomotor behavior and habitat use to assess behavioral positions with low levels of specificity. The absolute values of the frequencies for a given species are less important than the values relative to the other examined species. Refer to the original studies for details of the methods used in each case.

Whenever possible, I have pooled independent studies of each species‟ positional behavior to help moderate the impact of variation between populations within the same species. It is also hoped that grouping the results of independent studies will compensate for the comparability issues connected with reporting behaviors presented as proportions, which necessarily depend on the number of categories used (Dagosto and Gebo, 1998) as well as methodological differences among field studies (Carlson, 2005). In most cases, individual studies pertaining to one species yield results that are relatively similar to other studies of the same species. In general, studies comparing variations in positional behaviors within the same or phylogenetically similar species based on different habitats, season, or both have demonstrated a lack of difference in the rank order in which frequencies of locomotor behaviors are observed. For instance, the most common behaviors remain so despite the habitat or season in which the behaviors are observed

(Dagosto and Gebo, 1998). This reinforces my confidence in the use of these data to calculate a general profile of each species‟ positional behaviors.

133 Quantitative data were obtained from studies performed in wild settings for almost all factors assessed in this study. Unless no other data were available, research on captive animals and qualitative assessments were included in my descriptions of a species

(provided in the introduction chapter) but not factored into the development of the final positional profiles. However, in a few specifically mentioned cases, I was forced to incorporate systematic studies of captive animals or qualitative data from wild animals.

For the purposes of this study, I am interested predominantly in locomotor behaviors, as they involve more active behaviors which are more likely to result in fractures. Obviously, when discussing locomotor modes, only locomotor behaviors are involved. However, when discussing habitat use, including arboreality and height above ground, both locomotor and postural positional behaviors may come into play. For instance, time spent resting in the trees may differ from time spent locomoting. The first involves postural activities whereas the second involves locomotor activities. In those rare cases in which information was not obtained during all activities for arboreality and height above ground, profiles were derived from locomotion or travel activities.

Figure 3.1 depicts the profile developed to describe the degree of arboreality for each taxonomic group examined here. Each profile was created by averaging the data from Table 2.3, excluding data obtained from studies of captive animals. Saguinus oedipus was used, excluding S. midas as a non-target species; however, Saimiri sciureus was used as a replacement for S. boliviensis, as data about the target species was not available. To better match its habitat, only the subspecies Gorilla gorilla gorilla and Pan troglodytes (not P. t. verus or P. t. schweinfurthii) were used.

134 Microcebus murinus Propithecus verreauxi Eulemur fulvus Galago senegalensis Otolemur crassicaudatus Aotus lemurinus Alouatta seniculus Saguinus oedipus Leontopithecus rosalia Cebus apella Saimiri boliviensis Chlorocebus pygerythrus Macaca fascicularis Macaca mulatta Papio spp. Mandrillus sphinx Procolobus badius Colobus guereza Hylobates spp. Pongo pygmaeus Gorilla gorilla Pan troglodytes

0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%

Figure 3.1 Degree of arboreality profiles for each taxa.

Figures 3.2 and 3.3 present the profiles created for the vertical dimension of forest utilization for each species. The profiles were developed by averaging the frequencies for all data included in Table 2.4. In those cases in which categories were combined

(e.g., 0-10 meters instead of 0-5 meters and 6-10 meters), the categories were divided equally to provide frequencies for both categories. If the original authors had used 5 meter categories instead of larger increments, it is likely that frequencies in both categories would not be equal, meaning that the values of one of the categories may be slightly inflated and the other slightly reduced. However, it is hoped that combining data from multiple reports will lessen possible inaccuracies in the profiles. No captive studies

135 were included in this analysis. Non-target species were excluded unless no other data was available, including substituting species information for P. verreaxi and S. boliviensis. P. troglodytes verus was used for P. troglodytes troglodytes even though there may be slight habitat differences between the two subspecies. Only the P. pygmaeus was used, excluding P. abelii.

Figures 3.4 and 3.5 depict the locomotor mode profiles developed for each taxa based on data presented in Table 2.5. Frequencies for bipedalism, bridging, and drop tended to be quite small, unavailable, or zero. Consequently, values for bipedalism were pooled with quadrupedalism, values for bridging were pooled with leaping, and values for drop were pooled with suspension. Only P. troglodytes was included for Pan, to provide the most accurate values possible for their habitat. However, P. abelii and G. g. berengei were used for Pongo and Gorilla, respectively. Captive studies were excluded from the analysis, except for Microcebus as no quantitative studies were available for that genus using data from wild primates.

It is possible that leaping frequencies may be over-estimated for Microcebus.

Traditionally, Microcebus is considered an arboreal quadruped (Napier and Napier, 1967;

Martin, 1990; Kimura, 2002). However, Gebo (1987) reported higher frequencies of leaping than quadrupedalism in captive M. murinus. Other discrepancies between the profiles used in this study and typical classifications for the target species include

Otolemur, Gorilla, and Pan. Napier and Napier (1967) and Kimura (2002) consider

Otolemur crassicaudatus leapers, although Terranova (1995) and Oxnard et al. (1981) qualify the classification with the caveat that they leap only infrequently and less than other galagines. The profile used in this study features data from Crompton‟s (1983)

136 study, in which both quadrupedalism and climbing frequencies exceed those of leaping.

Gorilla and Pan both were determined to be primarily quadrupeds for this study, although their locomotor behavior also has been reported to have considerable armswinging components (Martin, 1990; Kimura, 2002). Nevertheless, the field studies from which the locomotor profiles were developed based their conclusions on data collected quantitatively on wild populations and I therefore feel confident that the profiles accurately describe locomotor behaviors for those species.

137

Figure 3.2 Height above ground profiles from pooled field studies data.

138

Figure 3.3 Height above ground profiles from pooled field studies data, cont.

139

Figure 3.4 Locomotor mode profiles from pooled field studies data.

140

Figure 3.5 Locomotor mode profiles from pooled field studies data, cont.

141 Figure 3.6 presents the arithmetic mean body masses for each species in males and females, based on data compiled by Smith and Jungers (1997) in a review of the primate body mass literature. Means for males and females were combined because sex- specific behavioral data was not available for most species for most of the criteria examined in this investigation. This was an unavoidable caveat of this study. However, of those species in which sex-disaggragated data are available, interspecific differences in positional behavior outweigh intraspecific differences. It is assumed that that would hold true for other species as well. In order to normalize for the sexual dimorphism present in some species, the natural log of the average body mass of each species was obtained.

Additionally, the natural log of males was subtracted from the natural log of females and the resultant numbers used as a measure of body mass. Larger numbers represent species with a greater amount of sexual dimorphism. Both sets of mass profiles were used in statistical analyses.

There are a number of issues involved in using body mass as the basis for species comparisons, including inter-observer differences in measurement, definitions of adulthood, the habitats of animals (e.g., captive vs. natural environments), treatment of data on pregnant animals, and variations in body mass within a species (Smith and

Jungers, 1997). However, for this study it was important only to obtain a general comparison of body masses to assess the impact body size may play in conjunction with positional behavior on fracture risk.

142 1000.00 males females

large 100.00 very very

10.00 large

medium 1.00

143

0.10 small

0.01

Figure 3.6 Average body masses for male (blue diamonds) and female (red triangles) primate species, in kilograms. Data are based on numbers published in Smith and Junger’s (1997) review. They are used to develop body mass profiles. See text for details. Determination of small, medium, large, and very large (green lines on left) are based upon distinctions made by Rose (1973). 143 3.6 Statistical Analyses

Fracture frequencies were analyzed statistically based on morphological and behavioral data from the 22 taxonomic groups examined. All statistical tests were accomplished using SAS 9.2 (SAS Institute, Inc.) at the Ohio State University. The level of significance was set at 5% (α < 0.05).

Chi-square tests of significance were performed to evaluate whether fracture frequencies differ significantly between males and females within each species. Chi square analyses also indicated whether differences exist between fracture frequencies in applicable species collected for this investigation and comparative populations obtained from published accounts. Pearson‟s chi square tests were used for all the comparative population tests and some of the sex-specific tests. Both Fisher‟s exact tests and Egon‟s

(n-1) chi-square tests were used when calculating smaller sample sizes, i.e., when the expected values of any cells in contingency tables were less than five. Since Fisher‟s exact tests give no p-values, chi square values are presented. Egon‟s (n-1) chi-square tests were used as an alternative to the more widely used Fisher‟s exact tests because

Egon‟s chi-square test is recommended for use in two-by-two tables with small sample sizes when the minimum expected number is at least one (Campbell, 2007). Egon‟s chi square is determined through the following equation: χ2*(N-1)/N, where χ2 is the

Pearson‟s chi-square value and N is the total sample size (Paul Sciulli, pers. comm.).

Comparisons were made based upon the total number of fractures exhibited as well as the total number of individuals with at least one fracture. It is important to make

144 comparisons using both sets of calculations in order to obtain a more accurate assessment of fracture frequencies since individuals often exhibit multiple fractures.

A multiple correspondence analysis (MCA) was performed in order to assess relationships amongst the fracture frequencies of the long bones of all the taxonomic groups. The MCA contained 22 items (taxa) and 11 categorical variables (prevalence of fractures for each element and prevalence of four fracture types). It was coded using a

Burt matrix, the complete set of pairwise cross-tabulations of the multi-way contingency table (Greenacre, 2007). The MCA revealed patterns of association based on the clustering of long bone frequencies in a two dimensional graphical display.

To test associations between fracture frequencies and each of the locomotor and habitat use profiles independently, fracture frequency data were entered into a principal components analysis (PCA) of compositional data using the covariance method. Height above ground data (Figure 3.7) and locomotor mode data (Figure 3.8) also were subjected to PCAs. The principal components of the PCAs were used as dimension reduction devices obtained for use as input in Pearson product-moment correlations. The datasets pertaining to the frequency of arboreality and average body mass did not need to undergo a variable reducing procedure.

145 Height Above Ground PCA 0-5 m eul 6-10 m mfa mfapro prosai aotsai 11-20 m pon aot chl man sag pap Prin3 +20 m

ceb →

3.33 col pan mic

mmu leo mmugal gor oto gal 0.80

10 m 10 -1.73 – alo

pba 5.51 ← 6 ← -4.26 3.70

-1.59

1.27 hyl Prin1

Prin2 -8.69 -1.16

-3.59 -15.79

Figure 3.7 Height above ground frequencies PCA. Color codes are determined by relatively high proportion of that height category. Taxa labels: alo Alouatta, aot Aotus, ceb Cebus, chl Chlorocebus, col Colobus, eul Eulemur, gal Galago, gor Gorilla, hyl Hylobates, leo Leontopithecus, man Mandrill, mfa M. fascicularis, mic Microcebus, mmu M. mulatta, oto Otolemur, pan Pan, pap Papio, pba P. badius, pon Pongo, pro Propithecus, sag Saguinus, and sai Saimiri.

In a PCA, groups of variables which act together are combined to produce scores which explain the majority of the variance within the data set. The advantage of the PCA lies in the projection of species and parameters in multidimensional space into fewer dimensions, represented by the scores that make up the first three principal components

(Youlatos, 2004). The parameters must sum to unity in PCAs of compositional data, which are based on eigenanalysis of the covariance matrix. The fracture PCA consisted of 14 parameters (the proportions of each element fractured and each element not 146 fractured) that characterized each of the 22 taxa. In the height above ground PCA, 6 parameters (0-5 m, 6-10 m, 11-15 m, 16-20 m, 21-25 m, and +25 m) characterized the 22 taxa. In the locomotor mode PCA, 4 parameters (quadrupedalism/bipedalism, climbing, leaping/bridging, and suspensory/drop) characterized the 22 taxa.

Locomotor Mode PCA pan pon Quad Climb gor Prin3 hyl Leap pap 0.83 chlcol mmu aloalo mfa pba Susp 0.09 ceb mic sagsag col leo aotaot -0.65 manmanotooto sai 3.88

-1.39 gal 3.39 pro 1.85

0.99 eul Prin1 Prin2 -0.17 -1.40

-3.79 -2.20

Figure 3.8 Locomotor mode frequencies PCA. Color codes are determined by relatively high frequency of that locomotor mode.

When interpreting the plot generated by the height above ground PCA, two of the

5 meter categories were pooled into 10 meter categories, creating the following ranges: 0-

5 m, 6-10 m, 11-20 m, and +20 m. The first principle component of the height above

147 ground PCA (Prin1 in Figure 3.7) explains 82.58% of the total variance within the data set. Taxa primarily active at lower and mid forest levels of 0-20 meters above the ground cluster at the upper end of the axis, whereas taxa active at heights above 20 meters cluster at the lower end of the axis. Primates commonly occupying heights above 25 meters lie above the centroid. The orthogonal axis (accounting for 9.42% of the remaining variance) is largely an index of the mid-level height range. Primates most commonly occupying heights of 0-5 meters cluster at negative values on the axis and primates commonly found at 6-20 meter heights cluster at positive values. However, heights over

20 meters actually cluster in the center of the axis, between the 0-5 m and 6-20 m heights.

The proportion of the variance accounted for by the third axis is 4.66% and mainly distinguishes between the 6-10 meter categories and the rest. A scatter plot of Prin1 and

Prin2 helps to illustrate these distinctions (Figure 3.9).

148 CORR HAGp1*HAGp2

HAGp2

4 eul

→ 20 m m 20

- 3 6 mfa proaot 2 sai ceb pon sag

1 col man gor chl leo 0 pba +20 m +20 pan

149 -1 alo hyl oto -2

pap

-3 mic 5 m 5

- mmugal 0

← ← -4

-20 -10 0 10

← +20 m (+25 m) HAGp1 -20 m →

Figure 3.9 Scatter plot of the first and second axes of the height above ground PCA, depicting separation of primates commonly found at heights above and below twenty meters on the first principle axis (HAGp1). The second axis (HAGp2) distinguishes low and mid-level heights, although heights above twenty meters are plotted between them. The third axis (not shown) mainly distinguishes the 6-10 meter range from other ranges. 149 The first principle component of the locomotor mode PCA explains 49.90% of the variance within the data set (Prin1 in Figure 3.8). Suspensory primates are quite distinct from primates more commonly practicing other locomotor behaviors. Leaping and climbing also is distinguished from quadrupedalism. The second principle component accounts for 44.66% of the remaining variance. Quadrupedalism and climbing cluster on the positive side of the axis while the more risky leaping and suspensory behaviors cluster on the negative side of the axis. The first three components combined explain all

100% of the variance; however, no distinct patterns emerge in the third axis. Figure 3.10 is the scatter plot of Prin1 and Prin2.

150 CORR LOCp1*LOCp2

LOCp2 4 gor

pap

uad. → uad. 3 pan q

2 alo man chl 1 mfa

aot mmusai sag 0 oto pba climb ceb col

15 gal leo pon -1 eul 1 mic

-2 hyl

., ., leap -3

susp pro

← ← -4

-3 -2 -1 0 1 2 3 4

← leap, climb LOCp1 quad. susp. →

Figure 3.10 Scatter plot of the first and second axes of the locomotor mode PCA, depicting separation of suspensory and leaping/climbing primates on the first principle axis (LOCp1) and separation of quadrupedal and more risky locomotor behaviors on the second axis (LOCp2). 151 Pearson product-moment correlations were performed to test associations between fracture frequencies and each of the positional behavior profiles independently. The

Pearson‟s correlation coefficient measures the strength and direction of the linear relationship between two categorical variables. Plots of the components of each PCA of compositional data were correlated to determine which of the first three components best explained the variance in the data. Also, the extracted components of the fracture PCA were correlated separately with each profile (arboreality, the first three components of the height above ground PCA, the first three components of the locomotor mode PCA, and the two assessments of body mass).

Associations between fracture frequencies and each of the profiles while controlling for mass were assessed by running 3-variable PCAs using the correlation method. Any of the components of the compositional data PCAs for locomotor mode and height above ground, as well as arboreality and both mass profiles, which were found to be significantly correlated with fracture frequencies were subjected to principal components analysis. Partial correlations controlling for mass also were performed.

Relationships amongst fracture frequencies and all four locomotor and habitat use profiles were examined with 5-variable PCAs using the correlation method. The PCA consisted of the first component of the fracture PCA, arboreality, the first component of the height above ground PCA, the first component of the locomotor mode PCA, and the log of the average body mass. The second and third components of the fracture PCA also were examined with the aforementioned four other variables. Scores from a 4-variable

PCA involving arboreality, height above ground, locomotor mode, and mass were tested for correlations with fracture frequencies.

152 3.7 Chapter summary

Skeletal elements from a variety of species within the primate order were analyzed using macroscopic and radiographic techniques. Full locomotor and habitat use profiles – including frequencies of arboreality, common locomotor modes, common heights utilized, and average body masses – of each primate species examined were created, based upon previously published accounts. Statistical analyses were undertaken to test associations between positional behaviors and fracture frequencies.

153

CHAPTER 4: Results

4.1 Descriptive data

When discussing fracture frequencies, it is most common to obtain a frequency by dividing the total number of fractures within a population by the total number of individuals within that population, regardless of whether an individual has multiple fractures. For clarity, I have termed this unit the cross frequency throughout this paper.

Comparisons using this frequency work well when examining long bones alone; however, frequencies can get quite large (over 200%) when examining the entire skeleton. Consequently, it is also common to use what I have called the individual frequency, which is the proportion of individuals with one or more fractures (number of individuals with at least one fracture divided by the total number of individuals).

Comparing the cross and individual frequencies identifies populations in which individuals are especially prone to receiving multiple injuries. For instance, 8 individuals out of a total sample of 65 individuals in the Procolobus badius sample exhibit at least one fracture, which results in an individual frequency of 12.3%. However, those 8 individuals had a total of 18 long bone fractures, which results in a crossy frequency of

27.7% (18 fractures / 65 individuals). Another measurement used when comparing

154 populations, which I have termed the element frequency here, is obtained by dividing the total number of fractures by the total number of elements examined. For example, using the abovementioned Procolobus badius sample, 537 long bones were examined for evidence of fractures, resulting in an element frequency of 3.4% (18/537). It is much more common to use this frequency when comparing specific skeletal elements within a population than when comparing overall frequencies between populations. This frequency is especially useful when identifying particular skeletal elements which have comparatively few or numerous fractures. It is also helpful for obtaining accurate fracture frequencies in populations in which full skeletons are not always available. It is important to be aware which frequencies are being used when comparing populations from multiple published accounts.

4.1.1 Demographic comparisons

Of the twenty-two taxonomic groups examined, at least one individual in each group exhibited one or more fractures. Table 4.1 depicts the frequencies of fractures for each taxonomic group examined. In total, 1672 primates were examined for evidence of long bone fractures; 300 fractures were recorded in 223 of those primates. Pongo pygmaeus (29.79%) and Procolobus badius (27.69%) had the most fractures per population when comparing cross frequencies. However, 75% of the Procolobus badius population with fractures had more than one fracture. Consequently, when examining the number of individuals with at least one fracture, Procolobus badius moves down in rank to 12th highest fracture prevalence at 12.31% and Pongo pygmaeus (25.53%) and Cebus

155 apella (20.65%) have the highest individual frequencies overall. The populations with the highest element frequencies are Procolobus badius (3.35%) and Cebus apella

(2.77%), followed by Pongo pygmaeus (2.38%). It is likely that Pongo pygmaeus has a lower frequency here not only because of the number of multiple fractures Procolobus badius has, as mentioned previously, but also because the Pongo pygmaeus population had more complete skeletons. Saguinus oedipus (5.63%, cross) and Galago senegalensis

(8.82%, cross) exhibited the fewest number of fractures regardless of frequency measurement used.

Table 4.2 depicts the element frequencies for all elements examined in all species.

The fibula was the most frequently fractured element when all 22 species are pooled.

The second highest fracture frequency of any element in any species was the fibula in

Leontopithecus rosalia at 7.04%, only surpassed by fractures of the clavicle in

Procolobus badius at 7.69%. Figures 4.1 and 4.2 show the contribution of fractures per each element to the total number of fractures for each species. One hundred percent of fractures in Propithecus verreauxi occurred in the clavicle; however, Propithecus verreauxi only had one fractured element. Several species had no fractures in one or more elements. Overall, fractures of the fibula, clavicle, and ulna were most common, although distribution varied among species.

156 Table 4.1 Comparison of fracture frequencies by species individuals elements cross % N n % N n % (En/IN) Microcebus murinus 22 3 13.64 250 3 1.20 13.64 Propithecus verreauxi 10 1 10.00 121 1 0.83 10.00 Eulemur fulvus 29 3 10.34 358 3 0.84 10.34 Galago senegalensis 34 2 5.88 403 3 0.74 8.82 Otolemur crassicaudatus 34 7 20.59 432 8 1.85 23.53 Aotus lemurinus 85 12 14.12 1169 16 1.37 18.82 Alouatta seniculus 70 7 10.00 838 9 1.07 12.86 Saguinus oedipus 71 4 5.63 927 4 0.43 5.63 Leontopithecus rosalia 38 6 15.79 489 9 1.84 23.68 Cebus apella 92 19 20.65 902 25 2.77 27.17 Saimiri boliviensis 83 8 9.64 1028 14 1.36 16.87 Chlorocebus pygerythrus 56 6 10.71 616 8 1.30 14.29 Macaca fascicularis 38 5 13.16 418 5 1.20 13.16 Macaca mulatta 484 62 12.81 6673 85 1.27 17.56 Papio spp. 64 12 18.75 815 14 1.72 21.88 Mandrillus sphinx 18 2 11.11 235 2 0.85 11.11 Procolobus badius 65 8 12.31 537 18 3.35 27.69 Colobus guereza 54 4 7.41 518 5 0.97 9.26 Hylobates spp. 91 14 15.38 975 20 2.05 21.98 Pongo pygmaeus 47 12 25.53 588 14 2.38 29.79 Gorilla gorilla 105 12 11.43 1347 16 1.19 15.24 Pan troglodytes 82 15 18.29 985 18 1.83 21.95 Total: 1672 223 13.34 20624 300 1.45 17.94 individuals: N = total number of individuals examined; n = individuals with at least one fracture elements: N = total number of individuals examined; n = total number of fractures cross %: (En/IN) = total number of fractures (element n) / total number of individuals (individual N)

157 Table 4.2 Comparisons of fracture frequencies by element clavicle humerus radius ulna femur tibia fibula N n % N n % N n % N n % N n % N n % N n % Microcebus murinus 33 1 3.03 30 0 0.00 37 0 0.00 37 1 2.70 37 0 0.00 38 0 0.00 38 1 2.63 Propithecus verreauxi 17 1 5.88 15 0 0.00 18 0 0.00 19 0 0.00 15 0 0.00 18 0 0.00 19 0 0.00 Eulemur fulvus 44 1 2.27 50 0 0.00 53 0 0.00 53 1 1.89 51 1 1.96 53 0 0.00 54 0 0.00 Galago senegalensis 55 0 0.00 57 0 0.00 58 0 0.00 58 0 0.00 56 1 1.79 61 0 0.00 58 2 3.45 Otolemur crassicaudatus 61 3 4.92 65 0 0.00 67 1 1.49 67 1 1.49 52 1 1.92 60 0 0.00 60 2 3.33 Aotus lemurinus 162 4 2.47 166 1 0.60 166 2 1.20 166 4 2.41 169 1 0.59 170 1 0.59 170 3 1.76 Alouatta seniculus 71 0 0.00 128 3 2.34 122 0 0.00 123 0 0.00 133 4 3.01 132 0 0.00 129 2 1.55 Saguinus oedipus 130 0 0.00 140 0 0.00 140 1 0.71 140 1 0.71 124 1 0.81 126 0 0.00 127 1 0.79 Leontopithecus rosalia 57 0 0.00 73 0 0.00 74 0 0.00 73 1 1.37 68 1 1.47 73 2 2.74 71 5 7.04 Cebus apella 91 1 1.10 135 3 2.22 136 2 1.47 137 4 2.92 132 5 3.79 135 1 0.74 136 9 6.62 Saimiri boliviensis 125 1 0.80 148 1 0.68 153 0 0.00 152 2 1.32 145 1 0.69 155 4 2.58 150 5 3.33 158 Chlorocebus pygerythrus 89 3 3.37 108 0 0.00 76 1 1.32 76 1 1.32 112 1 0.89 78 1 1.28 77 1 1.30

Macaca fascicularis 52 0 0.00 68 1 1.47 62 0 0.00 63 2 3.17 63 1 1.59 57 1 1.75 53 0 0.00 Macaca mulatta 935 14 1.50 957 3 0.31 954 5 0.52 953 24 2.52 964 2 0.21 958 3 0.31 952 34 3.57 Papio spp. 79 1 1.27 123 1 0.81 122 4 3.28 121 6 4.96 121 0 0.00 124 1 0.81 125 1 0.80 Mandrillus sphinx 26 1 3.85 35 0 0.00 35 1 2.86 36 0 0.00 33 0 0.00 35 0 0.00 35 0 0.00 Procolobus badius 52 4 7.69 82 2 2.44 74 1 1.35 75 3 4.00 94 1 1.06 77 3 3.90 83 4 4.82 Colobus guereza 69 2 2.90 98 0 0.00 60 1 1.67 61 1 1.64 100 0 0.00 66 0 0.00 64 1 1.56 Hylobates spp. 154 1 0.65 135 3 2.22 139 2 1.44 139 4 2.88 138 5 3.62 135 2 1.48 135 3 2.22 Pongo pygmaeus 83 3 3.61 88 4 4.55 85 2 2.35 84 2 2.38 83 1 1.20 80 1 1.25 85 1 1.18 Gorilla gorilla 183 2 1.09 194 4 2.06 192 3 1.56 193 0 0.00 199 3 1.51 193 2 1.04 193 2 1.04 Pan troglodytes 132 3 2.27 145 2 1.38 138 3 2.17 139 6 4.32 145 0 0.00 143 2 1.40 143 2 1.40 Total: 2700 46 1.70 3040 28 0.92 2961 29 0.98 2965 64 2.16 3034 30 0.99 2967 24 0.81 2957 79 2.67 N = total number of elements examined; n = total number of fractures

158

Figure 4.1 Comparison of fracture frequencies by element.

159

Figure 4.2 Comparison of fracture frequencies by element, cont.

160 In most species, fracture frequencies among males and females were similar, as indicated in Tables 4.3 and 4.4, although males had slightly higher frequencies than females. Of the sexed individuals, there are no significant differences between the individual frequencies of males and females in any species. However, there are significant differences between the cross frequencies of males and females in five species. The results of Pearson‟s chi-square, Egon‟s (n-1) chi-square, and Fisher‟s exact tests are included in Table 4.5 for all elements and Table 4.6 for individuals with at least one fracture. As shown in Figure 4.3, females exhibited significantly more fractures than males in Aotus lemurinus: 5 out of 47 males (11%) and 8 out of 26 females (31%) had at

2 least one fracture (χn-1 1 = 4.5713, P = 0.0325*). All of the fractures in Leontopithecus rosalia capable of being sexed occurred in females (7 fractures in 15 females or 46.67%;

2 χn-1 1 = 7.2800, P = 0.0070**). Males exhibited significantly more fractures than females

2 in Saimiri boliviensis (12 fractures in 46 males or 26.09%; χn-1 1 = 6.1796, P = 0.0129*),

2 Procolobus badius (17 fractures in 42 males or 40.48%; χ 1 = 7.7983, P = 0.0052**), and

2 Hylobates spp. (15 fractures in 44 males or 34.09%; χ 1 = 5.9264, P = 0.0149*).

161 Table 4.3 Comparison of fracture frequencies by sex (by cross frequency) male & male? female & female? indeterminate N n % N n % N n % Microcebus murinus 10 3 30.00 11 0 0 1 0 0 Propithecus verreauxi 5 0 0 4 1 25.00 1 0 0 Eulemur fulvus 9 0 0 14 2 14.29 6 1 16.67 Galago senegalensis 12 2 16.67 15 1 6.67 7 0 0 Otolemur crassicaudatus 22 6 27.27 9 0 0 3 2 66.67 Aotus lemurinus 47 5 10.64 26 8 30.77 12 3 25.00 Alouatta seniculus 19 1 5.26 29 5 17.24 22 3 13.64 Saguinus oedipus 37 1 2.70 15 2 13.33 19 1 5.26 Leontopithecus rosalia 12 0 0 15 7 46.67 11 2 18.18 Cebus apella 49 13 26.53 35 10 28.57 8 2 25.00 Saimiri boliviensis 46 12 26.09 37 2 5.41 0 0 0 Chlorocebus pygerythrus 29 4 13.79 26 4 15.38 1 0 0 Macaca fascicularis 23 5 21.74 11 0 0 4 0 0 Macaca mulatta 266 39 14.66 218 46 21.10 0 0 0 Papio spp. 29 7 24.14 18 6 33.33 17 1 5.88 Mandrillus sphinx 8 1 12.50 7 1 14.29 3 0 0 Procolobus badius 42 17 40.48 19 1 5.26 4 0 0 Colobus guereza 26 3 11.54 26 2 7.69 2 0 0 Hylobates spp. 44 15 34.09 42 5 11.90 5 0 0 Pongo pygmaeus 16 8 50.00 22 6 27.27 9 0 0 Gorilla gorilla 56 10 17.86 43 4 9.30 6 2 33.33 Pan troglodytes 31 10 32.26 51 8 15.69 0 0 0 Total: 838 162 19.33 693 121 17.46 141 17 12.06 N = total individuals examined; n = total number of fractures

162 Table 4.4 Comparison of fracture frequencies by sex (by individual frequency) male & male? female & female? indeterminate N n % N n % N n % Microcebus murinus 10 3 30.00 11 0 0 1 0 0 Propithecus verreauxi 5 0 0 4 1 25.00 1 0 0 Eulemur fulvus 9 0 0 14 2 14.29 6 1 16.67 Galago senegalensis 12 1 8.33 15 1 6.67 7 0 0 Otolemur crassicaudatus 22 6 27.27 9 1 11.11 3 0 0 Aotus lemurinus 47 5 10.64 26 5 19.23 12 2 16.67 Alouatta seniculus 19 1 5.26 29 4 13.79 22 2 9.09 Saguinus oedipus 37 1 2.70 15 2 13.33 19 1 5.26 Leontopithecus rosalia 12 0 0 15 4 26.67 11 2 18.18 Cebus apella 49 12 24.49 35 6 17.14 8 1 12.50 Saimiri boliviensis 46 6 13.04 37 2 5.41 0 0 0 Chlorocebus pygerythrus 29 3 10.34 26 3 11.54 1 0 0 Macaca fascicularis 23 5 21.74 11 0 0 4 0 0 Macaca mulatta 266 30 11.28 218 31 14.22 0 0 0 Papio spp. 29 6 20.69 18 5 27.78 17 1 5.88 Mandrillus sphinx 8 1 12.50 7 1 14.29 3 0 0 Procolobus badius 42 7 16.67 19 1 5.26 4 0 0 Colobus guereza 26 2 7.69 26 2 7.69 2 0 0 Hylobates spp. 44 9 20.45 42 5 11.90 5 0 0 Pongo pygmaeus 16 7 43.75 22 5 22.73 9 0 0 Gorilla gorilla 56 8 14.29 43 3 6.98 6 1 16.67 Pan troglodytes 31 8 25.81 51 7 13.73 0 0 0 Total: 838 121 14.44 693 91 13.13 141 11 7.80 N = total individuals examined; n = total individuals with one or more fractures

163 Table 4.5 Chi-square statistics for male versus female fracture frequencies † Pearson's Egon's Pearson's Egon's Fisher's SL χ2 χ2 P P P Microcebus murinus 3.8500 3.6667 0.0497 0.0555 0.0902 n.s. Propithecus verreauxi 1.4063 1.2500 0.2357 … 0.4444 n.s. Eulemur fulvus 1.4082 1.3470 0.2354 … 0.5020 n.s. Galago senegalensis 0.6750 0.6500 0.4113 … 0.5692 n.s. Otolemur crassicaudatus 3.0436 2.9454 0.0811 … 0.1447 n.s. Aotus lemurinus 4.6348 4.5713 0.0313 0.0325 0.0527 * Alouatta seniculus 1.5058 1.4744 0.2198 … 0.3805 n.s. Saguinus oedipus 2.2187 2.1760 0.1363 … 0.1964 n.s. Leontopithecus rosalia 7.5600 7.2800 0.0060 0.0070 0.0081 ** Cebus apella 0.0428 0.0423 0.8362 … … n.s. Saimiri boliviensis 6.2550 6.1796 0.0124 0.0129 0.0170 * Chlorocebus pygerythrus 0.0279 0.0274 0.8673 … 1.0000 n.s. Macaca fascicularis 2.8036 2.7211 0.0941 … 0.1499 n.s. Macaca mulatta 3.4313 3.4242 0.0640 … … n.s. Papio spp. 0.4693 0.4593 0.4933 … 0.5207 n.s. Mandrillus sphinx 0.0103 0.0096 0.9192 … 1.0000 n.s. Procolobus badius 7.7983 7.6705 0.0052 … … ** Colobus guereza 0.2213 0.2170 0.6381 … 1.0000 n.s. Hylobates spp. 5.9264 5.8575 0.0149 … … * Pongo pygmaeus 2.0563 2.0022 0.1516 … … n.s. Gorilla gorilla 1.4661 1.4482 0.2260 … … n.s. Pan troglodytes 3.0905 3.0593 0.0787 … … n.s. †examining all fractures (cross frequencies). SL = significance level (n.s. = not significant; * = significant at 0.05; ** = significant at 0.01).

164 Table 4.6 Chi-square statistics for male versus female fracture frequencies † χ2 Pearson's P Fisher's exact P Microcebus murinus 3.8500 0.0497 0.0902 Propithecus verreauxi 1.4063 0.2357 0.4444 Eulemur fulvus 1.4082 0.2354 0.5020 Galago senegalensis 0.0270 0.8695 1.0000 Otolemur crassicaudatus 0.9543 0.3286 0.6395 Aotus lemurinus 1.0454 0.3066 0.3140 Alouatta seniculus 0.8950 0.3441 0.6351 Saguinus oedipus 2.2187 0.1363 0.1964 Leontopithecus rosalia 3.7565 0.0526 0.1060 Cebus apella 0.6545 0.4185 … Saimiri boliviensis 1.3736 0.2412 0.2890 Chlorocebus pygerythrus 0.0201 0.8873 1.0000 Macaca fascicularis 2.8036 0.0941 0.1499 Macaca mulatta 0.9414 0.3319 … Papio spp. 0.3113 0.5769 0.7258 Mandrillus sphinx 0.0103 0.9192 1.0000 Procolobus badius 1.4929 0.2218 0.4155 Colobus guereza 0.0000 1.0000 1.0000 Hylobates spp. 1.1525 0.2830 … Pongo pygmaeus 1.8947 0.1687 … Gorilla gorilla 1.3156 0.2514 0.3402 Pan troglodytes 1.8827 0.1700 … †examining individuals with at least one fracture (individual frequencies). None are significant at 0.05. Egon's χ2 for Microcebus murinus = 3.6667, P = 0.05551.

165 Microcebus murinus Propithecus verreauxi Eulemur fulvus Galago senegalensis Otolemur crassicaudatus Aotus lemurinus Alouatta seniculus Saguinus oedipus Leontopithecus rosalia Cebus apella Saimiri boliviensis Chlorocebus pygerythrus male Macaca fascicularis female Macaca mulatta Papio spp. Mandrillus sphinx Procolobus badius Colobus guereza Hylobates spp. Pongo pygmaeus Gorilla gorilla Pan troglodytes

100-1 -800.8 -600.6 -400.4 -200.2 0%0 0.220 0.440 600.6 800.8 1001

Figure 4.3 Fracture distribution by sex. Proportion of all fractures occurring in males (red on left) and females (blue on right).

Potentially, sex-determined variation exists in the locomotor and habitat preferences of the examined primate species. However, because most of the species did not differ significantly in cross fracture prevalence and none of the species differed in individual fracture prevalence, it was deemed appropriate to pool data from previously published sources concerning male and female positional behaviors where available.

However, statistically significant sex-determined differences do exist between males and females in the five previously mentioned species. It was not possible to adjust the

166 positional behavior profiles in each of these species by separating them into distinct male and female behaviors because such data were lacking from field studies in many cases. It was determined that they should not be excluded from the positional behavior analyses altogether for two reasons. One, it is possible that sex-determined differences in fracture frequencies exist in these species based not on differences in their positional behavior, but rather some other factor, such as agression. This will be discussed in more detail below. Second, it is likely that more differences in positional behavior exist between species than within species. This is substantiated in those cases in which sex- differentiated data are available from positional behavior field studies (see the introductory chapter for a review of these studies). Sex-specific data pertaining to arboreality are available for mandrills (Chang et al., 1999), gorillas (Doran, 1996), and chimpanzees (Doran, 1993b). Sex-specific data regarding height preferences have been reported for long-tailed macaques (Vos et al., 1992), mandrills (Jouventin, 1975), guerezas (Gebo and Chapman, 1995), albibarbis gibbons (Cheyne, 2010), gorillas

(Remis, 1995), and chimpanzees (Doran, 1993b). Locomotor mode usage has been sex- disagregated for orangutans (Thorpe and Crompton, 2006), gorillas (Remis, 1998), and chimpanzees (Doran, 1993b). Although some variation occurs between the males and females of these species, their behaviors are not extensively different overall when compared across taxa. In most cases, it appears as if variation results primarily from body size differences (Doran, 1993b; Fleagle and Mittermeier, 1980). Locomotion in males in particular may be constrained by body size, which is addressed in this analysis through the standardization of body mass data, discussed below.

167 For most species, the majority of fractures occured in adults (Figure 4.4). The fractures observed for Alouatta seniculus consisted of 2 fractures in adults and 7 fractures in subadults (78%), although 3 of the subadult fractures involved 1 individual. In 9 out of the 22 species (41%), all fractures occurred in adults. As will be discussed in greater detail below, this does not necessarily mean that these injuries occurred during adulthood, since fractures accumulate over the lifetime of the individual.

Microcebus murinus Propithecus verreauxi Eulemur fulvus Galago senegalensis Otolemur crassicaudatus Aotus lemurinus Alouatta seniculus Saguinus oedipus Leontopithecus rosalia Cebus apella Saimiri boliviensis Chlorocebus pygerythrus subadult Macaca fascicularis adult Macaca mulatta Papio spp. Mandrillus sphinx Procolobus badius Colobus guereza Hylobates spp. Pongo pygmaeus Gorilla gorilla Pan troglodytes

100-1 80-0.8 -600.6 -400.4 -200.2 0%0 0.220 0.4 40 0.6 60 0.8 80 1001

Figure 4.4 Fracture distribution by age: subadults (red on left) and adults (blue on right).

168 In most species, fractures are distributed fairly evenly between the left and right sides of the body, as seen in Figure 4.5. The species in which all fractures are located on one side of the body have total few fractures. Microcebus murinus has only three fractures on the left side of the body, Propithecus verreauxi has one on the left side,

Galago senegalensis has three on the right side, and Mandrillus sphinx has two on the right side.

Microcebus murinus Propithecus verreauxi Eulemur fulvus Galago senegalensis Otolemur crassicaudatus Aotus lemurinus Alouatta seniculus Saguinus oedipus Leontopithecus rosalia Cebus apella Saimiri boliviensis Chlorocebus pygerythrus left Macaca fascicularis right Macaca mulatta Papio spp. Mandrillus sphinx Procolobus badius Colobus guereza Hylobates spp. Pongo pygmaeus Gorilla gorilla Pan troglodytes

-1001 - 0.8 80 - 0.6 60 - 0.440 - 0.220 0%0 0.220 0.440 600.6 800.8 1001

Figure 4.5 Fracture distribution by side: left (red on left) and right (blue on right).

169 The distribution of fractures between fore and hind limbs (excluding the clavicle) are less evenly distributed (Figure 4.6). The only fracture in Propithecus verreauxi is located on the clavicle; therefore, Propithecus verreauxi is not represented in this comparison. Mandrillus sphinx has only one limb fracture, on the radius, whereas the

Galago senegalensis has only three fractures, all involving the hind limb. The hind limb predominates in Leontopithecus rosalia (8 fractures, 88.89%) and Saimiri boliviensis (10 fractures, 76.92%), whereas the fore limb is most affected in Papio spp. (11 fractures,

84.62%), Pongo pygmaeus (8 fractures, 72.72%), and Pan troglodytes (11 fractures,

73.33%).

Microcebus murinus Propithecus verreauxi Eulemur fulvus Galago senegalensis Otolemur crassicaudatus Aotus lemurinus Alouatta seniculus Saguinus oedipus Leontopithecus rosalia Cebus apella Saimiri boliviensis Chlorocebus pygerythrus fore limb Macaca fascicularis hind limb Macaca mulatta Papio spp. Mandrillus sphinx Procolobus badius Colobus guereza Hylobates spp. Pongo pygmaeus Gorilla gorilla Pan troglodytes

-1 -0.8 -0.6 -0.4 -0.2 0 0.2 0.4 0.6 0.8 1

Figure 4.6 Fracture distribution by limb: fore limb (red on left) and hind limb (blue on right). 170

The majority of fractures across the entire series of long bones examined occurred to the diaphysis of the bone (93.67%). Instances of fractures involving other regions were recorded, including the anatomical neck, head, intercondylar and condylar areas, and metaphysis of the bone. The position of fractures within bone levels are recorded in

Figure 4.7. Overall, fractures are more likely to be located on the middle third of the bone rather than on either the proximal or distal bone ends.

171 Microcebus murinus 1 2 Propithecus verreauxi 1 Eulemur fulvus 2 1 Galago senegalensis 2 1 Otolemur crassicaudatus 2 5 1 Aotus lemurinus 3 7 6 Alouatta seniculus 2 5 2 Saguinus oedipus 3 1 Leontopithecus rosalia 5 3 1 Cebus apella 8 7 10 Saimiri boliviensis 6 4 4 proximal Chlorocebus pygerythrus 2 3 3 middle Macaca fascicularis 2 1 2 distal Macaca mulatta 16 29 40 Papio spp. 6 7 1 Mandrillus sphinx 1 1 Procolobus badius 7 7 4 Colobus guereza 1 4 Hylobates spp. 2 14 4 Pongo pygmaeus 3 6 5 Gorilla gorilla 2 9 5 Pan troglodytes 3 11 4

0% 20% 40% 60% 80% 100%

Figure 4.7 Fracture distribution by bone level: proximal (red on left), middle (green in middle), and distal (blue on right).

Figures 4.8 and 4.9 depict the proportion that each type of fracture contributes to the total fracture count for each species based on evaluation of radiographs. Again, as

Propithecus verreauxi only had one fracture, the fact that 100% of fracture types for that species are listed as comminuted is somewhat misleading. The most frequently encountered type of fracture was transverse (114/300 fractures, 38%), followed by oblique (81/300 fractures, 27%). Direct forces are involved in the formation of 172 transverse fractures, whereas indirect or torsional forces cause oblique and spiral fractures (Mann and Murphy, 1990). When spiral and oblique fractures are combined, they represent 34% of all fractures. Both Otolemur crassicaudatus and Cebus apella exhibit high frequencies of fractures caused by indirect or torsional forces, as represented by the combined frequency of spiral and oblique fractures (5/8 fractures, 62.5% and

16/25, 64%, respectively). Macaca mulatta, Papio spp., and Procolobus badius all exhibit high frequencies of fractures caused by direct forces striking at right angles to the bone, as represented by transverse fractures (48/85 fractures, 56.47%; 8/14, 57.14%; and

10/18, 55.56%, respectively).

173

Figure 4.8 Comparison of fracture frequencies by fracture type.

174

Figure 4.9 Comparison of fracture frequencies by fracture type, cont.

175 A multiple correspondence analysis was performed in order to identify associations among taxa, fracture location, and fracture type. The MCA used a three-way table involving the 22 taxonomic groups, fractures in 7 skeletal elements, and 4 types of fractures. The results of the MCA demonstrate clustering amongst the variables (overall

2 χ 1024 = 9605.94). However, there is little percent variation among the individual axes

(ranging from 1.76-5.69% of the inertia); therefore, no variables can be interpreted as standing apart from the others. Figure 4.10 is a graphical plot illustrating the clustering of the dataset. Taxa are outlined in black, skeletal elements are italicized in blue, and fracture types are underlined in red. The category miscellaneous refers to fracture types other than transverse, oblique, or spiral.

Clusters of associated variables have been bounded by ellipses in the plot. I determined the extent of the ellipses based upon each column point‟s contribution to inertia and squared cosine (Table 4.7). Contributions to inertia identify which variables contribute the most to the variance of the dataset. Squared cosines for the column points identify whether the position of each variable is determined more by the horizontal or vertical dimension.

176 Dim2 3 oto hyl

man radius pon pan 1 leo clavicle mfa misc. gor pba mmu ulna pro humerus transverse 0 tibia pap sag gal sai alo aot col spiral oblique fibula -1 chl femur

177 eul ceb

-2 mic

-3

-2 -1 0 1 2

Dim1

Figure 4.10 Plot of multiple correspondence analysis (overall χ2 = 9605.94). Skeletal elements italicized in blue. Fracture types underlined _NAME_ FXB 1024 FXC FXF FXH FXR in red. Taxa labels (in black): aloFXT Alouatta, aot AotusFXU, ceb Cebus, chl ChlorocebusTMI , col ColobusTOB , eul EulemurTSP, gal Galago, gor GorillaTTR , hyl Hylobates, leo Leontopithecus, manalo Mandrill, mfa M.aot fascicularis, micceb Microcebus, mmuchl M. mulatta, oto Otolemurcol , pan Pan, papeul Papio, pba P. badius, pon Pongo, pro Propithecusgal , sag Saguinusgor, and sai Saimiri. hyl leo man mfa mic mmu oto pan pap pba pon pro sag sai 177 Table 4.7 Statistics for the multiple correspondence analysis Taxa*Element*Type. Inertia Cosines Dim 1 Dim 2 Dim 1 Dim 2 Microcebus murinus 0.0022 0.0349 0.0038 0.0519 Propithecus verreauxi 0.0008 0.0007 0.0014 0.0010 Eulemur fulvus 0.0040 0.0293 0.0071 0.0445 Galago senegalensis 0.0124 0.0003 0.0215 0.0004 Otolemur crassicaudatus 0.0005 0.0199 0.0009 0.0294 Aotus lemurinus 0.0006 0.0022 0.0011 0.0033 Alouatta seniculus 0.0036 0.0054 0.0065 0.0084 Saguinus oedipus 0.0026 0.0005 0.0046 0.0008 Leontopithecus rosalia 0.0012 0.0257 0.0022 0.0400 Cebus apella 0.0156 0.0808 0.0291 0.1299 Saimiri boliviensis 0.0386 0.0019 0.0680 0.0028

Taxa Chlorocebus pygerythrus 0.0019 0.0207 0.0034 0.0320 Macaca fascicularis 0.0000 0.0078 0.0000 0.0118 Macaca mulatta 0.0102 0.0043 0.0178 0.0064 Papio spp. 0.1308 0.0020 0.3118 0.0041 Mandrillus sphinx 0.0071 0.0474 0.0128 0.0733 Procolobus badius 0.0084 0.0029 0.0146 0.0043 Colobus guereza 0.0164 0.0100 0.0300 0.0157 Hylobates spp. 0.0001 0.0363 0.0001 0.0538 Pongo pygmaeus 0.0407 0.0361 0.0729 0.0558 Gorilla gorilla 0.0586 0.0055 0.1057 0.0086 Pan troglodytes 0.0017 0.0401 0.0031 0.0628 clavicle 0.0141 0.0490 0.0284 0.0853 humerus 0.1042 0.0102 0.1963 0.0166 radius 0.0065 0.0904 0.0123 0.1475 ulna 0.0560 0.0239 0.1216 0.0448

Element femur 0.0906 0.0663 0.1719 0.1086 tibia 0.0223 0.0041 0.0414 0.0066 fibula 0.0422 0.1272 0.0978 0.2543 transverse 0.1769 0.0028 0.4874 0.0066 spiral 0.0245 0.0110 0.0451 0.0175

Type oblique 0.0121 0.1039 0.0283 0.2097 miscellaneous 0.0923 0.0964 0.2180 0.1964 Inertia = indices of the coordinates contributing most to the inertia for the column points Cosines = squared cosines for the column points

178 The horizontal dimension (Dim1) separates taxa mainly on the basis of fracture type although elements are also affected. For instance, transverse fractures contribute the most to the inertia of Dim1, with a value of 0.1769. Transverse fractures are distinguished from spiral and miscellaneous fractures based on their position in the plot.

However, oblique fractures are impacted more by the vertical dimension, with a larger squared cosine value for the vertical dimension (0.2097) than the horizontal dimension

(0.0283). Additionally, Dim1 seems to be determined by fractures occurring to the ulna versus those of the humerus, femur, and tibia. The vertical dimension (Dim2) distinguishes between fracture frequencies mainly on the basis of element, with fractures more often occurring to the clavicle or radius above the centroid and the fibula below it.

Based on the results of the multiple correspondence analysis, certain associations among primate taxa, fracture location, and fracture type have been revealed. When fractures occur among Galago senegalensis, Procolobus badius, and Papio spp., they are more likely to involve the ulna and transverse fractures, which are caused by tensile and bending forces. Fractures among Propithecus badius, Saguinus oedipus, Colobus guereza, Macaca mulatta, Pongo pygmaeus, Gorilla gorilla, and Saimiri boliviensis are more likely to be caused by various mixtures of forces (spiral fractures and other miscellaneous fracture types) and be located on the humerus, tibia, and femur. Oblique fractures, caused by compressive or shear forces, and fibulae fractures are associated with

Microcebus murinus, Alouatta seniculus, Aotus lemurinus, Chlorocebus pygerythrus,

Eulemur fulvus, and Cebus apella. If Mandrillus sphinx, Leontopithecus rosalia,

Hylobates spp., Macaca fascicularis, Pan troglodytes, and Otolemur crassicaudatus break a bone, it is more likely to be the clavicle or radius.

179 4.1.2 Assessment of fracture healing

Overall, the majority of fractures were well-healed or healing (81.33%), with only two nonunion fractures in Saimiri boliviensis and one nonunion each in Aotus lemurinus,

Saguinus oedipus, Leontopithecus rosalia, Macaca fascicularis, and Mandrillus sphinx.

However, 16.47% (14/85 fractures) of all Macaca mulatta fractures did not unite.

Endosteal and/or periosteal callus formation was present on radiographs of over half the fractures in all species (Figure 4.11) except for Propithecus verreauxi (0/1, 0%), Eulemur fulvus (1/3, 33%), and Otolemur crassicaudatus (3/8, 37.5%), all of which exhibited fewer than 10 fractures each. The radiographic presence of sclerosis on fractured bone ends was less extensive (Figure 4.12). In Galago senegalensis, Otolemur crassicaudatus,

Alouatta seniculus, Saguinus oedipus, and Pan troglodytes, less than half of examined fractures presented with sclerosis.

180 100 94.4 88.9 87.5 84.0 85.7 83.3 90 80.0 75.0 75.0 75.3 80 71.4 71.4 68.8 70 60.0 60 55.6 50 37.5 40 33.3 30 20 10 present (%)

Papio spp.Papio

Cebus apellaCebus

Gorilla gorillaGorilla

Hylobatesspp.

Eulemurfulvus

Pan troglodytesPan

Aotus lemurinusAotus mulattaMacaca

Colobusguereza

Pongo pygmaeusPongo

Saguinus oedipusSaguinus

Mandrillus sphinxMandrillus

Alouattaseniculus

Saimiri boliviensisSaimiri

Procolobusbadius

Macaca fascicularisMacaca

Microcebusmurinus

Galagosenegalensis

Propithecusverreauxi

Leontopithecusrosalia

Otolemur crassicaudatusOtolemur Chlorocebuspygerythrus

Figure 4.11 Frequency of callus formation (as noted on radiographs).

100 94.4 90 80.0 80.0 81.3 75.0 80 71.4 66.7 66.7 64.3 64.3 70 60.0 62.5 60.0 55.6 54.1 60 50.0 50 44.4 44.4 37.5 40 33.3 30 25.0 20 10 present (%)

Papio spp.Papio

Cebusapella

Gorilla gorillaGorilla

Hylobatesspp.

Eulemurfulvus

Pan troglodytesPan

Macaca mulattaMacaca

Aotus lemurinusAotus

Colobusguereza

Pongo pygmaeusPongo

Saguinus oedipusSaguinus

Mandrillus sphinxMandrillus

Alouatta seniculusAlouatta

Saimiri boliviensisSaimiri

Procolobusbadius

Macaca fascicularisMacaca

Microcebusmurinus

Galago senegalensisGalago

Propithecusverreauxi

Leontopithecusrosalia

Otolemur crassicaudatusOtolemur Chlorocebuspygerythrus

Figure 4.12 Frequency of sclerosis of bone ends (radiographic). 181 Figure 4.13 depicts the extent of apposition of bone fragments. Sample sizes in some of the species are small due to the removal of fractures (such as nonunion fractures) in which apposition could not be determined. However, of the species with more than three fractures in the sample, only Procolobus badius has fewer than 40% of fractures which healed with complete apposition. If a fracture heals with the ends of the bone fragments completely apposed, it can be inferred that the affected individual did not experience significant loss of mobility. The Procolobus badius sample also exhibited a large number of multiple fractures, the severity of which may have affected healing adversely. Table 4.8 shows the presence and direction of angulation of the distal bone fragment, obtained from radiographs. Overall, 32.43% of the fractures examined

(excluding inapplicable fractures, such as fractures which failed to unite), exhibited no angulation deformities, indicating healing with no significant loss of mobility. Of the fractures which exhibit some degree of angulation, the severity of the deformity varied by individual although, in general, fractures healed with minimal deformity. When examining limb fractures only, the most common direction of angulation was posterior

(36.17%), followed by lateral (23.94%), medial (22.34%), and anterior (17.55%). The extent of bone overlap, corrected for size differences among primate taxa, was most extensive in Propithecus verreauxi and Mandrillus sphinx and least extensive in Saguinus oedipus and Saimiri boliviensis (Figure 4.14). Figure 4.15 provides an example of a fracture exhibiting bone overlap, partial apposition, and medial angulation.

182 Microcebus murinus 1 2 Propithecus verreauxi 1 Eulemur fulvus 2 Galago senegalensis 1 2 Otolemur crassicaudatus 5 2 Aotus lemurinus 7 8 Alouatta seniculus 5 4 Saguinus oedipus 2 1 Leontopithecus rosalia 6 2 Cebus apella 16 9 Saimiri boliviensis 8 4 compete Chlorocebus pygerythrus 4 4 partial/absent Macaca fascicularis 2 Macaca mulatta 28 41 Papio spp. 6 6 Mandrillus sphinx 1 Procolobus badius 1 17 Colobus guereza 4 1 Hylobates spp. 9 11 Pongo pygmaeus 8 4 Gorilla gorilla 4 6 Pan troglodytes 7 6

0% 20% 40% 60% 80% 100%

Figure 4.13 Extent of apposition of bone ends: complete (red on left) and partial/absent (blue on right).

183 Table 4.8 Direction of angulation of distal fractured bone ends † N A P M L CA CP CS CI X Microcebus murinus 2 0 0 0 1 0 0 0 0 0 Propithecus verreauxi 0 0 0 0 0 1 0 0 0 0 Eulemur fulvus 0 0 0 1 0 1 0 0 0 0 Galago senegalensis 1 0 (1) 1 0 0 (1) 0 0 0 0 1 Otolemur crassicaudatus 1 1 1 (1) 0 0 (1) 0 2 (1) 0 (1) 0 2 Aotus lemurinus 5 1 0 (3) 2 1 (3) 0 1 (1) 0 1 (1) 4 Alouatta seniculus 1 0 (1) 3 (1) 3 (2) 0 0 0 0 0 2 Saguinus oedipus 1 1 1 1 0 0 0 0 0 0 Leontopithecus rosalia 0 1 (1) 0 (3) 2 (3) 1 (1) 0 0 0 0 4 Cebus apella 10 5 (1) 4 (2) 1 (2) 2 (1) 0 0 0 0 3 Saimiri boliviensis 3 1 4 (1) 3 0 (1) 0 0 0 0 1 Chlorocebus pygerythrus 1 0 1 (1) 1 (1) 1 (1) 0 0 2 0 (1) 2 Macaca fascicularis 1 0 0 0 1 0 0 0 0 0 Macaca mulatta 25 5 (4) 14 (7) 4 (5) 4 (6) 0 (2) 0 1 2 (2) 14 Papio spp. 6 0 (1) 0 (1) 2 2 (2) 0 0 0 0 2 Mandrillus sphinx 0 0 0 0 0 0 0 0 1 0 Procolobus badius 4 3 (2) 1 (4) 1 (2) 1 (4) 1 1 0 0 6 Colobus guereza 2 0 0 0 2 0 0 (1) 0 (1) 0 1 Hylobates spp. 7 1 (2) 2 (4) 3 1 (5) 0 0 1 0 5 Pongo pygmaeus 3 1 4 0 2 2 0 0 0 0 Gorilla gorilla 5 1 2 (1) 0 (1) 1 0 0 0 0 1 Pan troglodytes 6 0 0 3 3 1 0 0 0 0 Total: 84 34 67 43 49 8 7 6 8 48 † N = no angulation; A = anterior; P = posterior; M = medial; L = lateral; CA = clavicle anterior; CP = clavicle posterior; CS = clavicle superior; CI = clavicle inferior; X = multiple (numbers in parentheses in each column refer to the directions of fractures that are angulated in multiple directions)

184 16 14.5 mean percent difference 14 12.0 12 9.6 10 8.8 7.6 8 7.4 6.1 5.0 5.1 6 4.9 4.5 4.8 4.4 3.9 4.3 4 3.2 3.4 2.2 1.3 1.0 1.3 2 0.4

Papio spp.Papio

Cebus apellaCebus

Gorilla gorillaGorilla

Hylobatesspp.

Eulemurfulvus

Pan troglodytesPan

Aotus lemurinusAotus mulattaMacaca

Colobusguereza

Pongo pygmaeusPongo

Saguinus oedipusSaguinus

Mandrillus sphinx Mandrillus

Alouatta seniculusAlouatta

Saimiri boliviensisSaimiri

Procolobusbadius

Macaca fascicularisMacaca

Microcebusmurinus

Galago senegalensisGalago

Propithecusverreauxi

Leontopithecusrosalia

Otolemur crassicaudatus Otolemur Chlorocebuspygerythrus

Figure 4.14 Proportion of bone shortening (corrected for size differences).

Figure 4.15 Anterior view of a Pan troglodytes right humerus with a spiral fracture (HTB 1775, Cleveland Museum of Natural History) showing A. bone overlap, B. partial apposition, and C. medial angulation. Radiograph taken with Faxitron x-ray system at 60 kVp for 30 s.

185 Complications which could inhibit healing of fractures are not prevalent in most species. Gorilla gorilla and Macaca fascicularis are represented by high frequencies of localized periosteal reactions adjacent to fractures compared to other primates, as seen in

Figure 4.16. The majority of healed or healing fractures (96.33%) are not associated with other traumas, such as gunshot wounds. Although many of the individuals examined are from wildshot collections, antemortem fractures caused by or in association with gunshot wounds were uncommon. Only one instance each in Leontopithecus rosalia, Papio spp.,

Procolobus badius, and Gorilla gorilla was recorded. It was far more common to see perimortem fractures caused by gunshot wounds, which were not included in this study.

Potential bite wounds, cutting, or piercing wounds associated with fractures were recorded in three Macaca mulatta and one each of Mandrillus sphinx, Papio spp., Pan troglodytes, and Gorilla gorilla.

186 70 present (%) 60.0 60

50.0 50 43.8

30 27.8 21.4 20.0 20.0 20 16.0 14.3 15.0 11.1 11.1 7.1 10 5.6

Papio spp.Papio

Cebus apellaCebus

Gorilla gorillaGorilla

Hylobatesspp.

Eulemurfulvus

Pan troglodytesPan

Aotus lemurinusAotus mulattaMacaca

Colobusguereza

Pongo pygmaeusPongo

Saguinus oedipusSaguinus

Mandrillus sphinx Mandrillus

Alouatta seniculusAlouatta

Saimiri boliviensisSaimiri

Procolobusbadius

Macaca fascicularisMacaca

Microcebusmurinus

Galagosenegalensis

Propithecusverreauxi

Leontopithecusrosalia

Otolemur crassicaudatus Otolemur Chlorocebuspygerythrus

Figure 4.16 Frequency of fractures with localized periosteal reaction present.

4.1.3 Comparative populations

Fracture frequencies in the current study were compared to fracture frequencies recorded for other primate taxa obtained from the literature. Cross frequencies for long bones were available for the following populations: Cayo Santiago macaques who died prior to or in 1972 (Buikstra, 1975), Darajani baboons (Bramblett, 1967), Chiengmai gibbons (Schultz, 1944), Virunga gorillas (Lovell, 1990b), Kibale and Gombe chimpanzees (Jurmain, 1989; Carter et al., 2008), and orangutans, gorillas and

187 chimpanzees from various museum collections (Duckworth, 1911; Randall, 1944; Lovell,

1990a). There is no overlap in individuals between the samples studied for the present investigation and the samples to which they were compared. For instance, The Cayo

Santiago macaques examined in the present study all died after 1972 (in many cases, they were not even born prior to 1972), prohibiting them from being a part of the series studied by Buikstra (1975). Chronologically, the earliest death recorded for the sample I examined was a macaque which died in September 1988 (born in December 1954). The latest death recorded in my sample was a macaque which died in October 2005.

Pearson‟s chi square tests were performed to determine whether differences in fracture patterns exist between the current sample and previously published samples.

Table 4.9 presents the results of the statistical tests. There were no statistically significant differences in fracture frequencies between the species described here and previously published accounts of the same species (or genus). The injuries sustained in the current samples are comparable to those in published samples. This suggests that the fracture frequencies reported in this study in general provide a good representation of fracture frequencies for each taxon as a whole.

188 Table 4.9 Chi-square statistics for fracture frequencies in comparative collections † χ2 P Macaca mulatta x pre-1972 Cayo Cantiago macaques 0.4656 0.4950 Papio spp. x Darajani 1.0746 0.2999 Hylobates spp. x Chiengmai 0.5303 0.4665 Pongo pygmaeus x (Cambridge)a 2.1990 0.1381 Gorilla gorilla x (USNM) x (Western Reserve) x Virunga 2.2150 0.5290 Pan troglodytes x (USNM) x Kibale x Gombe 1.1538 0.7641 †examining all fractures per total individuals (cross frequency) a = adults only None are statistically significant at α = 0.05 Sources: Buikstra (1975); Bramblett (1967); Schultz (1944); Duckworth (1911); Lovell (1990a, 1990b); Randall (1944); Jurmain (1989); Carter et al. (2008)

4.2 Associations of fracture frequencies with positional behavior

Most of the sampled primates do not exhibit long bone fractures; however, the location of fractures appears to be associated with positional behaviors and habitat use preferences. Principal components analyses (PCA) using compositional data were performed in order to reduce the cloud of data points into component scores used to determine these associations. Values were determined based upon the frequency of each element that was fractured as well as the frequencies of each element which was not fractured (i.e., the frequency of fractured clavicles, the frequency of non-fractured clavicles, the frequency of fractured humeri, the frequency of non-fractured humeri, and so on). The first three axes of a PCA accounting for most of the variance in elements fractured among primates (Figure 4.17) was plotted. Unless otherwise noted, cross 189 fracture frequencies (the proportion of all fractures per all individuals within a taxon) are used when discussing fracture frequencies throughout the rest of this chapter.

Fracture (Element) PCA Clav alo Ulna Hum/Fem gor

gal ceb Tib/Fib Prin3 hyl sag Mix 1.07

→ leo mfa eul 0.25 sai

pon man -0.58 pro chl mmu oto col pap aot 1.75

← Ulna ← -1.41 mic 1.49 pan pba

0.63

0.62 Prin1

Prin2 -0.49 -0.24

-1.11 -1.61

Figure 4.17 Fracture (element) frequencies PCA. Color codes are determined by relatively high presence of that element (or those elements). Mix indicates that several long bones exhibited the same or similar proportion of fractures for that species. Taxa labels: alo Alouatta, aot Aotus, ceb Cebus, chl Chlorocebus, col Colobus, eul Eulemur, gal Galago, gor Gorilla, hyl Hylobates, leo Leontopithecus, man Mandrill, mfa M. fascicularis, mic Microcebus, mmu M. mulatta, oto Otolemur, pan Pan, pap Papio, pba P. badius, pon Pongo, pro Propithecus, sag Saguinus, and sai Saimiri.

Based on the fracture (element) PCA, high fracture frequencies of the humerus and femur were linked as were high fracture frequencies of the tibia and fibula. Several

190 species, including Microcebus murinus, Eulemur fulvus, Aotus lemurinus, Saguinus oedipus, Mandrillus sphinx, and Procolobus badius, did not show a preference for fractures in any particular long bone. They were labeled mixed when interpreting the

PCAs.

The first principle component (Prin1 in Figure 4.17) of the fracture PCA accounts for 30.19% of the total variance in the dataset. It distinguishes between clavicle (and to a lesser extent, radius) fractures (which have values of less than -0.49 on the Prin1 axis) and fractures of the other elements (values greater than -0.49). Mixed fractures cluster with clavicular fractures. In general, this axis corresponds with increases in fracture frequencies among taxonomic groups, with higher frequencies represented by positive values. However, fractures of the clavicle represent over 30% of the total fracture distribution of several taxa: Microcebus murinus, Propithecus verreauxi, Eulemur fulvus,

Otolemur crassicaudatus, Chlorocebus pygerythrus, Mandrillus sphinx, and Colobus guereza. Consequently, the PCA separated clavicles from the other elements, meaning that species with low fracture frequencies do not necessarily cluster towards the negative end of the axis. These results are comparable to the vertical dimension (Dim2) of the multiple correspondence analysis, discussed above, which also distinguishes between the clavicle (and the radius to a lesser extent) and other elements.

The orthogonal dimension (Prin2 in Figure 4.17) explains 21.77% of the variance following the first component, distinguishing between proportions of fractures involving the humerus and femur (lower values) and those involving the tibia and fibula (higher values). In both Prin1 and Prin2, ulnar fractures tend to cluster around the centroid.

191 A scatter plot of Prin1 and Prin2 further illustrates these distinctions (Figure

4.18). In Prin3 of the PCA, the third axis has an eigenvalue proportion of 16.63%. The ulna is distinct from the other elements on this axis.

192 CORR FXp1*FXp2

FXp2 2

gor

/femur /femur → alo

1 mfa humerus sag pap hyl

man eulpon ulna pro ceb 0 pan col chl gal

193 aot

oto mmu sai mic -1 pba leo

← tibia/fibula ← -2

-2 -1 0 1 2

← clavicle, mix ulna FXp1 other elements →

Figure 4.18 Scatter plot of the first and second principle axes of the fracture PCA, depicting separation of fractures of the clavicle from fractures of all other elements on the first principle axis (FXp1) and separation of tibia and fibula fractures from humerus and femur fractures on the second principle axis (FXp2). The third axis (not shown) mainly distinguishes ulnar fractures from other long bone fractures. 193 The scores from the first three axes of the fracture PCA of compositional data were used as synthetic variables in correlations testing hypotheses about locomotor and habitat use. Each set of positional behavior variables was correlated with the scores pertaining to fracture frequencies. Scores computed from PCAs of compositional data on both height above ground utilization (Figure 3.7 in Materials and Methods) and locomotor mode preferences (Figure 3.8 in Materials and Methods) also were used in these analyses. Arboreality values remained unchanged (Figure 3.1 in Materials and

Methods). Two sets of log-transformed values for average body mass (Figure 3.6 in

Materials and Methods) were used to account for extreme size differences and sexual dimorphism.

Table 4.10 lists the Pearson‟s product-moment correlation coefficients for each test of whether fracture frequencies are correlated with each positional profile, independent of other profiles. The scatter plot of every statistically significant (α < 0.05) correlation is provided (Figures 4.19-4.30). Although several locomotor and habitat use profiles were statistically significant, none alone explained more than 42% of the variability in fracture frequencies among the representative taxa.

194 Table 4.10 Correlation statistics for fracture patterns versus positional behavior r P SL FXp1*ARB 0.27405 0.0718 n.s. FXp2*ARB -0.38539 0.0098 ** FXp3*ARB 0.24578 0.1078 n.s. FXp1*HAGp1 -0.36426 0.0151 * FXp1*HAGp2 -0.18015 0.2419 n.s. FXp1*HAGp3 -0.28323 0.0625 n.s. FXp2*HAGp1 -0.36837 0.0139 * FXp2*HAGp2 0.21659 0.1579 n.s. FXp2*HAGp3 0.42982 0.0036 ** FXp3*HAGp1 0.17605 0.2530 n.s. FXp3*HAGp2 0.01599 0.9179 n.s. FXp3*HAGp3 -0.33412 0.0267 * FXp1*LOCp1 0.34736 0.0209 * FXp1*LOCp2 -0.01497 0.9232 n.s. FXp1*LOCp3 -0.23184 0.1300 n.s. FXp2*LOCp1 0.03815 0.8058 n.s. FXp2*LOCp2 0.37399 0.0124 * FXp2*LOCp3 0.09992 0.5187 n.s. FXp3*LOCp1 -0.64302 <0.0001 *** FXp3*LOCp2 -0.33140 0.0280 * FXp3*LOCp3 0.01527 0.9217 n.s. FXp1*Mln -0.20779 0.1759 n.s. FXp2*Mln 0.48436 0.0009 *** FXp3*Mln -0.43305 0.0033 *** FXp1*Msd -0.18399 0.2319 n.s. FXp2*Msd 0.54530 0.0001 *** FXp3*Msd -0.17916 0.2446 n.s. SL = significance level (n.s. = not significant; * = significant at 0.05; ** = significant at 0.01; *** = significant at 0.001) FX = fracture PCA; ARB = arboreality frequencies; HAG = height above ground PCA; LOC = locomotor mode PCA; Mln = natural log of average body mass; Msd = sexual dimorphism body mass st nd rd p1, p2, or p3 = scores of PCA 1 , 2 , or 3 principal components

195 4.2.1 Fractures and arboreality

Arboreality does not appear to have as much of an impact on fracture frequencies as other examined factors when assessing the impact of arboreality alone on nonhuman primate fractures. There is no correlation between overall fracture frequencies and

2 arboreality in primates (r42 = 0.01348, P = 0.9308, r = 0.02%). Furthermore, there does not appear to be any association between arboreality and fracturing any particular element in primates except for a slight tendency to fracture the humerus or femur in terrestrial primates and a tendency to fracture the tibia or fibula in completely arboreal primates (r42 = -0.38539, P = 0.0098**). However, even this small association explains only 14.85% of the variation seen in the correlation (Figure 4.19).

196 CORR FXp2*ARB

ARB pba otosai aot ceb hyl leo col pro eul sagmfa

→ 100 mic gal pon chl 90 alo

arboreality igh

h 70

60 pan mmu 50

197

man pap gor 20

-2 -1 0 1 2

← tibia/fibula FXp2 ulna humerus/femur →

Figure 4.19 Fracture (Prin2) x arboreality correlation (r = -0.38539 , df = 42, p = 0.0098**). 197 4.2.2 Fractures and height above ground preference

There is no correlation between overall fracture frequencies and vertical

2 utilization of forest types (r42 = -0.23239, P = 0.1290, r = 5.40%). However, statistically significant associations between the frequencies of certain fractured elements and common height above ground usage are apparent. When fractured bones do occur in primates commonly active at heights over 20 meters, it is more common to fracture the humerus and femur and less common to fracture the clavicle (r42 = -0.36426, P =

2 2 0.0151*, r = 13.27% and r42 = -0.36837, P = 0.0139*, r = 13.57%; Figures 4.20-4.21).

These associations are even more common at heights over 25 meters. Primates active below 20 meters are slightly more likely to fracture their clavicle, tibia, or fibula. In particular, fractures in primates commonly active at heights of 6-10 meters often involve

2 the tibia or fibula (r42 = 0.42982, P = 0.0036**, r = 18.47%; Figure 4.22). There is an association between long bones other than the ulna and heights other than 6-10 meters

2 (r42 = -0.33412, P = 0.0267*, r = 11.16%; Figure 4.23).

198 CORR FXp1*HAGp1

HAGp1

10 →

20 m m 20 oto mmu gal

- mic leo man pap pro aot mfa sai chl eul

pon sag 0 pan

col ceb

199

gor

-10 alo

pba

hyl

-20 m +20 ← (+25 m)

-2 -1 0 1 2

← clavicle, mix ulnaFXp1 other elements →

Figure 4.20 Fracture (Prin1) x height above ground (Prin1) correlation (r = -0.36426 , df = 42, p = 0.0151*).

199 CORR FXp2*HAGp1

HAGp1

10 →

20 m m 20 mmuoto gal

- leo mic man pap aot pro mfa sai chl eul

pon sag 0 pan

col ceb

200 gor

-10 alo

pba

hyl

-20 m +20 ← (+25 m)

-2 -1 0 1 2 ← tibia/fibula FXp2 ulna humerus/femur →

Figure 4.21 Fracture (Prin2) x height above ground (Prin1) correlation (r = -0.36837 , df = 42, p = 0.0139*).

200 CORR FXp2*HAGp3

HAGp3 4 pap

2 gor other heights → mic chl 1 pon eul sag sai pan ceb alo man mfa pba mmu 0 colgal pro aot -1

201 hyl

-2 oto -3

10 m 10 -4 leo

- 6

← ← -5

-2 -1 0 1 2 ← tibia/fibula FXp2 ulna humerus/femur →

Figure 4.22 Fracture (Prin2) x height above ground (Prin3) correlation (r = 0.42982, df = 42, p = 0.0036**).

201 CORR FXp3*HAGp3

HAGp3 4 pap

2 gor other heights → mic chl 1 pon eul sag pan ceb sai alo mfa man pba mmu 0 col pro gal aot -1

202

hyl -2 oto -3

10 m 10 -4 leo

- 6

← ← -5

-2 -1 0 1 2

← ulna FXp3 other elements →

Figure 4.23 Fracture (Prin3) x height above ground (Prin3) correlation (r = -0.33412 , df = 42, p = 0.0267*).

202 4.2.3 Fractures and locomotor mode preference

There is a strong association between overall fracture frequencies and locomotor mode preference (r42 = 0.63172, P = <0.0001***). Although the positive correlation between cross frequencies and the scores provided by the first principle component of the locomotor mode PCA explains only 39.91% of the variation, this association is nevertheless the strongest of all when comparing overall fracture frequencies and the various positional behavior profiles separately. Primates most commonly engaging in suspensory behaviors exhibit the highest overall fracture frequencies, followed by quadupeds, and then leapers.

Patterns also exist regarding the locomotor mode preferences of primates and the location on the body where injuries occur. Primates who often leap or climb are more likely to fracture their clavicle whereas suspensory primates are more likely to fracture a

2 long bone (r42 = 0.34736, P = 0.0209*, r = 12.07%; Figure 4.24). There is a positive correlation between risky locomotor behaviors and fracture location (r42 = 0.37399, P =

0.0124*, r2 = 13.99%; Figure 4.25). Injuries occurring to quadrupedal primates are more likely to involve fractures of the humerus or femur, whereas climbing, leaping, and suspensory behaviors are more often associated with fractures of the tibia or fibula. In addition, fractures in quadrupedal primates tend to involve the ulna (r42 = -0.64302, P =

2 2 <0.0001***, r = 41.35%; Figure 4.26; r42 = -0.33140, P = 0.0280*, r = 10.98%; Figure

4.27).

203 CORR FXp1*LOCp1

LOCp1 4 hyl

pon

. → . usp s 3

2 pan pba

mic ceb uad.

q 1 gor mfa sai mmu leo pap col 0

204 man

-1 alo chl

pro eul otoaot sag

-2 gal leap, leap, climb

← ← -3

-2 -1 0 1 2

← clavicle, mix ulna FXp1 other elements →

Figure 4.24 Fracture (Prin1) x locomotor mode (Prin1) correlation (r = 0.34736, df = 42, p = 0.0209*). 204 CORR FXp2*LOCp2

LOCp2 4 gor

pap

3 pan quad. → quad.

2 man alo chl 1 mfa

mmusai aot 0 oto sag climb pba ceb col leo gal eulpon

205 -1 mic

-2 hyl

., ., leap -3

susp pro

← ← -4

-2 -1 0 1 2 ← tibia/fibula FXp2 ulna humerus/femur →

Figure 4.25 Fracture (Prin2) x locomotor mode (Prin2) correlation (r = 0.37399, df = 42, p = 0.0124*). 205 CORR FXp3*LOCp1

LOCp1 4 hyl

pon

. → . usp

s 3

pan pba ceb mic

1 uad. gor

q mfa mmu sai leo pap

col 0

206

man -1 alo

chl

pro aot eul oto sag

-2 gal

leap, leap, climb ← ← -3

-2 -1 0 1 2

← ulna FXp3 other elements →

Figure 4.26 Fracture (Prin3) x locomotor mode (Prin1) correlation (r = -0.64302 , df = 42, p = <0.0001***). 206 CORR FXp3*LOCp2

LOCp2 4

gor

uad. → uad. 3 pap

q pan

man alo

chl 1 mfa

aotmmu sai 0 sag

pba oto climb ceb col gal 207 pon leo -1 eul mic

-2 hyl

., ., leap -3 susp

pro ← ← -4

-2 -1 0 1 2

← ulna FXp3 other elements →

Figure 4.27 Fracture (Prin3) x locomotor mode (Prin2) correlation (r = -0.33140 , df = 42, p = 0.0280*).

207 4.2.4 Fractures and body mass

There is not a statistically significant correlation between overall fracture

2 frequencies and average body mass (r42 = 0.16660, P = 0.2797, r = 2.78%). Larger primates are slightly more often associated with humeral and femoral fractures than smaller primates, who are more often associated with tibial and fibular fractures (r42 =

2 2 0.48436, P = 0.0009***, r = 23.46%; Figure 4.28; r42 = 0.54530, P = 0.0001***, r =

29.74%; Figure 4.29). Larger primates are likely to have higher frequencies of fractured

2 ulnae (r42 = -0.43305, P = 0.0033***, r = 18.75%; Figure 4.30).

208 CORR FXp2*Mln

Mln 5 gor

pan pon 4

man 3

igh mass mass → igh pap

h col mmu pba 2 hyl alo mfa chl proceb eul

209 1

oto aot 0 sai leo sag -1 gal

-2

mic -3

-2 -1 0 1 2 ← tibia/fibula FXp2 ulna humerus/femur →

Figure 4.28 Fracture (Prin2) x body mass (log of average) correlation (r = 0.48436, df = 42, p = 0.0009***). 209 CORR FXp2*Msd

Msd man 0.9 gor

0.8 pon

0.7 igh mass mass → igh

h 0.6 pap

0.5

mfa col 0.4 chl ceb

210

0.3 pan sai alo mmu 0.2 gal pro hyl 0.1 oto leo aot pba sag 0.0 eul mic

-0.1

-2 -1 0 1 2 ← tibia/fibula FXp2 ulna humerus/femur →

Figure 4.29 Fracture (Prin2) x body mass (sexual dimorphism) correlation (r = 0.54530, df = 42, p = 0.0001***). 210 CORR FXp3*Mln

Mln 5 gor

pan pon 4

man 3

igh mass mass → igh pap

h col mmu pba 2 hyl alo mfa chl ceb pro 1 eul

211 oto aot 0 sai leo sag -1 gal

-2

mic -3

-2 -1 0 1 2

← ulna FXp3 other elements →

Figure 4.30 Fracture (Prin3) x body mass (log of average) correlation (r = -0.43305 , df = 42, p = 0.0033***). 211 4.2.5 Fractures and positional behavior, controlling for body mass

Testing correlations between fracture patterns and various locomotor and habitat use profiles separately might result in a false positive. Body weight places constraints on or facilitates the ability to maneuver in three dimensional space (Cant, 1992). It also impacts the force with which objects fall, affecting the severity of potential subsequent injuries. Consequently, PCAs using the correlation method were performed for each statistically significant correlation. The PCAs consisted of three parameters for each of the 22 taxa:

1. one of the components of the fracture PCA of compositional data,

2. the natural log of the average body mass, and

3. one of the data sets pertaining to the other positional behaviors (arboreality, height above ground, or locomotor mode).

Associations between arboreality and fracture patterns when scaled for the effect of body mass revealed various associations. Fractures using the first component of the fracture PCA (FXp1), mass, and arboreality were subjected to a PCA (Figure 4.31; Table

4.11). Fractures have positive eigenvectors on the first and second principle components

(0.4085 and 0.9083, respectively). Fractures are more strongly associated with mass

(0.3536) than with arboreality (-0.2234) in the second principle component (Prin2), in which fractures explain the largest amount of the variation. However, arboreality is more

212 associated with fractures than mass is in the first component (Prin1). Together, the first two components explain 87% of the variation revealed in the PCA.

Although associations are not clear-cut, in general, the results of the PCA lead to the following conclusions. Terrestrial primates (all large) are associated with fractures of the ulna. Large arboreal primates are associated with humeral and femoral fractures.

Small arboreal primates are associated with tibial and fibular fractures. Small and medium sized arboreal primates are associated with clavicular fractures. Terrestrial primates exhibit more variety and less consistency in the location of fractures received.

When the second component of the fracture PCA (FXp2) is used to test associations between fractures, mass, and arboreality, a similar pattern emerges (Figure

4.32; Table 4.12). The eigenvectors pertaining to fractures that contribute the most variation are found in Prin2 (0.8224). They are associated with arboreality (0.5331) rather than mass (-0.1988), although no clear patterns with particular elements are indicated, suggesting that much of the variation the PCA is reflecting is in fact simply noise. Overall, it appears that mass plays a greater role in explaining fracture patterns than does arboreality, although mass and arboreality are closely linked.

213 ceb F1*M*A hyl Clav leo alo Ulna pbamfa sai Prin3 Hum/Fem pon gal 1.24 Tib/Fib eul col sag aototoaot oto 0.45 chl Mix mmu pan gor pro mic -0.35 1.66 -1.14 1.58 pap 0.22

0.47 man Prin1 Prin2 -1.23 -0.65

-1.76 -2.67

Figure 4.31 Fracture (Prin1) x mass x arboreality PCA. Color coded element labels are based on the results of the compositional data PCA concerning fractured elements. See Figure 3.15 for species labels.

Table 4.11 Correlation matrix eigenvalues, eigenvectors for FXp1*ARB*M eigenvalues eigenvectors eigenvalue difference proportion cumulative Prin1 Prin2 Prin3 Prin1 1.7628 0.9111 0.5876 0.5876 F1 0.4085 0.9083 -0.0897 Prin2 0.8517 0.4663 0.2839 0.8715 A 0.6552 -0.2234 0.7217 Prin3 0.3854 0.1285 1.0000 M -0.6355 0.3536 0.6864 FX = fracture PCA; ARB = arboreality frequencies; HAG = height above ground PCA; LOC = locomotor mode PCA; M = natural log of average body mass p1, p2, or p3 = scores of 1st, 2nd, or 3rd principal components of the original compositional data PCAs Prin1, Prin2, or Prin3 = scores of 1st, 2nd, or 3rd principal components of the resultant correlation data PCA

214 F2*M*A Clav pon Ulna alo gor Prin3 mfamfahylhyl Hum/Fem 1.13 eul col pan Tib/Fib cebpro 0.38 sag chl Mix pba pap man -0.37 aot oto sai 3.43 gal mmu -1.12 1.39 leo

1.52

0.38 mic Prin1 Prin2 -0.38 -0.63

-1.64 -2.28

Figure 4.32 Fracture (Prin2) x mass x arboreality PCA

Table 4.12 Correlation matrix eigenvalues, eigenvectors for FXp2*ARB*M eigenvalues eigenvectors eigenvalue difference proportion cumulative Prin1 Prin2 Prin3 Prin1 1.9926 1.3595 0.6642 0.6642 F2 0.5277 0.8224 -0.2127 Prin2 0.6331 0.2587 0.2110 0.8752 A -0.5841 0.5331 0.6120 Prin3 0.3744 0.1248 1.0000 M 0.6167 -0.1988 0.7617 see Table 4.11 for a description of the abbreviations used here

Associations between fractures and the vertical distribution of primates remain when controlling for mass. The first principle component accounts for 48% of the variance in the PCA measuring fractures (FXp1), mass, and height above ground

215 (HAGp1) (Figure 4.33; Table 4.13). Fractures exhibit high positive loads on all three components, yet the second component has the highest eigenvector pertaining to the fractures variable (0.7373). Neither mass nor HAG have positive loadings for the second eigenvector, suggesting that mass and HAG are more closely connected to each other than either are with fractures. In the first component, the variables mass and fractures both have positive loadings while mass has negative loadings, suggesting that fracture frequencies are associated with mass more than with HAG. Fracture patterning is less clustered in this PCA, although clavicular fractures appear to be associated with small and medium sized primates commonly occupying heights of less than ten meters.

The PCAs comparing FXp2, mass, and HAGp1 (Figure 4.34; Table 4.13), FXp2, mass, and HAGp3 (Figure 4.35; Table 4.15), and FXp3, mass, and HAGp3 (Figure 4.36;

Table 4.16) all show the highest eigenvalues for the variable fracture in the third component. Unfortunately, the third component for each of these PCAs largely consists of noise, without clear patterns, so the first components were examined more closely.

The first component of the FXp2*M*HAGp1 PCA has positive loadings for fractures

(0.5903) and mass (0.5982), but not HAG (-0.5419). Large and very large primates active at heights greater than 20 meters tend to fracture their humerus or femur. The first component of the FXp2*M*HAGp3 has strong positive loadings for all three variables, but fractures (0.627705) are slightly more closely associated with mass (0.566012) than

HAG (0.534431). Large and very large primates commonly found at heights of 0-5 meters tend to fracture their ulna. Small primates typically distributed at less than ten meter heights are more likely to fracture their tibia or fibula. The first component of the

FXp3*M*HAGp3 PCA has negative loadings for fractures (-0.6131) and positive

216 loadings for both height (0.5269) and mass (0.5886). Overall, it appears as if fractures are highly associations with mass and height above ground preferences.

F1*M*H1 ceb Clav

leo Ulna

Prin3 alo hyl Hum/Fem sai 0.95 gor Tib/Fib gal mfa mmu Mix 0.32 pba pon pan pap pan

-0.31 sag eul aototo chl 2.58 col -0.95 1.81 mic man 1.09

0.59 pro Prin1 Prin2 -0.39 -0.63

-1.84 -1.87

Figure 4.33 Fracture (Prin1) x mass x height above ground (Prin1) PCA

Table 4.13 Correlation matrix eigenvalues, eigenvectors for FXp1*HAGp1*M eigenvalues eigenvectors eigenvalue difference proportion cumulative Prin1 Prin2 Prin3 Prin1 1.4384 0.2311 0.4795 0.4795 F1 0.4098 0.7373 0.5371 Prin2 1.2072 0.8528 0.4024 0.8819 H1 -0.7711 -0.0346 0.6357 Prin3 0.3544 0.1181 1.0000 M 0.4873 -0.6747 0.5544 see Table 4.11 for a description of the abbreviations used here

217 F2*M*H1

pon gor F2*M*H1 pan Clav man pap Ulna Prin3 mmu

col Hum/Fem 1.23 mfa pro chl Tib/Fib eul alo ceb 0.33 pba oto Mix hyl aot leo sai -0.57 sag gal 2.97

-1.47 1.19

mic 1.15

0.07 Prin1

Prin2 -0.67 -1.06

-2.49 -2.19

Figure 4.34 Fracture (Prin2) x mass x height above ground (Prin1) PCA

Table 4.14 Correlation matrix eigenvalues, eigenvectors for FXp2*HAGp1*M eigenvalues eigenvectors eigenvalue difference proportion cumulative Prin1 Prin2 Prin3 Prin1 1.8290 1.1726 0.6097 0.6097 F2 0.5903 0.4390 -0.6774 Prin2 0.6564 0.1417 0.2188 0.8284 H1 -0.5419 0.8375 0.0704 Prin3 0.5147 0.1716 1.0000 M 0.5982 0.3255 0.7323 see Table 4.11 for a description of the abbreviations used here

218 F2*M*H3 pap Clav Ulna Prin3 Hum/Fem

→ 1.34 chl mic pba pan pon gor mmu sai Tib/Fib ceb col 0.49 cebeul man Mix pro mfa sag eul alo gal -0.35 aot 2.71

← +20 ← -1.19 2.10 hyl oto 0.82

0.91 Prin1 Prin2 leo -1.06 -0.27

-1.46 -2.95

Figure 4.35 Fracture (Prin2) x mass x height above ground (Prin3) PCA

Table 4.15 Correlation matrix eigenvalues, eigenvectors for FXp2*HAGp3*M eigenvalues eigenvectors eigenvalue difference proportion cumulative Prin1 Prin2 Prin3 Prin1 1.8027 1.0808 0.6009 0.6009 F2 0.6277 -0.0816 -0.7742 Prin2 0.7219 0.2466 0.2406 0.8415 H3 0.5344 0.7683 0.3524 Prin3 0.4754 0.1585 1.0000 M 0.5660 -0.6349 0.5258 see Table 4.11 for a description of the abbreviations used here

219 F3*M*H3 Clav gor pap Prin3 Ulna

1.72 Hum/Fem alochl pon man pro Tib/Fib sag eul col pan 0.71 ceb colmmummu sai micgal Mix gal mfa pba -0.29 aot 2.89 -1.30 1.73 hyl

oto 1.12 0.57 Prin1 Prin2 -0.66 -0.58 leo

-1.74 -2.43

Figure 4.36 Fracture (Prin3) x mass x height above ground (Prin3) PCA

Table 4.16 Correlation matrix eigenvalues, eigenvectors for FXp3*HAGp3*M eigenvalues eigenvectors eigenvalue difference proportion cumulative Prin1 Prin2 Prin3 Prin1 1.7029 0.9664 0.5676 0.5676 F3 -0.6131 0.2382 0.7532 Prin2 0.7364 0.1758 0.2455 0.8131 H3 0.5269 0.8337 0.1653 Prin3 0.5607 0.1869 1.0000 M 0.5886 -0.4982 0.6367 see Table 4.11 for a description of the abbreviations used here

Figures 4.37-4.40 and Tables 4.17-4.20 illustrate associations between fracture patterns and locomotor mode preferences when controlling for body mass. When the variables fractures (FXp1), mass, and locomotion (LOCp1) were subjected to a PCA, the eigenvectors of fractures experienced the highest loadings in the second component

220 (0.7789). Locomotor modes were more associated with fractures than with mass in this component. When examining the other PCAs performed using the combinations of fractures, mass, and locomotor modes determined to be correlated significantly, both mass and locomotion eigenvalues were similarly loaded under the components with the largest fracture eigenvalues. Although both mass and locomotion had positive loadings in the FXp3*M*LOCp1 and FXp3*M*LOCp2 PCAs, locomotion was more closely associated with fractures than mass in both. The opposite situation occurred in the

FXp2*M*LOCp2 PCA, with both mass and locomotion having negative loadings with mass being more closely associated with fractures than locomotion.

PCAs testing associations between fractures and locomotor mode when controlling for mass suggest the following conclusions. Large suspensory primates tend to fracture humeri or femora. Primates that often engage in climbing behaviors are more likely to fracture their clavicle or ulna; if they are medium-sized, they are more likely to fracture their clavicle than their ulna. There is no association between leaping and fracture distribution. Those primates exhibiting ulnar fractures tend to be large and quadrupedal. Tibular and fibular fractures predominate in many large- and small-sized quadrupedal primates. Clavicular fractures also are often seen in large quadrupeds.

Overall, locomotor mode frequencies appear to be less dependent upon mass than habitat use preferences.

221 F1*M*L1 Clav ceb hyl Ulna leo alo Hum/Fem Prin3 gor sai 1.19 mfa Tib/Fib mmupba pon gal pan Mix 0.16 pap

-0.86 sag eul col chl mic aototo 2.26 -1.89 man 1.87

0.98 pro 0.62 Prin1 Prin2 -0.30 -0.63

-1.88 -1.58

Figure 4.37 Fracture (Prin1) x mass x locomotor mode (Prin1) PCA

Table 4.17 Correlation matrix eigenvalues, eigenvectors for FXp1*LOCp1*M eigenvalues eigenvectors eigenvalue difference proportion cumulative Prin1 Prin2 Prin3 Prin1 1.4443 0.2402 0.4814 0.4814 F1 0.3465 0.7789 0.5227 Prin2 1.2041 0.8525 0.4014 0.8828 L1 0.7666 0.0861 -0.6364 Prin3 0.3516 0.1172 1.0000 M 0.5407 -0.6212 0.5673 see Table 4.11 for a description of the abbreviations used here

222 F3*M*L1 gor pon Clav Ulna hyl Hum/Fem pan Prin3 man col mmu Tib/Fib alo 0.98 ceb pba Mix pro mfa 0.19 chl leo sai pap

oto eul -0.61 gal sag aot mic 2.55 -1.40 1.60

0.86

0.35 Prin1 Prin2 -0.84 -0.90

-2.16 -2.53

Figure 4.38 Fracture (Prin3) x mass x locomotor mode (Prin1) PCA

Table 4.18 Correlation matrix eigenvalues, eigenvectors for FXp3*LOCp1*M eigenvalues eigenvectors eigenvalue difference proportion cumulative Prin1 Prin2 Prin3 Prin1 1.9972 1.3504 0.6657 0.6657 F3 -0.6114 0.3235 0.7221 Prin2 0.6468 0.2907 0.2156 0.8813 L1 0.6034 -0.3998 0.6900 Prin3 0.3561 0.1187 1.0000 M 0.5120 0.8576 0.0492 see Table 4.11 for a description of the abbreviations used here

223 F2*M*L2 Clav alo gor Ulna sag Prin3 mfa Hum/Fem 1.24 pap hyl eul Tib/Fib man gal 0.43 pon Mix ceb pro chl -0.38 aot mic col pan 3.35 sai -1.19 oto 1.51 leo mmu 1.40 pba 0.59 Prin1 Prin2 -0.56 -0.33

-1.26 -2.51

Figure 4.39 Fracture (Prin2) x mass x locomotor mode (Prin2) PCA

Table 4.19 Correlation matrix eigenvalues, eigenvectors for FXp2*LOCp2*M eigenvalues eigenvectors eigenvalue difference proportion cumulative Prin1 Prin2 Prin3 Prin1 1.9092 1.2826 0.6364 0.6364 F2 0.5568 0.7355 0.3860 Prin2 0.6266 0.1624 0.2089 0.8453 L2 0.5652 -0.6760 0.4729 Prin3 0.4642 0.1547 1.0000 M 0.6087 -0.0451 -0.7921 see Table 4.11 for a description of the abbreviations used here

224 F3*M*L2 gor Clav Ulna Hum/Fem Prin3 man pan Tib/Fib 1.59 alo pon Mix colmmu 0.65 chl pap

-0.30 otopro ceb mfa pba eul hyl sai 2.70 sag aot -1.24 gal leo 1.88

1.08

0.80 Prin1 Prin2 mic -0.54 -0.28

-1.36 -2.16

Figure 4.40 Fracture (Prin3) x mass x locomotor mode (Prin2) PCA

Table 4.20 Correlation matrix eigenvalues, eigenvectors for FXp3*LOCp2*M eigenvalues eigenvectors eigenvalue difference proportion cumulative Prin1 Prin2 Prin3 Prin1 1.8482 1.1726 0.6161 0.6161 F3 -0.5390 0.7927 0.2849 Prin2 0.6756 0.1993 0.2252 0.8412 L2 0.5750 0.5934 -0.5633 Prin3 0.4763 0.1588 1.0000 M 0.6156 0.1398 0.7756 see Table 4.11 for a description of the abbreviations used here

225 4.2.6 Associations between fractures and positional behavior

For some skeletal elements, fracture frequencies are associated with positional behaviors both independently and when controlling for body mass. In order to determine which locomotor and habitat use preferences contribute the most to fracture frequencies, all variables were subjected to a PCA. The Full PCA was composed of all five variables: fracture element frequencies (FX), arboreality (ARB), height above ground (HAG), locomotor mode (LOC), and body mass (MASS) (Figure 4.41 and Table 4.21). In order to test the validity of the associations made between fracture patterns and positional behavior in the Full PCA, it was compared to a Positional Behavior PCA. The Positional

Behavior PCA was composed only of the four positional behavior variables: arboreality

(ARB), height above ground (HAG), locomotor mode (LOC), and body mass (MASS)

(Figure 4.42 and Table 4.22).

Figure 4.41 and Table 4.21 depict the results of the Full PCA performed on the variables FX, ARB, HAG, LOC, and MASS. The eigenvectors for the variables FX and

LOC both have positive loadings for each of the first three components, which combined account for 86.22% of the variance. The most positive loading for FX occurs in the second component (0.617739). Both ARB and LOC also have positive loadings, although arboreality is slightly more associated with fractures than locomotion on that axis, with eigenvalues of 0.570163 and 0.230432, respectively. This component mainly seems to reflect arboreality. The first component more closely reflects overall fracture frequencies (cross frequencies) than the second component. The first component also seems to reflect mass and differentiate between heights above and below twenty meters.

226 FX (0.167594), LOC (0.543159), and MASS (0.568335) all have positive loadings for this axis. FX (0.539259) and HAG (0.603803) have approximately equal positive loadings for the third component and consequently are associated, although only heights above twenty meters and heights below five meters seem to drive the variation reflected in the third component. In essence, frequencies of fractured elements among nonhuman primates appear to be most closely associated with locomotor mode, followed by arboreality, vertical distribution, and body mass, although each of these variables are interconnected.

Clav F*A*H*L*M hyl ceb Ulna

leo Hum/Fem Prin3 gor 1 pon sai mmu Tib/Fib

5 m m → 5 1.31

- pap mfa pap alo pba panpan Mix 0.45 mic gal -0.40 2 3 4 man col 2.65 sag chl -1.26 aot eul ← +20 m +20 ← 2.39 oto

1.11 0.62 5 pro Prin1 Prin2 -0.42 -1.14

-2.91 -1.96

Figure 4.41 Full PCA – Fractures x Arboreality x Height Above Ground x Locomotor Mode x Mass (FXp1*A*HAGp1*LOCp1*M). Fracture legend: C = clavicle, H/F = humerus/femur, U = ulna, T/B = tibia/fibula, M = mix (no preference for one element over the others). Sext text for a description of the five numbered clusters.

227 Table 4.21 Correlation matrix eigenvalues, eigenvectors for F1*A*H1*L1*M eigenvalues eigenvalue difference proportion cumulative Prin1 2.0089 0.3132 0.4018 0.4018 Prin2 1.6957 1.0893 0.3391 0.7409 Prin3 0.6065 0.1113 0.1213 0.8622 Prin4 0.4951 0.3014 0.0990 0.9612 Prin5 0.1938 0.0388 1.0000 eigenvectors Prin1 Prin2 Prin3 Prin4 Prin5 F1 0.1676 0.6177 0.5393 -0.4539 0.3058 A -0.3130 0.5702 -0.4770 0.3918 0.4426 H1 -0.5059 -0.3188 0.6038 0.3575 0.3873 L1 0.5432 0.2304 0.2977 0.7158 -0.2256 M 0.5683 -0.3722 -0.1687 -0.0162 0.7139 F1 = 1st component of fracture PCA; A = arboreality frequencies; H1 = 1st component of height above ground PCA; L1 = 1st component of locomotor mode PCA; M = natural log of average body mass

Five clusters are revealed in the Full PCA and have been bounded by numbered ellipses in Figure 4.41.

1. Suspensory Primates: Hylobates spp. and Pongo pygmaeus are both large, arboreal, suspensory primates.

2. Small/Medium Arboreal Quadrupeds: Cebus apella, Saimiri boliviensis,

Leontopithecus rosalia, and Microcebus murinus are small- or medium-sized arboreal quadrupeds which primarily occupy heights of less than ten meters.

3. Large Arboreal Quadrupeds: Macaca fascicularis, Alouatta seniculus, Procolobus badius, and Colobus guereza are large, arboreal quadrupeds. Chlorocebus pygerythrus is considered to be a large semi-terrestrial quadruped. 228 4. Terrestrial Quadrupeds: Gorilla gorilla, Mandrillus sphinx, Papio spp., Pan troglodytes, and Macaca mulatta are very large, terrestrial quadrupeds.

5. Leaping/Climbing Primates: Propithecus verreauxi, Eulemur fulvus, and Galago senegalensis primarily engage in leaping behaviors and Otolemur crassicaudatus, Aotus lemurinus, and Saguinus oedipus primarily engage in climbing behaviors. Together, they are all small- or medium-sized, arboreal primates active at heights of less than twenty meters.

Overall, large suspensory primates experience some of the highest fracture frequencies (cross fractures) while small/medium leaping primates experience some of the lowest frequencies of fractures. When Suspensory primates break a bone, it tends to be either the humerus or femur. The Terrestrial Quadruped and Large Arboreal

Quadruped groups do not appear to exhibit any patterns in which elements fracture most often, although they tend to have few, if any, tibial or fibular fractures. Papio spp.,

Macaca fascicularis, and Pan troglodytes tend to fracture their ulna whereas Colobus guereza, Mandrillus sphinx, and Chlorocebus pygerythrus tend to fracture their clavicle.

Gorilla gorilla and Alouatta seniculus preferentially fracture their humerus or femur.

Procolobus badius shows no preference in fracture location. Macaca mulatta tends to exhibit fractures of the fibula. Conversely, primates in the Small/Medium Arboreal

Quadruped group most often experience tibial and fibular fractures. One exception is

Microcebus murinus, which shows no preference for fracture location (e.g., mix). The

Leaping/Climbing Primates cluster features species which tend either to involve the

229 clavicle preferentially or are independent of location (e.g., mix). Galago senegalensis is an exception, predominantly featuring tibial or fibular fractures.

The Full PCA was compared to the Positional Behavior PCA (Figure 4.42 and

Table 4.22) to determine which primates have fracture patterns which are appreciably different from expectations. The first three components combined account for 93.92% of the variance. In short, these components represent the following variables: the first component reflects mass; the second, arboreality; and the third, height above ground

(dividing taxa into primates active above and below twenty meters). The eigenvalues of the variable LOC have positive loadings on all three components. The first component distinguishes leaping and climbing from suspensory behaviors and quadrupedalism, whereas the second category distinguishes suspensory from quadrupedal movements.

The second component also distinguishes mass categories of quadrupedal primates

(small/medium quadrupeds, large quadrupeds, and very large terrestrial quadrupeds).

230 CORR FXp1*ARB pMln

Clav A*H*L*M hyl pon Ulna Hum/Fem Prin3 Tib/Fib pba 1 1.39 pan ceb Mix gor mic mfa sai 0.40 leo col mmu pap

20 m m 20→ leo -

-0.59 alo 2 man chl 3 2.82

eulpro -1.57 sag aototo 4 ← +20 m +20 ← 2.58 gal

1.17

0.95 5 Prin1 Prin2 -0.49 -0.69

-2.14 -2.33

Figure 4.42 Positional behavior PCA – Arboreality x Height Above Ground x Locomotor Mode x Mass (A*HAGp1*LOCp1*M). Sext text for description of the five numbered clusters.

Table 4.22 Correlation matrix eigenvalues, eigenvectors for A*H1*L1*M eigenvalues eigenvectors eigenvalue difference proportion cumulative Prin1 Prin2 Prin3 Prin4 Prin1 1.9923 0.7684 0.4981 0.4981 A -0.3992 0.6982 -0.0113 0.5942 Prin2 1.2239 0.6831 0.3060 0.8040 H1 -0.4489 -0.5458 0.6141 0.3514 Prin3 0.5408 0.2977 0.1352 0.9392 L1 0.4981 0.3872 0.7686 -0.1056 Prin4 0.2431 0.0608 1.0000 M 0.6253 -0.2545 -0.1786 0.7158 A = arboreality frequencies; H1 = 1st component of height above ground PCA; L = 1st component of locomotor mode PCA; M = natural log of average body mass

Despite the addition of fracture scores in the Full PCA, values do not differ appreciably from those revealed in the Positional Behavior PCA. Taxa form the same

231 clusters in both PCAs. The six species which shifted the most in their locations in three- dimensional space between the two PCAs are Propithecus verreauxi, Leontopithecus rosalia, Cebus apella, Galago senegalensis, Colobus guereza, and Pongo pygmaeus.

These species shifted in two of the three dimensions, except for Propithecus verreauxi, which shifted in all three dimensions. However, Propithecus verreauxi is unique in that only one fracture was observed, thereby inflating the significance of the value recorded for it. Pongo pygmaeus, Cebus apella, and Leontopithecus rosalia have the first, third, and fourth highest overall (cross) fracture frequencies, respectively. Conversely, Galago senegalensis, Colobus guereza, and Propithecus verreauxi have the second, third, and fourth lowest overall fracture frequencies, respectively.

4.3 Impact of intraspecific factors at Cayo Santiago

Subsets of a population may experience different injury risks which could influence fracture frequencies. The free-ranging colony of rhesus macaques (Macaca mulatta) on the island of Cayo Santiago in Puerto Rico was observed more closely to examine such intraspecific factors. Fracture frequencies were compared by sex and age categories as well as by changes in managed care over time. In total, 484 Cayo Santiago macaques were examined for evidence of antemortem long bone fractures. Within this sample, 85 fractures were recognized, distributed across 62 individuals.

232 Tables 4.23 and 4.24 and Figure 4.43 depict the sex and age categories of fracture frequencies at Cayo Santiago. Age categories are based on criteria for adulthood in rhesus macaques by Wells and Turnquist (2001). Advanced age appears to be associated with increased fracture frequencies. Fracture frequencies increase sequentially as age categories increase: 2% of all fractures occur in infants, 8% in juveniles, 26% in young adults, 34% in middle adults, and 30% in mature adults. This increase is statistically

2 significant (χ 4 = 61.6242, P = <0.0001***). There is no statistically significant

2 difference between male and female fracture frequencies (χ 1 = 3.4313, P = 0.0640).

However, females over twenty years of age have fracture frequencies surpassing one hundred percent (106.25% using cross frequencies). Likely these high frequencies are due to the tendency for females to live longer than males coupled with the likelihood for older individuals of both sexes to suffer from multiple injuries.

233 Table 4.23 Comparison of fracture frequency by sex and age in the Cayo Santiago population (cross %) Infant Juvenile Adult I Adult II Adult III N n % N n % N n % N n % N n % Males 16 2 12.50 38 3 7.89 124 6 4.84 69 21 30.43 18 10 55.56 Females 16 0 0.00 35 2 5.71 90 14 15.56 60 10 16.67 16 17 106.25 Total: 32 2 6.25 73 5 6.85 214 20 9.35 129 31 24.03 34 27 79.41 Infant = 0-10 mo., Juvenile = 10 mo. - 3 yr., Adult I = 3-10 yr., Adult II = 10-20 yr., Adult III = 20+ yr. N = total number of individuals examined; n = total number of fractures; % = cross frequency

Table 4.24 Comparison of fracture frequency by sex and age in the Cayo Santiago population (individual %)

234 Infant Juvenile Adult I Adult II Adult III N n % N n % N n % N n % N n %

Males 16 1 6.25 38 3 7.89 124 6 4.84 69 14 20.29 18 7 38.89 Females 16 0 0.00 35 1 2.86 90 11 12.22 60 8 13.33 16 11 68.75 Total: 32 1 3.13 73 4 5.48 214 17 7.94 129 22 17.05 34 18 52.94 Infant = 0-10 mo., Juvenile = 10 mo. - 3 yr., Adult I = 3-10 yr., Adult II = 10-20 yr., Adult III = 20+ yr. N = total number of individuals examined; n = number of individuals with one or more fractures; % = individual frequency

234 Infant

Juvenile

Adult I female Adult II male

Adult III

100-1 - 800.8 -600.6 -400.4 - 0.220 0%0 0.220 0.440 0.660 0.880 1001

Figure 4.43 Fracture distribution by sex and age at Cayo Santiago

Provisioning for and managed care of the Cayo Santiago macaques has improved dramatically since shortly after the inception of the colony in 1938 (Rawlings and

Kessler, 1986). Throughout the 1940s and 1950s, the colony was virtually abandoned due to lack of financial support for the population and the involvement of the United

States in World War II. Malnutrition, wounds and injuries from fighting, and cannibalism all were recorded in census records during the unfunded interval. However, in 1958, regular provisioning and advancements in water collection became available for the colony. Subsequent population pressure due to annual population increases led to a cull in 1972. Buikstra (1975) examined fractures in a series of skeletal samples derived in part from the 1972 cull. Following another cull in 1983, annual trapping and removal of some yearlings has served to maintain a stable colony population size to the present.

The skeletal sample used in this study consists of 484 Cayo Santiago-derived rhesus macaques (Macaca mulatta) which died after 1972. In order to assess whether changes in provisioning and managed care have affected fracture frequencies over time at

Cayo Santiago, a smaller subset of the sample consisting of 352 macaques with known 235 births dating from 1973 or later was compared to the sample Buikstra (1975) examined:

175 macaques sacrificed in 1972 or otherwise obtained prior to that time. Pre-cull refers to Buikstra's (1975) full sample of Group K and non-K series combined, prior to the start of regular provisioning. Post-cull refers to a subset of the present sample born after the

1972 cull and the advancements in managed care.

Of the Post-cull sample of 376 macaques examined, 52 fractures were observed in

39 individuals (Table 4.25). Buikstra (1975) reported 26 out of 175 individuals with fractures in the Pre-cull sample. When juveniles are excluded, the Post-cull adult sample

2 exhibits a significantly lower cross fracture frequency than the Pre-cull adult sample (χ 1

= 5.9197, P = 0.0150*), although frequencies in the total population of the Pre-cull and

Post-cull samples are not significantly different when examining either cross frequencies

2 2 (χ 1 = 2.8405, P = 0.0919) or individual frequencies (χ 1 = 2.3084, P = 0.1287).

Table 4.25 Comparison of fracture frequencies before and after provisioning 1 individuals elements cross % N n % N n % (En/IN) Died before or in 1972 cull2 175 26 14.86 … … … … Died before or in 1972 cull2,4 77 23 29.87 … 27 … 35.06 Born after 1972 cull3 376 39 10.37 5181 52 1.00 13.83 Born after 1972 cull3,4 171 28 16.37 2371 37 1.56 21.64 N = total number of individuals or elements examined n = total number of fractures in individuals or elements 1. using Buikstra's criteria for sexually mature adults at 6 years old 2. data derived from Buikstra (1975) 3. present study 4. adults only

236 4.4 Chapter summary

Fractures were most commonly found in Cebus apella, Procolobus badius, and

Pongo pygmaeus and least commonly found in Galago senegalensis, Saguinus oedipus, and Colobus guereza. In general, it is most common for primates to fracture their fibula, clavicle, or ulna, although fracture location varies considerably among species.

Transverse fractures were more common than any other fracture type observed. Most fractures healed fairly well, with minimal deformity and few complications. Fracture patterns appear to be most closely associated with locomotor mode, followed by arboreality, vertical distribution, and body mass, although each of these variables are interconnected. Numerous factors may alter fracture frequencies within populations or species, although these variations usually are not significantly different.

237

CHAPTER 5: Discussion

5.1 Impact of arboreality on fracture frequencies

The analysis of fracture frequencies relative to degree of arboreality yielded results that were counter to expectations. Arboreal primate taxonomic groups were predicted to exhibit increased fracture frequencies compared to terrestrial primates, when examined independent of other positional behaviors. These data indicate that falls related to degree of arboreality alone seem unlikely to explain overall fracture frequencies (r42 =

0.01348, P = 0.9308). However, on the scale of arboreality, those primates that are completely arboreal (including Procolobus badius, Cebus apella, Otolemur crassicaudatus, and Hylobates spp.) tend to have very high overall fracture frequencies.

The locomotor behaviors of these taxa differ considerably, suggesting that this association has more to do with degree of arboreality than locomotor mode preferences.

Degree of arboreality and fracture location (the patterning of fractures based on affected skeletal elements) are significantly correlated (r42 = -0.38539, P = 0.0098**).

When a bone is fractured among terrestrial primates, it is more likely to be the humerus or femur, whereas arboreal primates are more likely to fracture their tibia or fibula. This association is stronger in smaller arboreal primates than in larger arboreal primates. The

238 location of fractures appears to vary functionally and will be discussed further in the

Implications for Primate Evolution subheading of this chapter. Fractures appear to be associated more with mass than arboreality. The large-bodied Pongo pygmaeus exhibits the highest fracture frequencies in this sample and, although it is not completely arboreal, it is the most arboreal of the great apes.

Pontzer and Wrangham (2004) tested the hypothesis that arboreal adaptations in chimpanzees minimize energy expenditure by decreasing the energy spent climbing.

They found that climbing incurs a significant energy cost, suggesting that other factors, such as minimizing mortalities caused by falls, drive the maintenance of costly arboreal adaptations. Thorpe and Crompton (2006) suggest that orangutan locomotor adaptations should be directed even more towards avoiding falls, since they have a higher degree of arboreality than chimpanzees. Their larger body mass also makes it less likely that they will survive falls from heights (Thorpe and Crompton, 2006). Although orangutans are careful climbers, this study substantiates prior findings (Schultz 1956) of high fracture prevalence. The substantial amount of time they spend in the trees in combination with their large body mass results in orangutans being more vulnerable to fractures from falling than any other primate examined in the current sample.

When ranking taxa in terms of overall fracture frequencies, those taxa which are the least arboreal tend to have fracture frequencies in the middle range. Overall fracture frequencies for Papio spp. and Pan troglodytes are slightly higher than the average of all primates examined in this study, whereas Mandrillus sphinx, Gorilla gorilla, and Macaca mulatta frequencies are slightly lower than average. Bramblett (1967) suggested that the high frequencies of fractures exhibited by the yellow baboons (Papio cynocephalus) in

239 his skeletal sample could be explained by the fact that baboons frequently fell out of trees, because they were unskilled at maneuvering within arboreal habitats. Lovell

(1991) partially supports Bramblett‟s explanation, based on comparisons of fracture frequencies obtained from the literature, including Bramblett‟s sample. However,

Lovell‟s series included only apes and a few monkey species. The primates compared in the current study provide a more comprehensive series of taxa exhibiting varying degrees of arboreality, including prosimians and a larger selection of monkeys. Based on these results, baboons (Papio spp.) rank only the 8th highest in overall fracture frequencies.

They and other primate taxa more suited to terrestrial locomotion appear not to experience more severe falls from heights resulting in long bone fractures than many arboreal primates.

The published literature does little to shed light on whether terrestrial primates fall more often than arboreal primates. Quantitative information concerning the prevalence of falls among primate species is lacking in the literature and mainly consists of descriptions of isolated incidents. For instance, Bramblett (1967) cites that baboons at

Darajani (P. cynocephalus) are noisy and clumsy climbers, often falling from trees as branches break beneath them, as evidence to support his proposition that high fracture frequencies within his sample are due to falls. However, Rowell (1966) never saw a fall when surveying a forest-dwelling troop of P. anubis in Uganda. Hall (1962) never observed serious accidental falls from rock climbing among P. ursinius, although falls from trees occurring during playing among subadults were not uncommon. Male yellow baboons (Papio cynocephalus) in Tanzania were observed to fall from heights of up to 12 meters during agonistic encounters with conspecifics, although none resulted in injury

240 (Drews, 1996). Rather than falling due to their unfamiliarity with being in an arboreal environment, as Bramblett (1967) suggests, some of these baboons were induced to fall when rival baboons shook terminal branches until they fell off (Drews, 1996). One adult male olive baboon (Papio anubis) in Kenya was observed to leap off a cliff ledge 10 meters above the ground, when confronted by a higher ranking male (Harding, 1980). He was apparently stunned, unable to move for 10 minutes. No deaths due to falling were recorded during either a four year study of a chacma baboon (Papio ursinus) troop in

Namibia (Brain, 1992) or a ten year study of a gray-footed chacma baboon (Papio ursinus griseipes) troop in Botswana (Cheney, et al., 2004). However, one adult male who was weakened when most of his mouth was bitten off during a fight with a rival, stumbled around and eventually fell onto a cobra which struck him twice, killing him

(Brain, 1992). Whether any baboons fell and survived the fall was not recorded in either study. Observations of falls among Papio spp. do little either to refute or support the proposition that baboons (and other terrestrial primates) are more likely to fall from heights when they are arboreal than primates which spend more time in the trees.

5.2 Impact of height above ground on fracture frequencies

It was hypothesized that primate groups commonly ranging at greater heights above the ground when arboreal will have an increased risk of receiving fractures, should they fall, than primates more commonly active at lower vertical dimensions. These data

241 suggest that canopy height utilization alone contributes little to overall fracture risk (r42 =

-0.23239, P = 0.1290). Of the primates exhibiting the lowest fracture frequencies,

Galago senegalensis and Colobus guereza are most often active at 6-10 meter heights; however, Saguinus oedipus is most often active at heights over 20 meters. Of the primates exhibiting the highest fracture frequencies, Procolobus badius and Cebus apella are commonly active at heights above 20 meters, whereas Pongo pygmaeus is most active at heights ranging from 11-20 meters. These findings are comparable to results reported for trauma in cercopithecoids as related to canopy usage – the hypothesis that canopy height utilization alone explains the variation in fracture frequencies is rejected by the data (Chapman, et al., 2007; Chapman and Legge, 2009).

The location of fractures is correlated with the canopy heights that primates prefer. Primates active at heights above 20 meters are more prone to fracture the humerus or femur (r42 = -0.36426, P = 0.0151* and r42 = -0.36837, P = 0.0139*), whereas primates more commonly active at 6-10 meter heights tend to fracture the tibia or fibula preferentially (r42 = 0.42982, P = 0.0036**). Vertical distribution appears to be less associated with fracture frequencies than mass. In general, large and very large arboreal primates prefer to remain high in the canopy. Colobus guereza is the only large arboreal primate in this study which commonly travels in the canopy at heights under 10 meters, and even then can be found relatively equally in all height categories above 5 meters. Conversely, small and medium sized primates in general prefer to remain lower in the canopy. Clavicular fractures are common in these primates, including Microcebus murinus, Propithecus verreauxi, Eulemur fulvus, and Otolemur crassicaudatus.

242 Terrestrial primates, who rarely exceed heights of 5 meters when they are arboreal, except for Gorilla gorilla, tend to fracture their ulna.

5.3 Impact of locomotor mode on fracture frequencies

As expected, overall fracture frequencies are correlated with locomotor mode frequencies among nonhuman primates, when examined independently of all other positional behaviors (r42 = 0.63172, P = <0.0001***). Primate taxa that engage in more specialized locomotor modes, including leaping and suspensory behaviors, were expected to have higher fracture frequencies than primates which utilize less risky locomotor behaviors, such as generalized quadrupedalism. This hypothesis is partially supported by the data: suspensory behaviors (including brachiation) are indeed associated with high fracture frequencies. However, counter to expectations, leaping (primarily vertical clinging and leaping) is associated with low frequencies of fractures independent of body size.

Although long bone fractures are uncommon in all primates examined in this study, the distribution of skeletal trauma is associated with common locomotor mode frequencies. When they fracture a bone, taxa that engage in high frequencies of leaping and climbing are more likely to break their clavicle (r42 = 0.34736, P = 0.0209*).

Clavicular fractures are especially closely associated with medium-sized primates which climb frequently. Fractures of the tibia, fibula, or ulna are most often associated with

243 quadrupedal primates (r42 = 0.37399, P = 0.0124*; r42 = -0.64302, P = <0.0001***; r42 =

-0.33140, P = 0.0280*). Specifically, fractures in large or very large quadrupedal primates tend to involve the ulna whereas fractures in small and medium sized quadrupedal primates involve the tibia and fibula preferentially. Suspensory primates are also likely to fracture their humeri or femora when they break a bone.

Mass and locomotion are interrelated. For instance, there are no really large leapers: primates most commonly exhibiting climbing or vertical clinging and leaping behaviors are also small or medium sized. Climbing tends to increase with body size.

Suspensory primates are large or very large in body mass. These results reflect trends documented for New World monkeys in Surinam (Fleagle and Mittermeier, 1980).

Locomotor mode and body mass both effect fracture frequencies and patterning.

Although it is difficult to separate the impact caused by locomotion from that caused by mass, locomotion is correlated more with fracture frequencies than mass is correlated with fracture frequencies. Consequently, falls resulting in trauma appear to be more closely associated with locomotor mode preferences than with mass.

Leapers exhibit the lowest fracture frequencies of the current sample. Even amongst the leapers examined in this study, there is an inverse relationship between leaping and fracture prevalence rates. For instance, Otolemur crassicaudatus, which leaps with the least frequency of all the galagines (Oxnard, et al., 1981), exhibits the highest fracture frequencies of all the prosimians. Although all fractures in Galago senegalensis are located on the lower limb, leaping and climbing behaviors in general are associated with clavicular fractures. These differences may be related to the forces generated by leaping, in that Galago senegalensis is both small-bodied and a frequent

244 leaper. The unique cylindrical shape of the femoral heads in Galago senegalensis assists in the creation of simple flexion-extension movements (rather than the rotational movements of the ball-and-socket joint exhibited in other primates) which help maintain mechanical efficiency and avoid the possibility of receiving twisting injuries during takeoff (Fleagle, 1999).

Although neither Colobus guereza nor Procolobus badius were classified leapers in this study, both primates engage in pronograde leaping relatively frequently.

Procolobus badius, however, covers further horizontal distances and longer vertical drops during leaps than Colobus guereza (Gebo and Chapman, 1995). Colobines are considered confident jumpers and good leapers (Fleagle, 1999; Arlet et al., 2009). No falls were observed among guerezas at Kibale in Uganda during several months of behavioral observations (Arlet et al., 2009). Conversely, falls among red colobus monkeys at Kibale are common, often involving immature monkeys (Struhsaker, 2010).

Procolobus badius at Taï are also rather clumsy leapers (Scott McGraw, pers. comm.). A red colobus monkey lands feet-first after a leap: “It then attempts to grasp onto a branch with its feet (often slipping off and only braking or slowing its falling body), while the hands and arms act as hooks on branches above the head to stop the downward descent as the individual impacts the now shaking and waving branches” (Gebo and Chapman,

1995, p. 64). If leaping style is correlated with fracture frequencies, it was predicted that red colobus monkeys, which engage in leaping behaviors more likely to result in a fall, would have higher fracture frequencies than guerezas. The findings of the present study compliment these behavioral data: Procolobus badius has the second highest fracture frequency of this sample while Colobus guereza has the third lowest frequency.

245 Pongo pygmaeus has the highest overall fracture frequencies within the current sample. Hylobates spp., the other suspensory primate examined here, also has relatively high fracture frequencies. Both Pongo pygmaeus and Hylobates spp. display fractures in all skeletal elements examined: however, there is a slight preference for lower limb fractures (especially the femur) in Hylobates spp. whereas there is a preference for upper limb fractures in Pongo pygmaeus (especially the humerus). The high frequency of fractures among gibbons has been attributed to falls occurring during brachiation

(Schultz, 1939, 1944). These data support that assertion, suggesting that falls during below-branch maneuvers may account for the high frequency of long bone fractures exhibited in gibbons and orangutans.

5.4 Impact of size/body mass on fracture frequencies

The hypothesis that primate taxa with larger average body masses exhibit higher fracture frequencies than those of smaller taxa is not borne out in this study when examining mass alone. Body size, independent of other variables, is not significantly correlated with overall fractures frequencies (r42 = 0.16660, P = 0.2797). Although larger primates are not more likely to break a long bone than smaller primates, when they do break a bone, there are some statistically significant tendencies for individual skeletal elements to covary with body mass. In general, larger primates are more likely to fracture the humerus, femur, or ulna whereas smaller primates are more likely to fracture

246 the tibia or fibula (r42 = 0.48436, P = 0.0009***; r42 = 0.54530, P = 0.0001***; r42 = -

0.43305, P = 0.0033***). However, these patterns may reflect the relationship of mass with other locomotor and habitat variables.

Species differences in body mass among primates contribute to positional behavior and musculoskeletal design (Garber, 2007). Body weight affects the manner in which primates face challenges within their habitats, constraining some solutions and facilitating others (Cant, 1992). For instance, orangutans cannot leap across gaps between trees, preferring to tree-sway (Cant, 1987). Based on comparisons of the locomotor behaviors of seven sympatric species in Surinam, Fleagle and Mittermeier

(1980) suggested that larger arboreal primates should leap less, climb and bridge more often, and engage in more frequent suspensory behavior than smaller primates. Large primates must either use large substrates or distribute their weight over a large area to supports their bodies (Cartmill and Milton, 1977). Suspension allows large animals to use small-diameter supports for feeding and traveling and extends their foraging radius at terminal branches (Thorpe and Crompton, 2006). It is more difficult for larger animals to remain on top of thin terminal branches, implying that suspensory behavior would be favored (Cant, 1992). However, it is more difficult for smaller animals to grasp and climb vertical supports (Cant, 1992). Consequently, the associations between fracture risk and positional behavior examined in this study are scaled for mass.

Size differences in bone also affect stress distribution (Radasch, 1999). Larger bones are likely to be stronger, stiffer, and more fracture resistant than smaller bones subjected to the same loads. Upon loading, internal forces are more widely distributed in larger bones, thereby reducing stress (Radasch, 1999). However, in the context of

247 fractures caused by falls, larger primates are likely to have more severe repercussions from falling than smaller primates, as they must dissipate greater amounts of kinetic energy caused by the fall.

5.5 Impact of intraspecific factors on fracture frequencies

Certain subsets of a population may be more prone to injury than others. I used the Cayo Santiago macaque population (Macaca mulatta) as a case study in order to address the possible impact various intraspecific factors may have on fracture frequencies among primate taxa in general. I tested three hypotheses. First, the hypothesis that fracture frequencies between males and females are not significantly different was

2 supported by the results of this study (χ 1 = 3.4313, P = 0.0640). Second, the hypothesis that younger macaques have higher fracture frequencies than older macaques was

2 rejected; the reverse was found (χ 4 = 61.6242, P = <0.0001***). Third, the hypothesis that fracture frequencies have decreased subsequent to improvements in managed care

2 was supported by the results of this study when excluding juveniles (χ 1 = 5.9197, P =

2 0.0150*), but not when examining all ages (χ 1 = 2.8405, P = 0.0919).

I hypothesized that juvenile primates would experience the highest fracture frequencies among age categories. Behavioral observations have shown that the amount of arboreal locomotion the Cayo Santiago macaques exhibit decreases with respect to age, after infancy (Dunbar, 1989). The most extensive morphological and behavioral

248 changes associated with locomotion occur in the juvenile period of macaque growth

(Wells and Turnquist, 2001). This is the time in which the greatest variety in locomotor behaviors is exhibited. Juveniles exploring their surroundings have bodies which are proportionate to adult bodies and a center of mass which is equivalent to that seen in adults. However, they have not yet reached the adult size and mass which would preclude certain maneuvers. Adults are much more sedentary and terrestrial. Infants are most commonly seen in association with their mothers, where they are protected from injury and fear. They are similar in locomotor behavior to adults (Wells and Turnquist,

2001). During my own observations of the Cayo Santiago macaques, juveniles appeared more daring in executing challenging locomotor maneuvers than adults. Consequently, I hypothesized that juveniles should exhibit higher fracture frequencies than infants or young, middle, or mature adults.

Counter to expectations, fracture frequencies in the Cayo Santiago macaque sample appear to be age-dependent. Fractures are much more common in adults than subadults and increase in frequency with each adult age grade (young, middle, and mature). My findings do not support the prediction that fracture frequencies would be highest in juveniles, due to their increased risk of falling, and lowest in infants, due to their protected status. However, it is important to note that fractures accumulate over the lifetime of the individual (Buikstra, 1975); consequently the age of occurrence of fractures which were not recent at the time of death is undetermined (Judd and Roberts,

1996). Bulstrode (1987) suggested that fracture frequencies in subadults are much greater than is commonly reported, and that fractures which occurred originally in juveniles constitute the bulk of well healed fractures in adults. Consequently, the

249 apparent association of fractures with age may be an artifact of superior angulation remodeling.

As hypothesized, fracture frequencies in males and females are not significantly different among the Cayo Santiago macaques. Macaques under three years old at the time of their deaths show no sex-based differences. Fractures are more common in middle adult males and in young and mature adult females. These data are consistent with the age-sex distribution of fracture frequencies in an older sample of Cayo Santiago macaques examined by Buikstra (1975).

I hypothesized that improvements in managed care at Cayo Santiago would result in decreased fracture frequencies over time. The extensive history of the Cayo Santiago macaques permits an examination of the effect of changes in managed care on fracture frequencies. The population at Cayo Santiago has had access to water in the form of rainwater collected via a catchment and cistern storage and dispersal system since C. R.

Carpenter shipped the original stock of 409 macaques from India in 1938 (Rawlings and

Kessler, 1986). Provisioning for the animals at Cayo Santiago was sporadic throughout the 1940s and 1950s. Financial support for the population dwindled, due to the completion of research grants and the United States involvement in World War II.

Animals were removed randomly for experimental use by various research facilities throughout the United States. By 1944, the population on the island was reduced to approximately 200 animals. Due to severe shortages of provisions and support, the animals were virtually abandoned; colony administrators at times used personal funds to prevent the animals from starving. Although monkeys attempted to swim to the mainland during the war years, by the mid-1950s they no longer attempted to do so. By 1955, only

250 115 monkeys were left, with evidence of malnutrition, wounds and injuries obtained from fighting, and cannibalism noted throughout the island. (Rawlings and Kessler, 1986)

In 1958, managed care of the colony was improved via regular provisioning with a prepared diet and the addition of a new cistern for water collection. A 16% annual population increase was recorded with the introduction of consistent provisioning, despite routine removal of animals for research purposes (Rawlings and Kessler, 1986). The population growth does not appear to have contributed to substantial increases in mortality rates during this time. However, by the mid-1960s, the growth of the colony was so great that it experienced population pressure. Consequently, the colony was culled in 1972, reducing the population to almost 200 animals representing four intact social troops. The cull included the removal and sacrifice of all of Group K, which was examined by Buikstra (1975). Since the 1972 population reduction, the colony has achieved a stable age distribution, a measure of the consistency of the colony management program (Rawlings and Kessler, 1986).

From 1972-1983, the colony consisted of a relatively intact and undisturbed population with a 13% annual growth rate. The colony was again culled in 1983, reducing the population to approximately 600 monkeys (about 50% of the colony).

Annual trapping and removal of some yearlings has served to maintain a stable colony population size since then. (Rawlings and Kessler, 1986) A tetanus inoculation program has been in effect since 1985 (Kessler et al., 2006). Primary immunizations of the tetanus toxoid are given to all yearlings and boosters given to all two year olds during the colony‟s annual trapping. Prior to the annual inoculations, tetanus was a major cause of death for the colony, contributing to 24.7% of deaths. Immediately after the

251 implementation of the immunization program, clinical tetanus infections were eliminated and the overall mortality rate of the colony was reduced by 42.2%. (Kessler et al., 2006)

Examination of the intestinal parasitic load of a subset of the population in 1984 revealed that the level of parasitism did not affect their overall clinical health, although half the examined macaques were infected with nematodes (File and Kessler, 1989). Periodic physical examinations, high birth rates, low total mortality rates, and low infant mortality rates all indicate that the population is healthy overall (File and Kessler, 1989; James

Ayala, pers. comm.). At the time of data collection, the summer of 2009, the colony at

Cayo Santiago consisted of approximately 1000 macaques, organized into several naturally formed social groups.

Since the natural island habitat itself has not changed drastically, it can be inferred that the majority of the statistically significant difference between the fracture frequencies in adults in the samples obtained prior to the 1972 cull (Buikstra, 1975) and subsequent to the cull (this study) can be explained by increased aggression. Macaques represented by the Pre-cull sample may have been involved in more group conflicts due to the neglect and marginal provisioning in the early history of the colony and due to increased population pressure as the colony later underwent rapid expansion after implementing constant provisioning. It is important to note, however, that there was little difference in mean annual mortality rates as a function of population size between the periods immediately preceding and succeeding the 1972 cull (Koford, 1965; Rawlings and Kessler, 1986). Rawlings and Kessler (1986) speculate that increases in population density are offset by greater access to resources due to provisioning. This suggests that,

252 although the Cayo Santiago macaques may have fought less as the population stabilized after the 1972 cull, this change did not affect survivorship significantly.

5.6 Linking behavior and morphology – Cayo Santiago case studies

With the exception of Jurmain (1989), there have been few attempts to attach life histories to pathological conditions observed in primate skeletons. Jurmain (1989) compared skeletal trauma in the well-documented Gombe chimpanzees (Pan troglodytes schweinfurthi) with events from each individual‟s life history recorded by Dr. Jane

Goodall. One difficulty with attempting these comparisons is that the consequences of injuries in wild primates rarely are included in the literature, although some examples of primates which have survived serious injuries have been recorded (Duckworth, 1911;

Schultz, 1956; Goodall, 1986; Crockett and Pope, 1988; Munn, 2006; Setchell et al.,

2006). The case studies from Cayo Santiago included in this dissertation in Appendix C represent an attempt to understand the pattern of involvement of fractures as one aspect of life history as well as a possible determinate of the timing of fracture repair.

There are several limitations to this particular set of case studies. First, this is an extremely small sample. Less than 13% of Macaca mulatta exhibit one or more long bone fractures, narrowing the sample size from 484 down to 62 individuals.

Additionally, census information was restricted to an approximately ten year time span

(1989-2000), further narrowing the sample down to 33 individuals. Since macaques live

253 over 20 years and, occasionally, over 30 years, only one generation is represented here.

Of the 33 individuals with fractures living within the census time span, only 6 fractures were able to be matched with an injury to the same anatomical region as recorded in the census reports.

It is highly likely that fractures are more prevalent than behavioral data alone would suggest. Furthermore, it is likely that many fractures are less debilitating than examination of the skeleton alone would suggest. Matching skeletal manifestations of injury with behavioral accounts of injuries observed in the wild is problematic. None of the primates included here actually were observed at the time of the injury. Furthermore, fractures occurring as a result of falls are likely to be missed by researchers in the field

(Crockett and Pope, 1988; Arlet, et al., 2009). Of the fractures submitted to be matched with behavioral observations, in only one case did Edgar Davila specifically describe the injury he observed in vivo as a broken bone. The severity of injuries may be obscured, especially in quadrupedal primates with three other limbs available to assist in support and propulsion. For instance, I was able to obtain some anecdotal information about one of the macaques whose injuries pre-dated the window of census data that was available to me. CSFS #735 (CPRC 1584) was an eleven year old male with poorly healed old tibial and fibular fractures exhibiting extensive remodeling and ankylosis of the left stifle

(knee) joint (Figure 5.1). It is believed that these injuries occurred during a mating fight with another male, at which time he caught his foot under a rock and was jumped on by the other male. He freed his foot then fought back successfully. When the researcher who observed the fight was shown the primate‟s skeleton upon its death years later, the

254 researcher was shocked and said that the monkey only had limped a little (Terry Kensler and Donald Dunbar, pers. comm.).

Figure 5.1 Fractures and ankylosis of stifle joint in rhesus macaque (CSFS #735) observed to ‘limp a little’. CPRC 1584 in lateral and posterior (inset) views.

255 5.7 Implications for primate evolution

Field observations of primates falling from heights and skeletal studies of the frequency and patterning of fractures among primates underscore the importance of falls as a selective pressure shaping primate anatomy (Pontzer and Wrangham, 2004). Male red colobus monkeys at Kibale have been known to fall 20-25 meters and survive

(Struhsaker, 2010). Goodall (1986) observed Gombe chimpanzees falling 51 times during a two year period (1978-1979); slightly over a third of these falls covered distances over ten meters. At least two primates obtained mortal injuries from falls: a middle-aged male broke his neck upon landing on rocks after a limb failed to support him and a two year old infant died from injuries sustained after he was blown from a 14 meter tall palm during strong winds (Goodall, 1986). Injuries sustained during such falls have been suggested to be the most frequent cause of long bone trauma among nonhuman primates (Buikstra, 1975; Lovell, 1991; Jurmain, 1997; Carter, et al, 2008). Not only has this study identified such injuries among primates, but also it has highlighted the association between the frequency and patterning of fractures and locomotor behaviors, habitat use, and body mass in primates. The question is, are these injuries severe enough to impact reproductive selection? If they are, then primates should be under strong selection to manifest mechanisms that prevent falls from occurring in the first place.

Several scenarios present themselves to compartmentalize the impact of injury (in this case, fractures) on reproductive success among primates. First, an injured primate may be past its reproductive years. Second, an injured primate may not have reached the

256 age of reproduction or at the time of the injury is capable of reproducing. However, this primate dies immediately, dies as a consequence of its injuries, or the injury results in its inability to reproduce. Third, an injured primate is or will be become capable of reproducing and the injury does not directly affect its reproductive success. However, the injury may still impact survival and reproduction indirectly. Each of these three scenarios will be examined in greater detail in the following paragraphs.

First, if an injured primate is post-reproductive, the injury obviously has no impact on evolution from the standpoint of its own reproductive success. However, the consequences of the injury may impact the reproductive success of the group as a whole, such as by holding back the entire group during travelling or by putting the group in increased danger from predators. Such circumstances appear to be rare events, as primates do not often care for injured conspecifics (Goodall; 1986; Silk 1992). It is important to note that fractures accumulate over the lifetime of the individual. Using fracture frequencies observed among the Cayo Santiago rhesus macaques in this study as an example, although 30% of recorded fractures are found in macaques over 20 years old, it is highly likely that at least some of these fractures actually occurred when they were younger. Additionally, macaques are reproductive from 3 to 4 years old until well into their 20s (Grynpas et al., 2000). Consequently, the majority of fractures in primates likely occur when the affected individuals are of reproductive age.

Since the majority of fractures appear to affect reproductively viable individuals, the second scenario, that an injured reproductive-aged primate does not survive its injury or is rendered unable to reproduce as a consequence of its injury, holds more validity than the first. Under this scenario, reproductive success will be impacted directly. However,

257 injuries consisting of long bone fractures are unlikely also to involve reproductive organs.

Falls from heights have been known to result in the immediate or eventual death of the individual, as described above, but more comprehensive field studies are required to determine just how often falls prove fatal. Furthermore, it is likely that both falls and injuries resulting in fractures are under-reported in the literature, based on the case studies from Cayo Santiago described in this study, in which only a small portion of fractures observed in skeletal remains could be matched to behavioral accounts of injuries observed in the field.

Although it is uncertain just how often falls result in the death of an individual, it is likely, based on the quantity of healed fractures examined in this study, that most primates who receive fractures from falls do survive the injury. Consequently, the third scenario, that the reproductive success of a reproductive-aged primate is not directly impacted by its injury, is most likely. However, numerous indirect consequences may contribute to a reduction in reproductive success in injured primates. So, the next question appears to be, just how much do fractures indirectly affect reproductive success under these conditions?

Lovell (1991) speculated that the reproductive success of an injured individual could be diminished through loss of rank, which has been observed among injured male baboons (Harding, 1980; Drews, 1996). Injured primates also may lose or suffer reductions in reproductive success due to a loss of or reduction in mobility. Because fractures in weight-bearing long bones are detrimental to locomotor function (Ulstrup,

2008), injured primates may be required to use modified forms of locomotor patterns or avoid some patterns entirely (Munn, 2006). For instance, injured chimpanzees have been

258 shown to suffer balance problems when travelling arboreally and be unable to perform certain locomotor maneuvers (Munn, 2006). Chimpanzees with limb deformities have been known to be unable to keep up with travelling groups (Goodall, 1986). Thus injuries have the potential to result in additional, possibly fatal falls, the use of more energy to maneuver around obstacles instead of using a preferred form of locomotion, and the increased likelihood of encountering predators outside of the protection of conspecifics. These increased dangers may be dependent upon locomotor anatomy. For instance, a leaper with a broken hind limb or a brachiator with a broken fore limb will have more difficulties maneuvering in the trees than a generalized quadruped with a single limb injury who can limp using three limbs more easily. Primates with injuries which restrict locomotion also may have limited or no access to food items, expending additional energy when obtaining food or foraging with impaired climbing abilities

(Drews, 1996). Wounded primates may be unable to access the terminal branch niche to cross gaps, to avoid predators, or to obtain food sources (Brain, 1992). Injured female primates have been reported to find it more difficult to carry infants or to carry them less

(Munn, 2006), thereby affecting reproductive success of the group as a whole. Any injuries to female primates also may impact their dependent offspring. Females may be unable to feed or care for infants due to their own lack of health. Consequently, it appears that even injuries which do not directly affect reproductive success do have potentially significant incidental impacts on reproduction.

Adaptations that decrease injury risk or provide compensatory measures for loss of movement if injuries occur thus may have played a significant role in primate evolution (Ripley, 1967; Munn, 2006). For instance, Drews (1996) suggests that the

259 potential costs of injury likely have wielded strong selective pressures in male baboons resulting in the evolution of massive canines and behavioral adaptations for avoiding conflict escalation. The possibility that risk avoidance has shaped arboreal climbing adaptations has been discussed above (Pontzer and Wrangham, 2004; Thorpe and

Crompton, 2006). In order to avoid the risk of falling, primates have adapted to a range of locomotor and positional behaviors, including distributing their body mass over several substrates, lowering their center of gravity by flexing and abducting their limbs, and adopting more suspensory postures during feeding (Garber, 2007). This study analyzes the frequency and patterning of fractures among primates, which in future research may uncover potential areas in which individual primate taxa are most vulnerable to fractures and consequently are most liable to be affected by them from an evolutionary standpoint.

Different locomotor modes present distinct mechanical demands on the primate skeleton (Fleagle, 1999). Some positional behaviors inherently involve more biomechanical stresses on the skeleton than others; in general, however, those behaviors with which a primate is most well-adapted should require less muscle activity and contribute less stress to bones (Thorpe and Crompton, 2006). Natural selection may act upon primate musculoskeletal design to limit the biomechanical stressors impacting bone in proportion to the frequency with which common locomotor behaviors are performed

(Hunt, 1991b). Nevertheless, the results of this study suggest that adaptations towards particular locomotor behaviors appear to contribute to the patterning of fractures among primates. For instance, the extremely long fore limbs of suspensory primates assist locomotion through extended bimanual stride length, foraging through climbing

260 efficiency, and feeding through increased reach (Hollihn, 1984; Fleagle, 1999). The fore limbs of catarrhine primates tend to be scaled positively allometrically with size; however, Hylobates spp. and Pongo pygmaeus have arms elongated even beyond this trend (Hollihn, 1984). However, when suspensory primates break a bone, it tends to be either the humerus or the femur. The humerus may be fractured preferentially in

Hylobates spp. because the excess stresses placed upon it during brachiation make it the most likely to break when a gibbon falls. On the other hand, Pongo pygmaeus is more likely to fracture its femur. Pongo pygmaeus relies less on orthograde suspensory locomotion than does Hylobates spp. and is the only ape to exhibit pronograde suspensory behaviors (Thorpe and Crompton, 2006). Its reliance on both above- and below-branch suspensory behaviors to access the fine branch niche may contribute to its higher frequency of femoral fractures.

When leaping and climbing primates break bones, they tend either to involve the clavicle preferentially or show no preference for location. Galago senegalensis is an exception, predominantly featuring tibial and fibular fractures. Perhaps the increased frequency of hind limb fractures in Galago senegalensis is explained by the excess stresses placed on it during vertical clinging and leaping, so that, when the bushbaby does fall, the tibia and fibula are least able of all the long bones to handle the additional stresses caused by the impact of the fall itself. Leapers experience a greater proportion of propulsive musculature in the hind limbs compared to generalized quadrupeds (Demes et al., 1998). Extremely long hind limbs maximize propulsive force by increasing the duration of time needed to accelerate and thus produce momentum for the leap (Lawler,

2008). Frequent leapers of similar size have been shown to have longer, stronger, and

261 more rigid femora and tibiae than infrequent leapers, due to the greater forces experienced in frequent leaping (Terranova, 1995; Connour, et al., 2000). Consequently,

Propithecus verreauxi and Eulemur fulvus, who both leap more frequently than Galago senegalensis, should have even higher frequencies of hind limb fractures than the bushbaby. They do not. However, this may be an artifact of the small sample size available for prosimians in general. The Propithecus verreauxi sample only includes one fracture. The fracture patterning likely would change with an expanded sample.

Generalized arboreal quadrupeds also have adapted numerous morphological and behavioral mechanisms in order to meet the challenge of maintaining stability and balance to avoiding falling (Cant, 1992). From a behavioral standpoint, arboreal quadrupedal primates and other arboreal mammals mitigate loading forces and center of mass displacements acting on the substrate by increasing joint excursion and the duration of contact with substrates when walking and by employing longer and less frequent strides (Young, 2009). From a morphological standpoint, arboreal quadrupeds maintain adhesion to substrates with grasping hands and feet of moderate length and maintain a low and flat center of mass with fore limbs and hind limbs of similar, relatively short length (Fleagle, 1999). Often, they have long tails that serve both as a counterbalance and stabilizing force, counteracting disruptive pitching and rolling movements (Larson and Stern, 2006). On the other hand, terrestrial quadrupeds maintain a narrow, deep trunk and long, similar length limbs designed for speed, as well as joints which facilitate more extended limb postures (Fleagle, 1999). Generally, arboreal quadrupeds have more robust limb bones than terrestrial primates, reflecting the need to cope with the challenges of walking in a three-dimensional space (Nakatsukasa, 1996).

262 These adaptations suggest that there should be distinct differences in fracture frequency and patterning among predominantly quadrupedal primates based on degree of arboreality. As discussed above, fracture frequencies are not correlated with degree of arboreality, aside from a tendency for completely arboreal primates (predominantly quadrupedal or otherwise) to exhibit high fracture frequencies. However, smaller arboreal quadrupeds, including Cebus apella, Saimiri boliviensis, Leontopithecus rosalia, and Microcebus murinus, most often experience tibial and fibular fractures. The most likely bones to break among the remaining arboreal quadrupeds and the terrestrial quadrupeds tend to involve any long bone except for the tibia and fibula. Macaca mulatta is the only exception, tending to exhibit fractures of the fibula. Papio spp.,

Macaca fascicularis, and Pan troglodytes tend to fracture their ulna. Colobus guereza,

Mandrillus sphinx, and Chlorocebus pygerythrus tend to fracture their clavicle. Gorilla gorilla and Alouatta seniculus preferentially fracture their humerus or femur. Procolobus badius shows no preference in fracture location. The tendency for smaller arboreal quadrupeds to fracture their tibia or fibula may be related to the load the hind limbs must bear. For instance, squirrel monkeys (Saimiri boliviensis) support most of their weight on their hind limbs (Schmidt, 2005b).

263 5.8 Future research

Future directions for this study will include expanding the current sample of nonhuman primates. Prosimians especially may have been under-represented. A larger sample of primates commonly practicing suspensory behaviors also should prove helpful.

Furthermore, a detailed assessment of intraspecific factors would bolster the conclusions reached here. Addressing the impact of social dominance hierarchy on locomotor and positional behavior may reveal variations in fracture risk. For instance, Macaca fascicularis mothers have been found to show variations in canopy usage based upon dominance rank (Vos et al., 1992). It is important to examine more closely sex differences in locomotor and habitat use preferences, especially in those taxa in which fracture frequencies were dependent upon sex. Significantly higher fracture frequencies in male Procolobus badius at Taï Forest may be related to the greater tendency for males to fall from trees during fights with other males (Struhsaker, 2010). These sex differences also may reflect the decreased likelihood that females would be found in open areas exposed to aerial predators (Field and McGraw, 2001). At present, further research into locomotor and habitat use preferences specifically targeted towards identifying potential sex-specific variations in positional behavior is limited by the lack of such data in the primatological literature.

Comparing fracture frequencies in humans as well as nonhuman primates may offer insights into the origins of bipedalism as well as common pathological conditions in humans. Chimpanzees might be more likely to practice bipedalism if they suffer from

264 upper body or arm injuries, including snare wounds or amputations. Goodall (1986) observed that Faben, a chimpanzee at Gombe, often walked bipedally after he developed polio, which paralyzed his arm. However, observations of a group of highly bipedal chimpanzees at Bwindi with few such wounds suggest that many other factors contribute to bipedal behaviors (Stanford, 2006). In addition, postcranial trauma in humans may be influenced by our unique mode of locomotion and lack of arboreality compared to other primates (Jurmain and Kilgore, 2005). Due to practicing habitual bipedality, humans are at increased risk for osteoporotic fracture of the hip and forearms and are the only species susceptible to spontaneous fractures (Grynpas, et al., 2000).

Continuing the present research may provide information regarding the use of nonhuman primates as animal models for skeletal maintenance and repair in humans.

Primates may heal with fewer repercussions than do humans. This supposition is corroborated by the scarcity of degenerative joint disease and complete lack of osteophytosis in chimpanzees (Jurmain, 1989), and rarity of osteoarthritis secondary to fracture in macaques (Nakai, 2003). However, degenerative joint disease has been reported frequently in baboons, gibbons, orangutans, and gorillas as well as less frequently in other catarrhines (Schultz, 1956). Chimpanzee and orangutan fractures consolidate almost perfectly, with much less callus formation and deformity than in humans with similar fractures (Lovell, 1991). Infection secondary to fracture is rare in nonhuman primates (Schultz, 1956). Nonhuman primates who contract infection consequent to fracture may be more likely to perish before skeletal manifestations develop than humans with similar injuries who have time for the infection to appear on the skeleton, thereby giving the appearance that nonhuman primates are healthier.

265 Nevertheless, recent clinical trials investigating the utility of using bone morphogenetic proteins to accelerate fracture healing have not been as successful in humans as they were in nonhuman primate models (Bishop and Einhorn, 2007; Giannoudis et al., 2007).

This research also provides a step toward determining the origins of medical treatment practices in early humans. Palaeopathological analysis of severe physical impairments has been used to debate the degree to which Neanderthals may have provided care or medical treatment for conspecifics (Rowlett and Schneider 1971;

Trinkaus and Zimmerman 1982; Lebel and Trinkaus 2002). These studies suggest that certain individuals were cared for because they could not have survived for as long as they had without some form of assistance from others. However, in each of these cases, the veracity of the authors‟ claims has been disputed (Tappen 1985; Dettwyler 1991), in some instances using nonhuman primate skeletal assemblages and behavioral observations in living primates as models for populations without access to medical treatment techniques (Silk 1992; DeGusta 2003). Similarly, Schultz (1956) has cited examples of well-healed fractures in a wild gibbon skeletal population to urge caution in suggesting a link between the presence of well healed fractures and the availability of medical treatment in archaeological populations. The knowledge of factors involved in fracture healing and mechanisms behind the distribution of fractures which have healed under natural conditions will provide essential data contributing to the search for the origins of medical intervention.

266 5.9 Chapter summary

Based on results of this study, commonly expressed locomotor behaviors and habitat preferences appear to contribute to the frequency and patterning of fractures among nonhuman primates. The primary source of long bone trauma among nonhuman primates is likely falls related to locomotor mode preference, although mass, arboreality, and height above ground utilization also contribute to fracture frequencies. The examination of fracture frequencies helps to underscore the importance of falls as a selective pressure shaping primate anatomy. Intraspecific factors, including sex, age, and shifting ecologies, also may impact fracture frequencies, although they are unlikely to significantly affect the ranks of frequencies between taxonomic groups. In future studies, fracture patterns may be used to address other intraspecific factors, including rank and aggressive interactions. Additionally, the current sample may be expanded to include a more comprehensive selection of prosimians as well as fossil hominids and humans.

267

CHAPTER 6: Conclusions

The purpose of this study is to test the thesis that locomotor and habitat preferences are associated with the location and prevalence of fractures in nonhuman primates. Long bones (clavicles, humeri, radii, ulnae, femora, tibiae, and fibulae) from twenty-two taxonomic groups representing ten families across the primate order were analyzed using macroscopic and radiographic techniques. Fracture prevalence rates for all seven elements for each taxonomic group were obtained. These frequencies then were subjected to a principal components analysis of compositional data to reduce the cloud of data points into component scores for comparative purposes.

Locomotor and habitat profiles for each taxonomic group were developed based upon quantitative field observations in the primatological literature. The degree of arboreality for each taxon was determined by averaging the percentages of time spent off the ground from multiple published accounts. The height above ground profile for each taxon was developed from frequencies at which each taxon spent in five meter increments along a vertical dimension. A PCA of compositional data was run using these frequencies, resulting in component scores used in later analyses. The locomotor profile for each taxon was created based upon the frequency each group was observed practicing common locomotor behaviors (quadrupedalism and bipedalism, climbing, leaping and bridging, and suspension and dropping). As with the height above ground data, scores

268 from a PCA of compositional data were developed from the locomotor mode data.

Published accounts provided the average body mass for each taxonomic group.

Most fractures healed fairly well, with minimal deformity and few complications.

Saguinus oedipus (5.63%) exhibited the lowest frequency of fractures whereas Pongo pygmaeus (29.79%) and Procolobus badius (27.69%) exhibited the highest frequencies.

The most commonly fractured element when comparing fracture frequencies of all elements in all taxa is the fibula in Leontopithecus rosalia (7.04%) and Cebus apella

(6.62%). The fibula also is the most commonly fractured element when combining all examined taxa (2.61%). The least fractured element overall is the tibia at 0.73%. Taxa differ in fracture frequencies, skeletal elements affected, and types of fractures received.

However, a multiple correspondence analysis reveals clustering among the dataset, including associations between transverse fractures and fractured ulnae; oblique fractures and fractured fibulae; spiral and miscellaneous other fracture types and humeral, tibial, and femoral fractures; and fractures of the clavicle and radius.

Several hypotheses were formed to test associations between fracture frequencies and locomotor and habit preferences. Locomotor mode preference was the only factor to be significantly correlated with overall fracture frequencies when examined

2 independently of other factors (χ 2 = 0.6317, P = <0.0001). However, fracture frequencies per element were significantly correlated with specific aspects of each positional profile. As expected, suspensory primates exhibited the highest fracture frequencies; in contrast, leapers exhibited the lowest fracture frequencies, probably because the primates in the sample which leaped most often also tended to be small.

269 The results of principle components analyses suggest that fracture patterns are most closely associated with locomotor mode, followed by arboreality, vertical distribution, and body mass, although each of these variables are interconnected. Five major associations between fracture frequencies and positional behaviors are revealed:

1. When Suspensory primates break a bone, it tends to be either the humerus or femur.

2. Small/Medium Arboreal Quadrupeds → tibia or fibula

3. Large Arboreal Quadrupeds → long bones other than the tibia or fibula

4. Terrestrial Quadrupeds → long bones other than the tibia or fibula

5. Climbing/Leaping primates → clavicle or no preference for location

Fractures are not distributed randomly within a population; frequencies may vary with age, sex, and changes in population pressures over time. Although the males and females of four of the taxonomic groups examined here had statistically different levels of fracture frequencies, the fracture prevalence rates of most species were not significantly sex specific. Fractures appear to be age dependent; however, because fractures accumulate over the lifetime of the individual, it is difficult to determine if fractures occurred prior to adulthood unless the fracture affected the growth plate.

Changes in managed care over time at Cayo Santiago have resulted in decreased fracture frequencies in adults subsequent to regular provisioning of the colony.

Fractures were matched with behavioral observations of injuries in only five individuals at Cayo Santiago. Only one of these case studies was mentioned specifically in the unpublished census records to have broken a bone. Successfully assessing the

270 timing of fracture occurrence using this method appears to be sporadic at best. These data suggest not only that fractures are likely under-reported in field studies but also that their capacity to impede mobility is over-estimated in morphological studies.

Comprehensive analyses of fracture healing in nonhuman primates are critical to reaching a greater understanding of the ways in which trauma has contributed to human and primate evolution, behavior, and survival. Exploring how locomotor behavior and habitat use covary with bone fracture frequencies among nonhuman primates may provide information on selective pressures underlying evolution, including risk avoidance and morphological adaptation to injury. Furthermore, evaluation of fracture patterns in wild primate skeletal series rather than in humans provides baseline data regarding the healing of injuries under natural conditions, an often overlooked component of research aimed at assessing the role of medical intervention in human history.

271

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294

APPENDIX A: SCORING CRITERIA FOR DATA COLLECTION

(PID#) Personal identification number for this project

Demographics

(M) Museum: 0 = OSU 1 = Cleveland Museum of Natural History 2 = American Museum of Natural History 3 = National Museum of Natural History (Smithsonian Institution) 4 = Caribbean Primate Research Center

(Cat #) Museum Catalog number

(G) Genus: 1 = Gorilla 2 = Hylobates 3 = Pongo 4 = Pan 5 = Papio 6 = Aotus 9 = Cebus 13 = Chlorocebus 14 = Colobus 17 = Galago 21 = Eulemur 22 = Leontopithecus 25 = Macaca 26 = Microcebus 29 = Otolemur 33 = Propithecus 34 = Saguinus 35 = Saimiri 41 = Alouatta 42 = Mandrillus 43 = Procolobus

295 (Sp) Species/subspecies: 1 = gorilla 2 = lar 3 = agilis 4 = concolor 6 = pygmaeus 7 = troglodytes 8 = hamadryas 9 = senegalensis 20 = guereza 22 = fulvus 24 = moholi 29 = rosalia 32 = fascicularis 36 = murinus 47 = oedipus 55 = apella 56 = boliviensis 57 = seniculus 59 = verreauxi 60 = sphinx 62 = hoolock 63 = pygerythrus 64 = lemurinus 65 = crassicaudatus 66 = anubis 68 = klossi 69 = moloch 70 = mulatta 71 = badius

(I) Skeletal Inventory: 1 = fragmentary (-50%) 2 = partial (50-90%) 3 = complete (90%+)

(S) Sex: 1 = male 2 = female 3 = male? 4 = female? 5 = indeterminate

296 (A) Age: Age of the individual, based on available museum records. 1 = infant 2 = juvenile 3 = young adult 4 = mature adult 5 = subadult nonspecific 6 = adult nonspecific

(AI) Acquisition Information: Geographic location where the individual was acquired, based on available museum records. 1 = Cameroon – Ebolwa 2 = Abong Mbong, French Cameroons 3 = Abong Mbong – Djaspoten 4 = Thailand (North) – Champee, Changmai 5 = Sumatra 6 = Borneo 7 = Sumatra – Pontianak 8 = No Data / Locality unknown 9 = Congo District (West Africa) (Tag: Central African Congo) 10 = Ethiopia 11 = Ethiopia (South) 12 = Ecuador 13 = Brazil – British Guiana 14 = Africa (East) 15 = Madagascar 16 = Palau Islands 17 = Peru – Loreto: Rio Samiria: Yana yaquillo 18 = Bolivia – (ca 4 km below Santa Cruz) 19 = Bolivia – Federal Gavea 20 = Bolivia – R Tabujos Linizal Ulalla 21 = Bolivia – Goyas Anapolis 22 = Bolivia – Matto Grosso Maracaju 23 = Bolivia – Santa Cruz -- Chapane River 24 = Bolivia – Dept. Beni -- opp Cuscaid 25 = Bolivia – Dept. Beni -- opp Cuscajal 26 = Bolivia – Dept. Beni (27 km from mouth of Ibare River) 27 = Bolivia – Dept. Beni Rio Manare (coordinates 12 26 5) 28 = Bolivia – Dept. Beni Sankorenzo (Itenez river mouth) 29 = Bolivia – Dept. Beni Seven Island Rapids (1946 Expedition) 30 = Mexico – Oaxaca Tapanatepec 31 = Columbia – Cacaquelito (HH Smith #1285) 32 = Columbia – Calavasa 33 = Columbia – Magdalena Bonda (HH Smith #244)

297 34 = Bolivia – Beni (Ibare river mouth) (DE Anez #0240, #0242) 35 = Bolivia – Dept. Cochabarnba (27 km NE Chimore river mouth) (Alferdo Ximenez #2998) 36 = Trinidad – Biche TRVL 37 = Madagascar – NE Ambatondradama 38 = Madagascar – Amboasary 39 = Zaire – Avakubi (#2476 Lang and Chapin) 40 = Cameroons – 6 mi N of Cuanbo; 27 km E of Kribi 41 = Cameroon – Bafia 42 = Bafuka 43 = India – Assamchangchang Peni (#43) 44 = India – Dhappa 45 = Kenya – Charangunyalate Hills 46 = Botswana – Seronga 47 = Mozambique – Mamica and Sofala: Avezole Lima Camp 48 = Columbia – North Coastal region 49 = No locality (New England Animal Exchange) 50 = Kenya – Nyanza Prov. Mahoroni (4200 ft) 51 = South Africa – Magoebaskloof Tzaneen Arsiberstein (10 mi W) 52 = Tanzania – Manyara Mbulu, Mto Wa Mbu 53 = Columbia – Baranquilla (Rec.d from NE Primates, RW Thorington, Middleton, MA) 54 = Columbia – Northern (Dr. Powers NIH Bldg 5) 55 = Locality unknown (Rec.d from Walter Reed Army Institute for Research) 56 = Locality unknown (Rec.d from NE Primates, RW Thorington, Middleton, MA)) 57 = Locality unknown (Oregon RDC -- 088-963) 58 = Locality unknown (Rec.d from RUSH, Medical Center, Dr. Deinhardt) 59 = Mozambique – Tete District, Vila Caldes Xaviers, HJ Hebert 60 = Rhodesia – Manocaland, Vmali Dist, Helvtia farm, SW Goussard 61 = Uganda – Toro Province, Bwamba (2500 ft alt) 62 = Kenya – MaNarok (Site A), RE Kuntz PMP547 63 = Kenya – Lake Naivasha (Loring JA 261) 64 = Kenya – Rift Valley Prov -- Marigot, 7 mi SE of Lake Beringo, Kuntz and Moore, 681-33 65 = Kenya – coord. 1 49 S, 36 5 E, RE Kuntz PMP362 66 = Kenya – 90 mi SW of Nairobi (RE Kuntz 515) 67 = Kenya – RE Kuntz (884) 68 = Borneo (Indonesia) – Batu Jurong, WL Abbott 5981 69 = Sumatra (Indonesia) – Mentawai Islands (Pagai), WL Abbott 2033 70 = Myanmar – Tanintharyi, Tanjonj Badak, WL Abbott 805 71 = Java (Indonesia) – Mount Salak, 3000 ft, O Bryant Palmer 277 72 = Borneo (Indonesia) – Sempang River, WL Abbott 5367 73 = Borneo (Indonesia) – Sempang River, Sungei Matan, WL Abbott 74 = Borneo (Indonesia) – Sungei Matan 75 = Borneo (Indonesia) – Kendawangan River, Upper Parui (6095)

298 76 = Borneo (Indonesia) – Kendawangan River, Lanchut (6097, 6106) 77 = Borneo (Malaysia) – Sabah, Jesselton, RE Kuntz (FM 1765 / PF / 9561 / 6295) 78 = Cayo Santiago 80 = Liberia (west of Cavally River) 81 = Taï Forest, Ivory Coast

Location

(M) Multiple fractures present: Whether there are any other long bone fractures present in the individual in addition to the scrutinized specimen. 1 = no (the individual exhibits only one long bone fracture) 2 = bilateral (the specimen and the contralateral element both have fractures, e.g. both humeri) 3 = there are three or more long bone fractures present 4 = off-side (the specimen and an element on the other side of the body that is not the contralateral element both have fractures, e.g. the left humerus and the right ulna) 5 = same-side (the specimen and an element that is on the same side of the body both have fractures, e.g., the left humerus and the left ulna)

(E) Element: 1 = clavicle 2 = humerus 3 = radius 4 = ulna 5 = femur 6 = tibia 7 = fibula

(S) Side: 1 = left 2 = right

(L) Location: 1 = proximal third 2 = middle third 3 = distal third

(R) Region affected: 1 = surgical neck 2 = anatomical neck 3 = head 4 = intercondylar 5 = condylar 6 = other epiphysis

299 7 = metaphysis 8 = diaphysis 9 = joint surface 10 = other (explain)

Pathological Condition

(T) Type of fracture: 1 = transverse 2 = spiral 3 = oblique 4 = comminuted 5 = greenstick 6 = partial 7 = avulsion 8 = impacted 9 = other (compressed, hairline)

(A) Associated Trauma: 1= none 2 = gunshot 3 = bite wound 4 = cutting/piercing wound

(I) Infection: 1 = none 2 = periostitis (minor) 3 = periostitis (severe) 4 = osteomyelitis (minor) 5 = osteomyelitis (severe)

(H) Degree of Healing: 1 = well-healed 2 = healing 3 = little healing 4 = nonunion 5 = poor healing

300 Measurements

(L) Left: measurement of the left element in millimeters, taken from digital calipers.

(R) Right: measurement of the right element in millimeters, taken from digital calipers.

(PD) PD: percent difference between left and right elements, based on the longer element. Formula used: (larger element – smaller element) / larger element.

Radiograph Data

(T) Revised Fracture Type, based on radiographic analysis: This determination is used in the final analyses, not the fracture type determination based on macroscopic analysis. 1 = transverse 2 = spiral 3 = oblique 4 = comminuted 5 = greenstick 6 = partial 7 = avulsion 8 = impacted 9 = other (compressed, hairline)

(Ap) Apposition: Degree to which the bone ends are apposed. 1 = complete (100% apposition indicates that both bone ends have unified with 100% of their surface area) 2 = partial 3 = absent (0% apposition indicates that none of the original fractured bone ends have healed together) 4 = not applicable (used for non-union fractures)

(Al) Alignment: The angle of displacement of the fractured bone from the normal bone line. The direction of angulation is determined based on the direction of the distal bone fragment (e.g., anterior means that the distal fragment is angled anterior to the normal bone line). 1 = none (no angulation) 2 = anterior 3 = posterior 4 = medial 5 = lateral 6 = clavicle anterior 7 = clavicle posterior 8 = clavicle superior

301 9 = clavicle inferior 10 = mixed (lack of alignment in two directions – see M1 and M2 columns for both directions) 11 = not applicable (used for non-union fractures)

(S) Sclerosis of bone ends: 1 = absent 2 = present

(M1 and M2) Mixed: Clarification of #10 = mixed in column Al = alignment. Indicates which two directions in which there is a lack of alignment. 1 = none 2 = anterior 3 = posterior 4 = medial 5 = lateral 6 = clavicle anterior 7 = clavicle posterior 8 = clavicle superior 9 = clavicle inferior 10 = mixed 11 = not applicable

(AAD) Age-at-death: The age-at-death of the Cayo Santiago macaques, based on census records.

302

APPENDIX B: RAW DATA

Demographics Location Pathology Measurements Radiograph Data PID M Cat # G Sp I S A AI M E S L R T A I C H L R O T Ap Al C S M1 M2 AAD 6 1 HTB 1752 1 1 3 2 6 1 5 6 1 2 8 2 1 1 3 1 231 280 0.175 3 3 3 2 2 7 1 HTB 1752 1 1 3 2 6 1 5 7 1 2 8 3 1 1 2 1 208 244 0.148 3 3 3 2 2 8 1 HTB 1730 1 1 3 1 6 1 5 6 2 2 8 8 1 5 4 5 308 277 0.101 1 2 10 2 2 3 4 9 1 HTB 1730 1 1 3 1 6 1 5 7 2 3 8 8 1 5 4 5 279 228 0.183 1 1 1 2 2 10 1 HTB 1736 1 1 3 1 6 1 4 2 1 2 8 2 1 1 1 4 NA 432 2 4 11 1 2

303 11 1 HTB 1736 1 1 3 1 6 1 4 5 2 2 8 2 1 5 2 4 369 NA 2 4 11 2 2 17 1 HTB 2821 1 1 3 1 6 2 1 2 1 2 8 4 1 5 3 1 453 430 0.051 4 2 5 2 2 18 1 HTB 2739 1 1 3 1 6 2 1 1 2 1 8 3 1 1 1 1 146 160 0.088 8 4 11 1 1 20 1 HTB 1996 1 1 3 2 6 2 1 3 1 2 8 6 1 1 1 1 308 305 0.010 6 1 1 2 2 21 1 HTB 2000 1 1 3 1 6 2 1 3 1 2 8 6 4 2 2 2 368 368 0.000 6 1 1 2 1 22 1 HTB 1991 1 1 3 1 6 2 1 1 1 3 8 8 1 1 1 1 185 173 0.065 5 2 1 1 2 23 1 HTB 1994 1 1 3 1 6 2 1 2 2 2 8 2 1 4 4 1 422 407 0.036 2 1 1 2 2 24 1 HTB 3878 2 2 3 1 6 4 5 6 1 2 8 3 1 1 1 1 154.77 170.19 0.091 3 2 10 2 2 3 5 25 1 HTB 3878 2 2 3 1 6 4 5 7 1 2 8 5 1 1 1 1 144.18 161.80 0.109 4 1 10 2 2 3 5 27 1 HTB 3886 2 2 3 1 6 4 1 4 1 2 8 1 1 5 4 2 291.48 291.89 0.001 1 1 1 2 1 28 1 HTB 3884 2 2 3 1 6 4 1 2 1 2 8 1 1 5 4 5 NA NA 1 3 5 2 1 29 1 HTB 3881 2 2 3 1 6 4 1 2 2 2 8 6 1 1 1 1 246.91 257.30 0.040 3 2 4 2 2 30 1 HTB 3888 2 2 3 1 6 4 1 5 2 2 8 6 1 1 1 1 198.17 200.34 0.011 5 1 1 2 1 303 Demographics Location Pathology Measurements Radiograph Data PID M Cat # G Sp I S A AI M E S L R T A I C H L R O T Ap Al C S M1 M2 AAD 34 1 HTB 3899 2 2 3 4 6 4 4 3 1 2 8 1 1 1 2 1 264.49 263.50 0.004 1 1 1 2 2 35 1 HTB 3899 2 2 3 4 6 4 4 1 2 2 8 3 1 1 1 1 94.48 90.33 0.044 1 2 8 1 1 36 1 HTB 3903 2 2 3 4 6 4 1 2 1 2 8 3 1 1 2 1 241.16 245.26 0.017 3 1 1 2 1 37 1 HTB 3904 2 2 3 4 6 4 5 5 2 1 8 3 1 1 1 1 194.33 164.63 0.153 3 3 3 2 2 38 1 HTB 3904 2 2 3 4 6 4 5 7 2 1 8 1 1 1 3 1 161.04 158.34 0.017 1 2 4 2 2 39 1 HTB 1030 3 6 3 2 6 7 1 3 1 2 8 9 1 2 1 2 333 336 0.009 6 1 1 1 2 40 1 HTB 1023 2 3 3 1 6 5 1 4 2 2 8 3 1 1 1 1 NA NA 3 2 1 2 2 41 1 HTB 2040X 4 7 3 3 6 1 1 7 2 2 8 3 1 1 3 1 NA 226 1 1 5 2 1 43 1 HTB 2040Y 4 7 3 3 6 1 1 3 1 3 7 1 1 1 2 2 301 299 0.007 8 4 11 2 2 44 1 HTB 2040Z 4 7 3 3 6 1 5 6 1 1 8 1 1 1 2 1 271 NA 1 2 5 2 2 45 1 HTB 2040Z 4 7 3 3 6 1 5 7 1 2 8 3 1 1 3 1 220 NA 2 3 5 2 2 46 1 HTB 2072 4 7 3 1 6 1 1 4 1 2 8 3 1 1 4 1 313 309 0.013 1 1 4 2 2 47 1 HTB 1721 4 7 3 2 6 1 1 1 1 2 8 2 1 1 1 1 110 122 0.098 5 1 1 1 1 49 1 HTB 1748 4 7 3 2 6 1 1 2 2 3 8 8 1 1 2 1 280 268 0.043 8 4 11 2 2

304 50 1 HTB 1768 4 7 3 3 6 1 1 4 2 3 8 1 1 1 4 1 326 324 0.006 3 1 4 2 1

52 1 HTB 2026 4 7 3 1 6 1 1 6 1 2 8 6 4 2 1 2 262 262 0.000 6 4 11 2 1 53 1 HTB 1770 4 7 3 2 6 1 1 3 1 1 7 2 1 1 2 1 254 248 0.024 3 1 1 2 1 54 1 HTB 1853 4 7 3 2 6 1 1 4 1 2 8 3 1 1 1 1 290 300 0.033 4 4 11 2 1 55 1 HTB 1880 4 7 3 2 6 1 1 4 2 2 8 2 1 1 1 1 301 303 0.007 2 3 1 2 1 56 1 HTB 1882 4 7 3 1 6 1 5 4 2 2 8 3 1 1 2 1 300 301 0.003 6 4 11 2 1 57 1 HTB 1882 4 7 3 1 6 1 5 3 2 2 8 3 1 1 3 1 282 282 0.000 3 1 1 2 1 58 1 HTB 1775 4 7 3 2 6 2 4 1 1 3 8 3 1 1 1 5 141 145 0.028 7 3 6 2 2 59 1 HTB 1775 4 7 3 2 6 2 4 2 2 2 8 3 1 1 4 1 328 314 0.043 2 2 4 2 2 60 1 HTB 2823 4 7 3 2 6 2 1 4 1 2 8 1 1 1 3 1 272 267 0.018 1 1 1 2 1 61 1 HTB 1027 5 8 3 2 6 11 1 4 1 1 10 7 1 2 1 5 200.67 196.68 0.020 7 4 11 2 2 62 1 HTB 1043 5 8 3 3 6 11 1 3 2 2 8 1 1 1 2 1 215.66 218.43 0.013 1 1 1 2 1 304 Demographics Location Pathology Measurements Radiograph Data PID M Cat # G Sp I S A AI M E S L R T A I C H L R O T Ap Al C S M1 M2 AAD 63 1 HTB 1028 5 8 3 2 6 11 1 6 2 1 6 7 1 1 1 1 179.81 178.33 0.008 7 4 11 1 2 64 1 HTB 1503 5 8 3 2 6 10 5 3 2 1 3 1 1 1 1 5 186.24 187.58 0.007 1 3 1 2 2 65 1 HTB 1503 5 8 3 2 6 10 5 4 2 1 3 6 1 1 1 5 197.20 199.85 0.013 8 1 1 2 2 66 1 HTB 1212 5 66 3 1 6 9 1 4 1 2 8 1 1 1 3 1 223.14 NA 1 1 1 2 1 69 1 HTB 1799 1 1 3 5 1 1 5 2 1 3 4 6 1 1 1 2 193.28 192.80 0.002 6 4 11 1 2 70 1 HTB 1799 1 1 3 5 1 1 5 3 1 1 8 3 1 1 2 2 141.94 156.90 0.095 3 4 11 2 2 73 1 HTB 1044 13 63 3 3 6 8 5 3 1 1 8 3 1 1 1 1 127.11 132.69 0.042 5 1 1 2 1 74 1 HTB 1044 13 63 3 3 6 8 5 4 1 1 8 1 1 1 1 1 141.13 147.54 0.043 5 1 5 2 1 75 1 HTB 1166 14 20 3 1 6 14 1 7 2 1 8 3 1 1 2 1 174.56 173.18 0.008 3 1 5 2 1 76 1 HTB 0138 21 22 3 5 6 8 1 4 1 1 8 1 1 1 2 1 98.56 99.18 0.006 2 1 4 2 2 83 1 HTB 1424 1 1 3 4 2 1 1 5 2 3 8 4 2 4 1 3 NA NA 8 4 11 1 1 84 1 HTB 1845 1 1 3 3 2 1 3 5 2 3 8 3 1 1 2 1 288 286 0.007 1 2 2 2 2 87 1 HTB 3540 4 7 3 3 2 3 1 1 2 1 8 3 1 1 1 1 83.28 83.27 0.000 1 2 1 2 2 88 1 HTB 0172 3 6 3 3 6 6 5 3 1 3 8 3 1 1 3 5 332 349 0.049 3 3 1 2 2

305 89 1 HTB 0172 3 6 3 3 6 6 5 4 1 3 8 3 1 1 3 5 346 368 0.060 1 3 5 2 2

90 1 HTB 1443 3 6 3 2 2 5 1 1 2 1 8 3 1 1 1 1 153 138 0.098 3 2 6 2 2 91 1 HTB 1444 3 6 3 1 2 5 1 1 2 3 8 2 1 1 1 1 203 186 0.084 5 1 6 1 2 101 0 12 group X 25 32 3 1 6 16 1 4 2 3 8 3 1 4 3 1 119.40 133.20 0.104 1 2 1 2 2 102 0 9 group G 25 32 3 1 5 16 1 6 2 3 6 8 1 4 1 1 NA NA 8 4 11 2 1 103 0 55 group D 25 32 3 1 6 16 1 4 2 1 6 7 1 1 1 4 NA 129.27 7 4 11 2 2 104 0 40 group Z 25 32 3 1 6 16 1 2 1 2 8 3 1 5 4 1 107.65 131.26 0.180 3 2 5 2 2 106 0 17 group A 25 32 3 1 6 16 1 5 1 1 2 1 1 1 1 1 141.01 140.50 0.004 8 4 11 1 2 107 0 94-14 43 71 3 1 6 80 3 2 2 1 8 1 1 1 2 1 152 145 0.046 1 2 2 1 2 108 0 94-14 43 71 3 1 6 80 3 4 2 1 8 8 2 1 1 1 163 156 0.043 1 2 1 2 2 109 0 94-14 43 71 3 1 6 80 3 3 2 2 8 3 1 1 2 1 151 149 0.013 3 2 10 2 2 3 4 110 0 94-14 43 71 3 1 6 80 3 1 2 1 8 3 1 1 1 1 56 58 0.034 1 3 7 1 2 305 Demographics Location Pathology Measurements Radiograph Data PID M Cat # G Sp I S A AI M E S L R T A I C H L R O T Ap Al C S M1 M2 AAD 111 0 94-32 43 71 3 1 6 81 5 6 2 3 8 1 1 3 3 5 NA 144 1 2 2 2 2 112 0 94-32 43 71 3 1 6 81 5 7 2 3 8 1 1 3 3 5 NA 133 1 3 10 2 2 4 2 113 0 22-58 43 71 3 1 6 81 5 2 1 3 8 3 1 1 3 1 159 168 0.054 2 2 2 2 2 114 0 22-58 43 71 3 1 6 81 5 4 1 2 8 3 1 1 3 1 178 177 0.006 1 3 1 2 2 115 0 22-9 43 71 3 1 6 81 5 6 1 2 8 1 1 1 2 5 106 154 0.312 3 3 10 2 2 3 5 116 0 22-9 43 71 3 1 6 81 5 7 1 2 8 1 1 1 2 5 NA 142 3 3 10 2 2 3 5 117 0 22-3 43 71 3 1 6 81 1 7 2 1 8 1 1 1 2 1 158 157 0.006 3 2 10 1 2 5 3 118 0 10-11 43 71 3 2 6 81 1 1 2 2 8 1 1 1 1 1 57 53 0.070 2 3 1 2 2 119 0 2101 43 71 3 1 6 81 3 5 2 1 8 1 1 2 4 1 178 156 0.124 1 3 10 2 1 2 5 120 0 2101 43 71 3 1 6 81 3 6 2 1 8 1 1 2 3 1 NA 156 2 3 5 2 2 121 0 2101 43 71 3 1 6 81 3 7 2 1 8 1 1 2 3 1 NA 143 2 1 4 2 2 122 0 2011 43 71 3 1 6 81 2 1 2 2 8 1 1 1 2 1 156 150 0.038 1 3 6 2 2 123 0 2011 43 71 3 1 6 81 2 1 1 2 8 1 1 1 2 1 156 150 0.038 1 2 1 2 2 124 0 22-58 43 71 3 1 6 81 5 4 1 3 8 3 1 1 2 1 178 177 0.006 1 2 3 2 2

306 201 2 188038 9 55 3 2 6 17 1 4 2 1 8 3 1 1 2 1 110.24 109.27 0.009 1 1 1 2 1

202 2 188046 9 55 3 2 6 17 1 5 1 1 8 3 1 1 2 1 114.96 120.88 0.049 3 1 5 2 1 203 2 188045 9 55 3 2 6 17 1 7 2 1 8 3 1 1 2 1 103.40 103.13 0.003 3 1 1 2 1 204 2 188047 9 55 3 1 6 17 2 7 1 3 8 3 1 4 1 1 118.41 118.45 0.000 3 1 2 2 2 205 2 188047 9 55 3 1 6 17 2 7 2 3 8 9 1 4 1 1 118.41 118.45 0.000 3 1 2 2 2 206 2 188030 9 55 3 2 6 17 5 1 1 1 8 3 1 1 1 1 39.46 43.94 0.102 8 1 1 2 2 207 2 188030 9 55 3 2 6 17 5 7 1 3 8 2 1 1 1 1 104.99 105.72 0.007 2 1 1 2 2 208 2 188035 9 55 3 1 6 17 1 5 1 1 8 4 1 1 3 1 125.39 132.72 0.055 3 1 2 2 2 210 2 210392 9 55 3 5 5 18 5 6 1 3 8 1 1 1 1 1 98.63 99.51 0.009 3 2 3 1 2 211 2 210392 9 55 3 5 5 18 1 7 1 3 8 1 1 1 1 1 92.68 93.52 0.009 3 2 3 1 2 212 2 133614 9 55 3 1 5 19 1 2 2 1 8 2 1 1 2 1 98.18 NA 3 2 10 2 1 4 3 214 2 133638 9 55 3 1 6 21 1 7 1 3 8 3 1 2 1 2 113.24 NA 2 1 5 2 1 306 Demographics Location Pathology Measurements Radiograph Data PID M Cat # G Sp I S A AI M E S L R T A I C H L R O T Ap Al C S M1 M2 AAD 215 2 133642 9 55 3 1 6 21 1 4 1 2 8 1 1 1 2 1 111.03 NA 1 1 1 2 1 216 2 133659 9 55 3 1 6 21 1 4 1 3 8 1 1 1 4 1 98.73 NA 3 1 1 2 1 217 2 133658 9 55 3 1 6 21 1 7 1 3 8 3 1 1 2 1 120.28 NA 1 3 10 2 2 4 3 218 2 133651 9 55 3 1 2 21 1 2 2 2 8 5 1 1 1 3 NA NA 5 1 4 1 1 219 2 133664 9 55 3 1 5 21 1 4 1 3 8 1 1 1 3 1 97.18 NA 1 2 1 2 1 220 2 133666 9 55 3 2 6 21 1 5 2 2 8 3 1 1 3 1 NA 113.68 3 2 2 2 2 221 2 133671 9 55 3 2 6 21 1 2 2 3 8 2 1 1 2 1 NA 92.80 8 2 1 2 2 222 2 133677 9 55 3 2 6 21 1 5 1 2 8 3 1 1 2 1 115.38 126.82 0.090 2 3 10 2 2 2 5 223 2 133815 9 55 3 1 6 21 1 3 1 1 8 1 1 1 1 1 105.02 106.47 0.014 8 1 3 1 2 224 2 133806 9 55 3 2 6 21 3 5 1 2 8 3 1 4 3 1 109.57 124.29 0.118 3 2 2 2 2 225 2 133806 9 55 3 2 6 21 3 3 1 2 8 3 1 1 2 1 89.41 93.01 0.039 3 1 1 2 1 226 2 133806 9 55 3 2 6 21 3 7 1 2 8 1 1 1 3 1 109.39 110.17 0.007 3 1 1 2 2 227 2 133637 9 55 3 1 6 22 1 7 2 1 8 1 1 1 3 1 107.84 108.17 0.003 8 1 3 2 2 228 2 211642 35 56 3 1 5 23 1 4 1 2 8 3 1 1 1 1 65.24 65.08 0.002 1 2 1 2 2

307 229 2 211601 35 56 3 1 6 24 1 4 2 3 8 9 1 1 1 1 75.90 74.42 0.019 1 3 1 2 2

230 2 211599 35 56 3 1 5 25 1 7 1 1 8 5 1 1 1 1 82.59 82.26 0.004 5 1 3 1 1 231 2 211606 35 56 3 2 6 26 1 7 2 2 8 1 1 1 2 1 81.32 81.61 0.004 1 2 2 2 2 232 2 211610 35 56 3 1 6 26 3 6 2 1 8 3 1 2 3 3 87.51 87.88 0.004 3 1 3 2 2 233 2 211610 35 56 3 1 6 26 3 7 2 1 8 1 1 1 2 4 80.91 NA 1 4 11 2 2 234 2 211610 35 56 3 1 6 26 3 6 1 1 8 3 1 1 2 1 87.51 87.88 0.004 5 1 10 1 2 3 5 235 2 211610 35 56 3 1 6 26 3 7 1 1 8 1 1 1 2 1 80.91 NA 3 1 3 2 2 236 2 211610 35 56 3 1 6 26 3 6 1 3 8 4 1 1 2 1 87.51 87.88 0.004 5 1 4 1 2 237 2 211610 35 56 3 1 6 26 3 7 1 3 8 1 1 1 2 1 80.91 NA 5 1 4 1 1 238 2 211610 35 56 3 1 6 26 3 1 2 2 8 1 1 1 2 1 30.85 30.56 0.009 3 1 1 2 1 239 2 211616 35 56 3 2 6 27 1 6 1 1 8 3 1 1 2 1 84.32 84.00 0.004 3 1 3 2 1 240 2 209930 35 56 3 1 6 28 1 5 2 2 8 2 1 1 2 1 88.76 84.88 0.044 2 2 4 2 2 307 Demographics Location Pathology Measurements Radiograph Data PID M Cat # G Sp I S A AI M E S L R T A I C H L R O T Ap Al C S M1 M2 AAD 241 2 209934 35 56 3 1 6 29 1 2 2 3 4 3 1 3 1 4 74.22 NA 3 4 11 2 2 243 2 23329 41 57 3 5 5 31 4 2 1 3 8 4 1 1 3 1 NA NA 4 3 10 2 2 4 2 245 2 23335 41 57 3 5 5 32 1 5 1 2 8 2 1 1 2 1 132.64 144.93 0.085 1 3 10 2 2 3 4 246 2 23355 41 57 3 2 6 33 1 7 1 1 8 3 1 1 3 1 129.51 NA 1 2 4 2 2 247 2 211534 41 57 3 2 5 34 1 5 1 2 8 3 1 1 3 1 121.48 125.99 0.036 5 1 3 2 1 248 2 211536 41 57 3 2 5 34 3 2 1 3 8 3 1 1 1 1 144.10 153.95 0.064 5 1 1 2 1 249 2 211536 41 57 3 2 5 34 3 5 1 2 8 1 1 1 1 1 166.56 164.51 0.012 3 1 3 2 1 250 2 211536 41 57 3 2 5 34 3 7 2 2 8 3 1 1 1 1 142.69 142.30 0.003 5 1 3 2 1 251 2 211540 41 57 3 2 6 35 1 5 2 1 8 4 1 4 3 5 145.17 128.11 0.118 1 3 4 2 2 252 2 235168 41 57 3 1 5 36 1 2 2 2 8 3 1 1 1 1 81.47 78.56 0.036 5 1 4 1 1 254 2 170728 21 22 3 2 6 37 1 1 2 2 8 1 1 1 1 1 31.70 30.71 0.031 1 1 6 1 2 255 2 170474 33 59 3 2 6 38 1 1 1 1 8 3 1 1 2 1 32.23 37.69 0.145 4 1 6 1 2 259 2 52206 14 20 3 1 6 39 4 3 2 2 8 2 1 2 2 1 161.91 153.08 0.055 1 3 5 2 2 260 2 52206 14 20 3 1 6 39 4 4 1 2 8 1 1 1 2 1 178.67 176.75 0.011 1 1 1 2 2

308 261 2 89365 42 60 3 2 6 40 1 1 2 2 8 3 1 1 1 1 53.77 47.32 0.120 1 3 9 2 2

262 2 170364 42 60 3 1 6 41 1 3 2 1 7 7 3 2 1 4 7 4 11 2 1 263 2 52676 5 8 3 1 5 42 1 2 2 3 8 2 2 1 3 2 NA 201.63 1 3 4 2 2 264 2 83414 2 62 3 1 5 43 2 3 1 3 8 5 1 1 1 3 NA NA 8 2 3 1 2 265 2 83414 2 62 3 1 5 43 2 4 1 3 8 5 1 1 1 3 NA NA 1 1 4 1 2 266 2 11092 2 62 3 2 6 44 1 4 2 2 8 5 1 1 1 1 5 1 1 1 1 267 2 60647 22 29 3 2 6 8 4 4 1 1 3 7 2 1 2 1 69.64 71.96 0.032 7 1 2 1 1 268 2 60647 22 29 3 2 6 8 4 5 2 1 8 3 1 3 4 5 70.16 60.37 0.140 3 3 5 2 2 269 2 174408 26 36 3 1 6 38 1 4 1 2 8 1 1 1 4 1 25.38 25.91 0.020 1 3 5 2 2 270 2 185628 26 36 3 1 6 38 1 1 1 2 8 9 1 1 4 1 10.02 10.86 0.077 3 3 1 2 2 271 2 185629 26 36 3 1 6 38 1 7 1 1 8 1 1 1 2 1 NA 31.97 1 1 1 2 1 272 2 34716 13 63 3 2 5 45 1 1 2 3 8 3 1 1 3 1 38.78 34.46 0.111 1 3 8 2 2 308 Demographics Location Pathology Measurements Radiograph Data PID M Cat # G Sp I S A AI M E S L R T A I C H L R O T Ap Al C S M1 M2 AAD 273 2 169430 13 63 3 1 6 46 1 1 1 3 8 3 1 1 2 1 NA NA 3 3 8 2 2 274 2 216252 13 63 3 2 6 47 5 6 2 2 8 3 1 1 1 1 136.02 128.70 0.054 3 2 10 2 2 3 5 275 2 216252 13 63 3 2 6 47 5 7 2 2 8 6 1 1 1 1 128.57 117.84 0.083 1 1 3 2 1 301 3 501091 34 47 3 2 6 48 1 4 1 2 8 3 1 1 2 1 54.80 54.75 0.001 3 1 2 2 2 302 3 501106 34 47 3 2 6 48 1 3 1 2 8 3 1 1 1 1 47.45 47.23 0.005 3 1 3 2 1 303 3 501111 34 47 3 5 6 48 1 7 1 2 8 4 1 1 3 4 64.19 N/A 1 3 1 2 1 304 3 501089 34 47 3 1 6 48 1 5 2 3 5 7 1 1 1 5 69.24 68.83 0.006 7 4 4 1 1 305 3 397875 17 9 3 2 6 8 1 7 2 1 8 1 1 1 1 1 58.32 57.69 0.011 1 2 3 2 1 306 3 397967 17 9 3 1 6 49 5 5 2 3 8 3 1 1 4 2 60.08 54.32 0.096 3 3 10 2 2 5 2 307 3 397967 17 9 3 1 6 49 5 7 2 1 8 1 1 1 2 1 53.14 51.70 0.027 1 1 1 2 1 309 3 382455 13 63 3 2 5 51 1 1 1 2 8 5 1 1 1 1 30.09 35.85 0.161 1 3 10 2 2 4 9 310 3 452607 13 63 3 1 6 52 1 5 1 3 8 3 1 1 1 1 131.82 150.09 0.122 5 1 4 1 2 311 3 588161 22 29 3 5 5 8 1 7 1 2 8 5 1 1 1 1 55.59 55.39 0.004 3 1 10 2 1 4 3 312 3 588171 22 29 3 2 6 8 1 7 1 1 8 1 1 1 4 2 69.27 69.81 0.008 1 1 10 2 2 3 5

309 314 3 588170 22 29 3 2 6 8 5 6 2 1 8 2 1 1 4 5 74.74 70.50 0.057 3 3 10 2 2 3 4

315 3 588170 22 29 3 2 6 8 5 7 2 1 8 2 1 1 2 4 70.63 N/A 2 4 11 2 2 316 3 589086 22 29 3 5 6 8 1 7 2 2 8 2 1 1 1 1 N/A 70.72 4 1 10 1 1 4 2 317 3 588172 22 29 3 2 6 8 5 6 1 3 8 8 1 1 1 1 62.51 76.25 0.180 5 1 4 1 2 318 3 588172 22 29 3 2 6 8 5 7 1 2 8 4 1 1 1 1 64.35 72.32 0.110 4 1 4 1 1 319 3 396746 6 64 3 1 6 53 1 2 2 2 8 4 1 1 4 5 68.99 57.69 0.164 4 3 4 2 1 321 3 396444 6 64 3 5 6 54 1 1 2 2 8 1 1 1 2 1 28.25 25.61 0.093 1 3 7 2 2 322 3 396503 6 64 3 2 6 54 2 1 2 2 8 1 1 1 2 1 29.07 N/A 1 2 10 2 2 7 9 324 3 396613 6 64 3 1 5 55 1 4 1 1 8 6 1 1 2 1 66.73 70.09 0.048 1 1 1 2 2 325 3 396683 6 64 3 2 6 55 1 7 1 1 8 1 1 1 1 1 85.26 85.69 0.005 3 1 5 2 2 326 3 396685 6 64 3 1 5 55 1 1 1 2 8 1 1 1 2 4 N/A 25.74 1 4 11 2 2 327 3 396688 6 64 3 1 6 56 1 7 1 1 8 1 1 1 3 2 97.1 97.32 0.002 1 1 1 2 2 309 Demographics Location Pathology Measurements Radiograph Data PID M Cat # G Sp I S A AI M E S L R T A I C H L R O T Ap Al C S M1 M2 AAD 328 3 396697 6 64 3 5 6 56 5 4 1 3 8 1 1 1 2 1 64.48 63.82 0.010 8 1 1 2 2 329 3 396697 6 64 3 5 6 56 5 3 1 3 8 1 1 1 1 1 53.06 55.72 0.048 8 2 1 1 1 330 3 396698 6 64 3 2 6 53 5 3 2 3 8 3 1 1 2 1 63.76 60.68 0.048 5 1 2 1 2 331 3 396698 6 64 3 2 6 53 5 4 2 3 8 8 1 1 1 1 72.23 71.15 0.015 8 1 4 1 2 332 3 396708 6 64 3 2 5 53 1 4 1 3 8 8 1 1 2 1 66.85 66.65 0.003 3 2 1 1 2 333 3 396709 6 64 3 1 6 53 1 5 2 2 8 3 1 1 3 1 87.45 82.74 0.054 2 3 10 2 1 3 5 334 3 396717 6 64 3 2 6 53 5 6 1 2 8 3 1 1 2 1 84.55 89.52 0.056 4 3 10 2 2 3 5 335 3 396717 6 64 3 2 6 53 5 7 1 3 8 1 1 1 3 1 78.39 84.50 0.072 1 3 10 2 1 3 5 337 3 542484 21 22 3 2 6 57 1 5 1 1 3 6 1 1 1 2 124.11 124.41 0.002 6 4 11 1 1 338 3 399057 29 65 3 5 6 58 4 5 1 2 8 3 1 1 1 1 82.38 89.42 0.079 3 2 2 2 2 339 3 399057 29 65 3 5 6 58 4 1 2 2 8 3 1 1 1 1 24.72 23.13 0.064 3 1 7 1 1 340 3 399059 29 65 3 1 6 8 1 1 2 2 8 5 1 1 1 1 25.91 24.65 0.049 5 1 7 1 1 341 3 399063 29 65 3 1 6 8 1 1 2 2 8 3 1 1 1 1 28.57 26.28 0.080 5 1 10 1 1 7 8 342 3 399667 29 65 3 1 6 58 1 3 1 1 8 7 1 1 1 5 N/A N/A 7 4 11 1 2

310 343 3 365714 29 65 3 1 6 59 1 7 2 3 8 3 1 1 1 1 83.49 82.89 0.007 3 1 10 1 1 3 5

344 3 425417 29 65 3 1 6 60 1 4 1 2 8 3 1 1 2 1 81.72 N/A 3 1 3 2 1 345 3 397990 29 65 3 1 6 8 1 7 1 1 8 3 1 1 2 2 81.05 82.85 0.022 3 3 1 2 2 346 3 452622 14 20 3 1 6 61 1 1 2 2 8 3 1 1 1 1 67.18 64.28 0.043 1 1 1 2 2 347 3 464983 14 20 3 2 6 8 1 1 2 2 8 3 1 1 1 1 55.37 50.98 0.079 2 1 10 2 2 7 8 348 3 384228 5 66 3 2 6 62 1 4 1 2 8 3 1 1 3 1 234 235 0.004 3 1 5 1 1 349 3 162899 5 66 3 1 6 63 1 3 2 2 8 3 4 5 3 5 243 236 0.029 1 2 10 2 2 5 2 350 3 395435 5 66 3 1 6 64 1 1 1 2 8 1 1 2 1 1 61.49 63.74 0.035 3 1 1 2 1 351 3 397476 5 66 3 2 6 65 1 4 2 1 8 3 1 1 2 1 222 220 0.009 2 2 5 2 2 354 3 354988 5 66 3 1 6 66 5 3 2 2 8 1 1 1 3 2 238 N/A 1 3 1 2 2 355 3 354988 5 66 3 1 6 66 5 4 2 2 8 1 1 1 3 2 262 262 0.000 1 2 4 2 1 356 3 354996 5 66 3 5 2 67 1 7 1 1 8 5 1 1 1 1 76.16 76.81 0.008 1 1 10 2 2 5 3 310 Demographics Location Pathology Measurements Radiograph Data PID M Cat # G Sp I S A AI M E S L R T A I C H L R O T Ap Al C S M1 M2 AAD 357 3 153796 2 67 3 1 6 68 1 5 1 2 8 3 1 1 2 1 198 198 0.000 3 2 10 1 1 5 2 358 3 121679 2 68 3 2 6 69 1 5 1 2 8 3 1 1 1 1 179 N/A 2 2 1 1 2 359 3 111970 2 2 3 1 6 70 1 5 2 2 8 3 1 4 4 2 N/A 205 3 3 2 2 2 360 3 154722 2 69 3 1 6 71 5 6 1 3 8 5 1 1 1 1 173.44 N/A 3 1 10 1 2 3 5 361 3 154722 2 69 3 1 6 71 5 7 1 3 8 5 1 1 1 1 N/A 156.65 5 1 10 1 1 3 5 362 3 145300 3 6 3 2 6 72 1 2 2 2 8 3 1 1 2 1 315 329 0.043 3 1 3 2 2 363 3 145304 3 6 3 1 6 73 1 6 2 2 8 6 1 1 2 1 N/A 254 6 1 1 2 1 364 3 145305 3 6 3 1 6 73 1 2 2 2 8 4 1 1 3 1 367 376 0.024 6 1 3 2 2 365 3 145308 3 6 3 2 6 73 5 2 1 3 8 8 1 1 1 5 329 336 0.021 8 4 11 2 1 366 3 145308 3 6 3 2 6 73 5 4 1 1 8 8 1 1 2 5 341 353 0.034 8 4 11 2 1 367 3 145310 3 6 3 1 6 74 1 2 1 3 8 3 1 1 4 5 351 347 0.011 3 3 3 2 2 368 3 153821 3 6 3 2 6 75 1 7 1 2 8 3 1 1 1 1 200 N/A 5 1 3 1 1 370 3 153823 3 6 3 1 6 76 1 5 1 1 8 5 1 1 1 1 304 N/A 5 1 5 1 1 371 3 317197 3 6 3 1 6 77 1 1 2 2 8 4 1 1 1 1 59.83 57.39 0.041 2 1 2 2 2

311 372 3 396503 6 64 3 2 6 77 2 1 1 2 8 3 1 1 1 1 29.07 N/A 1 1 9 2 2

401 4 3865 25 70 3 2 5 78 5 3 2 3 8 5 1 1 1 3 N/A N/A 5 1 3 1 1 01.203 402 4 3865 25 70 3 2 5 78 5 4 2 3 8 5 1 1 1 3 N/A N/A 5 2 4 1 1 01.203 403 4 3909 25 70 3 2 6 78 1 7 1 3 8 2 1 3 1 4 N/A 178.95 2 4 11 1 1 14.877 405 4 3912 25 70 3 2 6 78 1 4 1 3 8 3 1 1 2 1 149.42 151.90 0.016 1 1 10 2 1 3 5 20.044 406 4 3916 25 70 3 1 6 78 4 7 1 1 8 3 1 1 2 1 173.38 172.84 0.003 3 1 1 2 2 22.074 407 4 3916 25 70 3 1 6 78 4 1 2 1 8 3 1 1 1 1 62.16 56.86 0.085 3 2 9 1 2 22.074 408 4 3925 25 70 3 2 6 78 5 3 2 1 8 3 1 1 1 4 136.37 N/A 3 4 11 2 2 05.041 409 4 3925 25 70 3 2 6 78 5 4 2 2 8 1 1 1 2 1 149.28 150.98 0.011 1 1 10 2 2 5 2 05.041 410 4 3928 25 70 3 1 6 78 1 7 2 1 8 3 1 1 2 1 166.17 163.65 0.015 3 2 1 2 2 18.430 411 4 3931 25 70 3 2 5 78 5 6 1 3 8 8 1 1 3 1 148.89 150.54 0.011 8 1 10 2 1 17.425 412 4 3931 25 70 3 2 5 78 5 7 1 3 8 3 1 1 2 4 107.33 140.52 0.236 3 4 11 2 1 17.425 311 Demographics Location Pathology Measurements Radiograph Data PID M Cat # G Sp I S A AI M E S L R T A I C H L R O T Ap Al C S M1 M2 AAD 413 4 3984 25 70 3 1 6 78 1 7 2 3 8 1 1 1 1 1 168.76 166.47 0.014 1 2 1 1 1 19.438 414 4 3915 25 70 3 1 6 78 3 7 1 2 8 1 1 1 2 1 159.98 160.82 0.005 1 2 3 2 2 19.795 415 4 3915 25 70 3 1 6 78 3 3 1 2 8 1 1 3 1 4 N/A 158.65 1 4 11 1 1 19.795 416 4 3915 25 70 3 1 6 78 3 4 1 2 8 1 1 3 1 4 N/A 173.19 1 4 11 1 1 19.795 417 4 3913 25 70 3 2 6 78 1 1 1 3 8 7 1 1 1 4 41.54 47.61 0.127 3 4 11 2 1 23.485 418 4 4004 25 70 3 2 6 78 1 1 2 2 8 3 1 1 2 1 52.43 45.51 0.132 3 3 9 2 1 12.753 419 4 4174 25 70 3 1 6 78 2 7 1 2 8 3 1 1 2 1 170.81 169.64 0.007 3 1 1 2 1 13.715 420 4 4174 25 70 3 1 6 78 2 7 2 2 8 3 1 1 1 1 170.81 169.64 0.007 3 1 1 2 1 13.715 421 4 4181 25 70 3 2 6 78 1 7 2 3 8 1 1 1 2 1 150.95 148.13 0.019 3 2 1 2 2 28.948 422 4 4188 25 70 3 1 6 78 3 1 1 2 8 1 1 1 1 1 56.54 57.20 0.012 1 3 1 2 1 15.370 423 4 4188 25 70 3 1 6 78 3 1 2 1 8 3 1 1 2 1 56.54 57.20 0.012 3 2 3 2 2 15.370 424 4 4188 25 70 3 1 6 78 3 7 1 3 8 1 1 1 1 4 N/A 170.28 1 4 11 1 1 15.370 425 4 4235 25 70 3 1 6 78 1 4 1 3 8 1 1 1 2 1 160.53 161.58 0.006 1 1 1 2 1 11.496 426 4 4292 25 70 3 2 6 78 1 4 1 1 8 4 1 1 2 1 155.98 156.11 0.001 1 2 10 2 1 4 3 17.501

312 427 4 4316 25 70 3 2 6 78 1 4 1 3 8 3 1 1 2 1 156.93 162.37 0.034 3 2 4 2 1 23.403

428 4 3603 25 70 3 2 6 78 1 4 2 3 8 6 1 1 2 1 158.24 157.54 0.004 1 1 1 2 2 09.718 429 4 3632 25 70 3 2 5 78 1 7 2 2 8 1 1 1 2 1 N/A N/A 1 1 3 2 1 06.268 430 4 3635 25 70 3 2 5 78 1 7 2 2 8 1 1 1 1 4 N/A 141.60 1 4 11 1 1 07.088 431 4 3715 25 70 3 1 5 78 5 3 2 3 8 5 1 2 1 2 N/A N/A 5 1 2 1 2 00.573 432 4 3715 25 70 3 1 5 78 5 4 2 3 8 5 1 2 1 2 N/A N/A 5 1 5 1 1 00.573 433 4 3287 25 70 3 1 6 78 1 5 2 3 4 7 3 1 1 1 180.18 162.79 0.097 7 2 1 1 2 13.332 434 4 3289 25 70 3 2 6 78 1 4 2 2 8 1 1 1 2 1 158.50 155.95 0.016 3 1 10 2 1 4 3 21.986 435 4 3300 25 70 3 2 6 78 1 7 1 1 8 1 1 1 2 2 138.71 140.59 0.013 1 1 10 2 2 3 5 07.030 436 4 3307 25 70 3 2 6 78 3 4 1 1 8 1 1 1 3 1 150.28 154.87 0.030 1 2 3 2 2 31.444 437 4 3307 25 70 3 2 6 78 3 7 1 1 8 1 1 1 2 1 147.70 147.44 0.002 1 1 1 2 2 31.444 438 4 3307 25 70 3 2 6 78 3 7 1 3 8 1 1 1 3 1 147.70 147.44 0.002 1 3 5 2 2 31.444 312 Demographics Location Pathology Measurements Radiograph Data PID M Cat # G Sp I S A AI M E S L R T A I C H L R O T Ap Al C S M1 M2 AAD 439 4 3307 25 70 3 2 6 78 3 7 2 1 8 1 1 1 1 1 147.70 147.44 0.002 1 3 1 2 2 31.444 440 4 3316 25 70 3 2 6 78 1 4 1 3 8 1 1 1 3 1 155.66 153.67 0.013 1 2 1 2 1 18.523 441 4 3324 25 70 3 2 6 78 1 4 1 2 8 1 1 1 2 1 157.68 163.63 0.036 1 2 1 2 1 19.490 442 4 3342 25 70 3 2 6 78 1 7 1 1 8 1 1 4 2 4 N/A 141.59 1 4 11 2 1 15.083 443 4 3372 25 70 3 2 6 78 1 7 1 1 8 1 1 4 1 4 N/A 163.51 1 4 11 2 2 02.279 444 4 3393 25 70 3 2 6 78 2 7 1 3 8 1 1 1 2 1 151.97 150.52 0.010 1 1 2 2 2 19.940 445 4 3393 25 70 3 2 6 78 2 7 2 3 8 1 1 1 4 1 151.97 150.52 0.010 1 2 1 2 2 19.940 446 4 3539 25 70 3 2 6 78 1 1 2 2 8 1 1 5 2 1 51.19 49.82 0.027 1 1 10 2 1 6 9 09.068 447 4 1584 25 70 3 1 6 78 5 6 1 2 8 1 1 1 4 5 149.33 170.83 0.126 1 3 5 2 1 11.173 448 4 1584 25 70 3 1 6 78 5 7 1 2 8 1 1 1 4 5 131.40 157.65 0.167 1 3 4 2 1 11.173 450 4 2028 25 70 3 1 5 78 1 1 2 2 8 5 1 1 1 1 36.09 35.40 0.019 1 2 1 1 1 01.562 451 4 2038 25 70 3 1 6 78 1 4 2 3 8 1 1 1 2 1 173.78 175.15 0.008 3 2 10 2 2 3 4 33.753 452 4 2104 25 70 3 1 6 78 1 7 2 3 8 1 1 1 2 1 151.66 151.99 0.002 1 2 10 2 1 3 5 05.118 453 4 2967 25 70 3 2 6 78 3 3 1 3 8 1 1 1 3 1 120.14 126.69 0.052 1 2 10 2 1 5 2 21.964

313 454 4 2967 25 70 3 2 6 78 3 4 1 3 8 1 1 1 3 1 141.30 143.46 0.015 1 3 2 2 2 21.964

455 4 2967 25 70 3 2 6 78 3 2 1 3 8 1 1 1 3 1 132.15 139.67 0.054 1 1 4 2 1 21.964 456 4 2971 25 70 3 1 6 78 4 4 1 3 8 1 1 1 2 1 169.20 170.95 0.010 1 2 3 2 2 29.118 457 4 2971 25 70 3 1 6 78 4 7 2 1 8 1 1 1 1 1 164.33 162.21 0.013 3 3 10 2 2 5 3 29.118 458 4 3007 25 70 3 2 6 78 1 7 1 3 8 4 1 2 2 4 N/A 154.75 4 4 11 2 2 20.115 459 4 3017 25 70 3 2 6 78 1 4 1 3 8 1 1 3 1 4 N/A 155.09 1 4 11 1 2 10.595 460 4 3027 25 70 3 2 6 78 1 4 2 3 8 1 1 1 2 1 148.84 148.09 0.005 1 2 3 2 2 08.581 461 4 0782 25 70 3 1 6 78 4 1 1 3 8 1 1 1 1 4 N/A 65.70 1 4 11 1 2 22.644 462 4 0782 25 70 3 1 6 78 4 7 2 2 8 1 1 1 2 1 179.26 178.54 0.004 3 2 2 2 2 22.644 463 4 0793 25 70 3 2 6 78 5 4 1 3 8 3 1 1 3 2 148.09 151.06 0.020 3 1 3 2 1 21.348 464 4 0793 25 70 3 2 6 78 5 7 1 2 8 1 1 1 2 2 141.33 143.59 0.016 1 1 1 2 2 21.348 466 4 0794 25 70 3 1 5 78 1 7 1 2 8 5 1 1 2 1 95.63 100.54 0.049 5 1 3 2 1 02.540 313 Demographics Location Pathology Measurements Radiograph Data PID M Cat # G Sp I S A AI M E S L R T A I C H L R O T Ap Al C S M1 M2 AAD 467 4 0846 25 70 3 1 6 78 1 1 1 2 8 1 1 1 2 1 57.36 64.05 0.104 1 2 1 2 2 26.490 468 4 1210 25 70 3 1 6 78 1 7 2 2 8 1 1 3 2 1 169.00 166.68 0.014 1 3 1 2 2 25.195 469 4 1212 25 70 3 1 6 78 1 2 2 3 7 6 1 2 1 3 168.70 167.76 0.006 6 4 11 1 1 06.416 470 4 1216 25 70 3 1 6 78 1 2 1 3 4 8 1 1 2 1 167.62 171.84 0.025 6 1 10 2 2 4 2 18.745 471 4 1218 25 70 3 2 6 78 4 7 2 3 8 4 1 2 2 1 149.03 148.22 0.005 4 2 3 2 2 29.263 472 4 0690 25 70 3 1 6 78 1 1 1 2 8 3 1 5 2 1 57.80 64.85 0.109 4 3 8 2 2 17.978 473 4 0691 25 70 3 2 5 78 5 1 2 2 8 1 1 1 1 1 122.89 124.58 0.014 1 3 1 2 2 04.238 474 4 0691 25 70 3 2 5 78 5 7 2 2 8 3 1 1 2 1 47.42 45.98 0.030 3 2 10 1 2 2 4 04.238 475 4 0601 25 70 3 2 6 78 1 7 2 1 8 1 1 1 2 1 149.36 148.39 0.006 1 1 5 2 2 05.638 476 4 0623 25 70 3 2 5 78 1 4 1 3 8 1 1 3 2 1 135.23 134.65 0.004 1 2 2 2 2 04.132 477 4 0638 25 70 3 2 6 78 1 7 1 2 8 1 1 3 1 4 N/A 149.69 1 4 11 1 2 20.507 478 4 0643 25 70 3 1 6 78 1 1 1 2 8 1 1 1 2 1 56.21 65.03 0.136 3 2 1 2 2 22.115 479 4 0675 25 70 3 1 5 78 1 5 1 1 8 3 1 1 3 1 85.71 90.18 0.050 1 2 3 2 2 01.060 480 4 1218 25 70 3 2 6 78 4 4 1 3 8 1 1 5 2 1 160.36 159.72 0.004 1 2 1 2 1 29.263

314 481 4 0469 25 70 3 1 6 78 1 7 2 3 8 1 1 1 2 1 165.45 164.20 0.008 1 1 1 2 1 06.652

483 4 0499 25 70 3 1 6 78 4 1 1 2 8 1 1 1 2 2 56.54 62.67 0.098 1 3 10 2 2 6 9 10.542 484 4 0499 25 70 3 1 6 78 4 4 2 3 6 8 3 1 1 1 176.35 176.24 0.001 8 2 1 1 2 10.542 486 4 0514 25 70 3 2 6 78 1 6 1 2 8 3 1 1 3 1 154.25 155.65 0.009 3 1 3 2 2 08.507 487 4 0514 25 70 3 2 6 78 5 7 1 2 8 5 1 1 2 1 141.74 144.45 0.019 5 1 3 1 1 08.507 489 4 0551 25 70 3 1 6 78 1 1 2 1 8 1 1 1 1 1 62.33 58.99 0.054 7 4 11 1 2 08.062 490 4 0402 25 70 3 1 6 78 1 4 2 3 8 6 1 1 1 1 177.57 177.95 0.002 6 1 1 2 1 13.907 491 4 0421 25 70 3 1 6 78 1 4 1 3 8 8 3 1 2 1 177.12 N/A 1 1 3 2 2 06.874

314

APPENDIX C: TIMING OF FRACTURE REPAIR CAYO SANTIAGO CASE STUDIES

The Cayo Santiago macaques offer a unique opportunity to match behavioral observations with individual fractures within the skeletal sample. Of the list of 37 macaques with known fractures submitted to the Cayo Santiago Field Station (CSFS) administrative offices in Punta Santiago, 17 individuals had injuries that were listed in the personal field notes and census data recorded by Edgar Davila, Chief Census Taker,

CSFS. These include injuries that likely have nothing to do with the fractures observed, such as broken scrota and rib wounds in several individuals and a possible neoplasm located on one individual‟s lower lip. Five individuals have fractures in locations matching those of wounds observed in the census data. All of these individuals are included below, along with Edgar Davila‟s unpublished behavioral observations, translated from the original Spanish where applicable. However, only one individual is noted by Davila as having a broken limb. The other four individuals were observed mainly to have received slashes, which may be restricted to soft tissue wounds.

315 Case Study #1

Figure C.1 CPRC 3916 left fibula in lateral (top) and anterior (bottom) views. Arrow indicates the location of the fracture.

Figure C.2 Radiographs of CPRC 3916 fracture in antero-posterior (AP – left) and medio- lateral (ML – right) views. Taken with NOMAD at fixed 60 kV, fixed 2.3 mA, 0.10 s.

316 LPMG catalog number: 3916

Cayo Santiago tattoo: 933

Date of birth: 5/17/1978

Date of death: 6/7/2000

Age of death: 22.074 yrs

Potential date of fracture: 9/12/1990

Potential age of fracture: 9 yrs 8 mo 4 d

Behavioral observation notes: The lateral side of the crural portion of the left hind limb is indicated. There is a 2" x 1" slash with inflammation. Davila: He can't walk too much, bleeding.

Palaeopathological notes: The male rhesus monkey designated CPRC 3916 exhibits an old, well remodeled fractured left fibula with minimal deformity. Other pathological conditions present in this individual include a fractured right clavicle, a rib fracture, and a dental abscess. Periostitis is present on the right humerus, radius, ulna, and femur as well as on the left femur, tibia, and fibula. Degenerative joint disease is present on most vertebrae, the right humerus, the right ulna, and both fibulae. Both acetabula and the surrounding area exhibit DJD and non-specific infection; the right femoral head is necrotic.

Discussion: It is possible that the injury described by Davila is connected with the fractured left fibula based on the placement of both injuries. Davila noted that CPRC

317 3916 had difficulty walking, suggesting that the injury was more severe than simply superficial slashes would indicate. However, he made no mention of broken bones in his report. If these injuries are both from the same incident, this suggests that CPRC 3916 sustained the fracture during an aggressive interaction, possibly falling from a tree in the midst of the confrontation, although this is speculation.

Case Study #2

Figure C.3 CPRC 4188 fractured left (left top) and right (right top) clavicles in inferior views. Nonunion fracture of left fibula (bottom) in lateral view.

318

Figure C.4 Radiographs of CPRC 4188 fractures. Left: left clavicle in antero-posterior (AP) and medio-lateral (ML) views. Center: right clavicle in AP and ML views. Right: left fibula in ML view. Taken with NOMAD at fixed 60 kV, fixed 2.3 mA, 0.10 s.

LPMG catalog number: 4188

Cayo Santiago tattoo: S56

Date of birth: 2/8/1989

Date of death: 6/19/2004

Age of death: 15.370 yrs

There are two behavioral observations that pertain to this individual. The first

(Case study #2A) corresponds to the fractured left clavicle and possibly also the fractured right clavicle. The second (Case study #2B) corresponds to the fractured left fibula.

Other injuries Davila noted for this individual but that likely do not pertain to the fractured elements include bloody bites and slashes on the plantar surface of the right hind paw on 8/9/1990 and an abscess on the dorsal surface of the right fore-paw on 319 8/31/1990. On 5/10/2004, the left side of his face sustained several puncture wounds, his left eye became inflamed, and his left hind limb was lame. The latter injuries occurred approximately a month before the death of the individual.

2A: Potential date of fracture: 6/21/2000

2A: Potential age of fracture: 2 yrs 11 mo 28 d

2A: Behavioral observation notes: There are slashes on both the left shoulder and neck region (1" x 1") and crural portion of the right front limb (1" x 2 1/2").

2A: Morphological notes: The left clavicle features a healed fracture with overlap of the bone fragments and absent apposition of the distal fragment posteriorly. The right clavicle is also fractured, with slight overlap, angulation, and inferior and posterior partial apposition of the distal fragment. The proximal fragments are displaced anteriorly by m. sternocleidomastoideus in both clavicles. In the left clavicle, m. deltoideus and various ligaments contribute to the inferior displacement of the distal bone end.

2B: Potential date of fracture: 9/10/1999

2B: Potential age of fracture: 4 yrs 9 mo 9 d

2B: Behavioral observation notes: On the left hind limb, the cranial side of the thigh and the caudal side of the leg are indicated. On the right hind limb, the gluteal region is indicated. Davila: I see the bone of that wound, it is very bad!

320

2B: Morphological notes: A nonunion fracture of the distal left fibula is present.

2: Discussion: The clavicular fractures are less likely to be associated with the slashes observed on CPRC 4188‟s shoulder than that the fibular fracture is associated with the wound deep enough for Davila to have noticed bone.

Case Study #3

Figure C.5 CPRC 3307 right fibula in anterior (top) and lateral (bottom) views.

321

Figure C.6 Radiographs of CPRC 3307 in antero-posterior (AP – left) and medio-lateral (ML – right) views. Taken with NOMAD at fixed 60 kV, fixed 2.3 mA, 0.10 s.

LPMG catalog number: 3307

Cayo Santiago tattoo: FB

Date of birth: 3/11/1964

Date of death: 8/13/1995

Age of death: 31.444 yrs

Potential date of fracture: 10/04/1990

Potential age of fracture: 4 yrs 10 mo 9 d

Behavioral observation notes: Inflammation was observed in a 3" x 1/4" swath along the right hind limb, laterally. A broken limb was noted.

Morphological notes: CPRC 3307 contains a fracture of the right fibula with medial partial apposition of the distal fragment and bone overlap. Other traumas include a

322 transverse fracture of the proximal left ulna and a segmental fracture of the left fibula.

The spine, hips, and knees all show extensive DJD.

Discussion: This is the only individual from the list I provided which Davila specifically notes suffered from a broken limb. As such, it is safe to assume that the injury he noted and the fracture I recorded are the same, placing the age of this fracture at 4 years and 10 months prior to the death of the animal.

Case Study #4

Figure C.7 CPRC 3372 left fibula in lateral (top) and anterior (bottom) views. 323

Figure C.8 Radiographs of CPRC 3372 in antero-posterior (AP – left) and medio-lateral (ML – right) views. Taken with NOMAD at fixed 60 kV, fixed 2.3 mA, 0.10 s.

LPMG catalog number: 3372

Cayo Santiago tattoo: 928

Date of birth: 1/29/1978

Date of death: 11/29/1993

Age of death: 15.836 yrs

Potential date of fracture: 12/04/1989

Potential age of fracture: 3 yrs 11 mo 25 d

Behavioral observation notes: Slashes and inflammation were noted at the lateral side of the left hind leg, superior to the ankle.

Morphological notes: A nonunion fracture in the proximal third of the left fibula is noted.

Minimal healing has occurred and infection is present. This individual also exhibits infection adjacent to the deltoid tuberosity on the right humerus. 324 Discussion: Of the five case studies presented here, the fracture in CPRC 3372 is least likely to match the behavior observed by Davila. From the portion of the macaque outline shaded in by Davila in the census record, it appears as if that injury was located slightly inferior to the position of the fracture. Also, there appears to have been little healing for a fracture that occurred almost four years prior to the death of the animal.

Case Study #5

Figure C.9 CPRC 3393 right fibula in anterior (top) and lateral (bottom) views.

325

Figure C.10 Radiographs of CPRC 3393 in antero-posterior (AP – left) and medio-lateral (ML – right) views. Taken with NOMAD at fixed 60 kV, fixed 2.3 mA, 0.10 s.

LPMG catalog number: 3393

Cayo Santiago tattoo: 526

Date of birth: 2/23/1973

Date of death: 1/27/1993

Age of death: 19.940 yrs

Potential date of fracture: 8/2/1991

Potential age of fracture: 1 yrs 5 mo 25 d

Behavioral observation notes: There are punctures and slashes, one of which measures 2" x 1/2" all along the lateral surface of the right hind limb and trunk. Davila: Fresh, bleeding, deep wound.

Morphological notes: Bilateral fractures of the distal fibulae are noted, possibly having been caused by the same incident. The right fibula fracture is enveloped in extensive 326 callus although minimal deformity is present aside from partial apposition. Both femora and tibiae are infected and the clavicles are deformed and possibly dislocated.

Discussion: The fracture I observed and the punctures and slashes Davila observed may be connected, although the bone itself does not have any associated cutting or piercing injuries.

327