Capped Mangabey, in Sette Cama Gabon: a Phylogenetic Perspective

Home , Cercopithecinae, Crested mangabey, Cursorial, Diana monkey, Drill (animal), Durophagy

The Feeding, Ranging, and Positional Behaviors of Cercocebus torquatus, the Red- Capped Mangabey, in Sette Cama Gabon: A Phylogenetic Perspective.

Dissertation

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

Catherine Agnes Cooke, M.A.

Graduate Program in Anthropology

The Ohio State University

2012

Dissertation Committee:

W. Scott McGraw, Advisor

Debbie Guatelli-Steinberg

Dawn Kitchen

Jeff McKee

Catherine Agnes Cooke

2012

Abstract

The feeding, ranging, and positional behaviors of Cercocebus torquatus (red-

capped mangabey) were studied in Sette Cama, Gabon from 2008-2009. It has been

argued by several authors that hard-object feeding is the key adaptation of the

Cercocebus-Mandrillus clade and that durophagy influences many aspects of Cercocebus

social and behavioral ecology. The goal of this study was to evaluate the impact of

obdurate foods on C. torquatus adaptation and evolution by combining multiple lines of

evidence. Additionally, this information was used to test the hypothesis that C.

torquatus is the most primitive member of its genus and that C. torquatus is a sister

taxon to Mandrillus.

C. torquatus in Sette Cama fed predominantly on fruits and seeds, but seed

consumption was higher than that reported for other C. torquatus populations. The C.

torquatus diet in Sette Cama was dominated by foods with intermediate to high hardness values and their foods were comparable in hardness values to those reported in other studies. The consumption of obdurate foods remained constant throughout the wet and dry seasons, and C. torquatus showed no preference for any food group.

This suggests that durophagy is habitual among this population and does not serve as a fallback strategy.

C. torquatus in Sette Cama occupies a smaller home range than other Cercocebus

species of similar group sizes. The ranging behaviors of C. torquatus were influenced by the seasonal distribution and availability of fruits, particularly the location of Sacoglottis gabonensis seeds. The lack of competing primate species in their habitat along with the intensive use of both terrestrial and arboreal resources by C. torquatus may explain their small home range. C. torquatus also frequently divided into subgroups.

C. torquatus spent the majority of time on the ground followed by the understory (one to five meters) and forest canopy at heights of five to twenty meters.

Contrary to predictions based on phylogenetic relationships and morphology, C. torquatus is possibly one of the least terrestrial of all Cercocebus species studied. They used quadrupedal locomotion most frequently during travel and feeding followed by climbing and leaping. The most common postural behaviors were sitting and quadrupedal standing.

The feeding, ranging, and positional behavior data from this study supports a close relationship between C. torquatus, C. atys, and C. lunulatus within the Cercocebus-

Mandrillus clade. C. torquatus and C. atys are similar in their large group sizes and reliance on hard-object foods such as Sacoglottis gabonensis seeds throughout the year.

Previous cranio-facial studies specifically positioned C. torquatus as the sister taxon to

Mandrillus. Nevertheless, the behavioral evidence suggests that C. atys occupies a more

similar niche to mandrills than does C. torquatus. Since C. torquatus and Mandrillus

iii species are sympatric throughout much of their distribution, several behavioral differences would be expected between these groups.

This study does not refute the hypothesis that C. torquatus and Mandrillus are sister taxa. Their current sympatry and niche partitioning suggest they could have evolved from a common terrestrial ancestor by sympatric speciation. The recognition of a 1.5 to 2 million year old fossil species closely resembling C. torquatus and the behavioral ecology of C. torquatus suggests that the polarity of the features shared by C. torquatus and Mandrillus are ancestral rather than derived for this clade.

Dedication

To my mother, Agnes Cooke, for never giving up, Nathaniel Cooke Moussopo, my little mangabey, and in memory of Thomas Howard Cooke, Sr.

Acknowledgements

I would like to thank Dr. W. Scott McGraw for your guidance and advising on this dissertation and throughout my graduate study career. Thank you for never giving up hope that I would finish. I also thank the other members of my candidacy and dissertation committee for their patience and support. I thank the Ministere d’Eaux et Fôrets of Gabon, CENAREST, and the village chief of Sette Cama for permission to study the mangabeys and live at the Brigade d’Eaux et Forets. I am indebted to the WWF- Gabon, in particular Bas Huijbregts and Bas Verhage, for their logistical support and assistance in this project.

Thank you to all the members of “Equipe torquatus” including Joseph Ibinda Igouwe, Zico Ibamba Igalla, and Richard Moussopo Ibessa. Joseph, I would not have survived my two years in Gabon without your knowledge of the forest, companionship, humor, and good cooking. Richard, thank you for your helpful comments, map making skills, and your support and belief in my ability to finish this dissertation.

I am indebted to the various family members and friends who helped fund this endeavour, gave me books for the field, or moral support when I needed it! In particular I thank Agnes Cooke, Mary Cooke-Hall, Tom Cooke, Mary Adduci, Bonnie Martuarano, Ariane Payen, Lucy Keith, Elisabeth Hellmer, Michelle Rodrigues, and Indus Films. Thanks to Mary Cooke-Hall, Patrick Hall, Tom Cooke, Mary Beavers, and Elisabeth Hellmer for housing my cats at one time or another while I was off chasing mangabeys.

This research was funded by grants from The Ohio State University (Department of Anthropology, Office of International Affairs, Alumni Grant, OSU-Sigma Xi), Sigma Xi, Primate Conservation, Inc., and the International Primatological Society.

Vita

1999………………………………………………B.A., Anthropology, University of Missouri-Columbia

2003………………………………………………M.A., Anthropology, The Ohio State University

Publications

McGraw WS, Cooke C, and Shultz S. 2006. Primate remains from African Crowned eagle (Stephanoaetus coronatus) nests in Ivory Coast’s Tai Forest: Implications for primate predation and early hominid taphonomy in South Africa. Amer J Phys Anthropol 131:151-165.

Newell E, Guatelli-Steinberg D, Field M, Cooke C, and Feeney R. 2006. Life history, enamel formation, and linear enamel hypoplasia in the Ceboidea. Amer J Phys Anthropol 131:252-260.

Fields of Study

Major Field: Anthropology

vii

Table of Contents

Abstract ...... ii Dedication ...... v Acknowledgements...... vi Vita vii List of Tables ...... xi List of Figures ...... xv Chapter One: Introduction ...... 1 1.1 Introduction ...... 1 1.2 Species Profile: Cercocebus torquatus torquatus Kerr (1792) ...... 1 1.3 Background on the Cercocebus-Mandrillus clade ...... 7 1.4 Cercocebus-Mandrillus Morphology and Hard-object Feeding Adaptations...... 21 1.5 Cercocebus-Mandrillus Biogeography and Evolution ...... 26 1.6 Cercocebus-Mandrillus: The impact of obdurate feeding? ...... 29 1.7 Research Questions ...... 30 1.8 Organization of dissertation ...... 31 Chapter Two: General Methods and Basic Data ...... 42 2.1 Introduction ...... 42 2.2 Background ...... 42 2.3 Research Questions ...... 48 2.4 Methods ...... 48 2.5 Data Analyses ...... 61 2.6 Results ...... 64 2.7 Discussion ...... 76 2.8 Conclusions ...... 85

viii

Chapter Three: Diet and Food Hardness ...... 116 3.1 Introduction ...... 116 3.2 Background ...... 118 3.3 Research Questions ...... 138 3.4 Predictions ...... 139 3.5 Methods ...... 140 3.6 Data Analysis ...... 145 3.7 Results ...... 148 3.8 Discussion...... 155 3.9 Future Directions and Conclusions ...... 164 Chapter 4: Ranging and Subgrouping Behaviors ...... 188 4.1 Introduction ...... 188 4.2 Background ...... 189 4.3 Research Questions ...... 196 4.4 Predictions ...... 197 4.5 Methods ...... 199 4.5 Data Analysis ...... 201 4.7 Results ...... 204 4.8 Discussion...... 210 4.9 Future directions ...... 217 Chapter Five: Locomotion ...... 234 5.1 Introduction ...... 234 5.2 Background ...... 235 5.3 Research Questions ...... 256 5.4 Predictions ...... 257 5.5 Methods ...... 262 5.6 Data Analysis ...... 267 5.7 Results ...... 268 5.8 Discussion...... 287 5.9 Future Directions ...... 298

Chapter Six: Posture ...... 334 6.1 Introduction ...... 334 6.2 Background ...... 335 6.2 Research Questions ...... 348 6.3 Predictions ...... 349 6.4 Methods ...... 352 6.6 Data Analysis ...... 356 6.7 Results ...... 356 6.8 Discussion...... 362 6.9 Conclusions ...... 368 Chapter Seven: Conclusions and Future Directions ...... 381 7.1 Introduction ...... 381 7.2 Summary of findings and comparison to fellow clade members ...... 381 7.3 Cercocebus-Mandrillus phylogeny and biogeography ...... 393 7.4 Generalizations about Cercocebus species ...... 403 7.5 Future Directions ...... 405 Appendix A: C. torquatus foods ...... 414

List of Tables

Table 1.1. The Diets of Known Species of Cercocebus and Mandrillus

Table 1.2. The Overall Amount of Time Spent on the Ground for Several Cercocebus Species and Drills

Table 1.3. The Group Sizes, Day Ranges (in meters), and Home Ranges (in hectares) for Cercocebus and Mandrillus Species

Table 2.1. Some Common Plant Names in the Local Balumbu Language

Table 2.2. List of the Phenology Species, Identification Labels, Height (in meters), and DBH

Table 2.3. Sample Sizes for Group Scans and the Total and Average Number of Individuals Observed each Month by Age Class

Table 2.4. The Number of Focal Animal Scans by Month and Sex Class

Table 2.5. Monthly Averages for each Maintenance Activity

Table 2.6. Maintenance Activities for all Sexes and Age Classes

Table 2.7. The Monthly Averages for Height Class Use

Table 2.8. Average Height Class Use for every Sex and Age Class

Table 2.9. Simpson’s Diversity Index as a Measure of Vertical Group Spread by Month

Table 2.10. The Summary of Vegetation and Vegetation Analyses by Habitat Type

Table 2.11. Summary of all the Tree and Liana Species Identified within the Sentier Nature Forest and the Mean DBH

Table 2.12. The C. torquatus Fruit Trees Sampled within the Vegetation Plots and the Habitats in which They are Found

Table 2.13. Spearman’s Rank Correlation Values for Correlations between the Three Estimates of Fruit Availability Based on Phenological Data

Table 2.14. Spearman’s Rank Correlation and p Values for Correlations among the Food Availability Estimates and Maintenance Behaviors

Table 2.15. Spearman’s Rank Correlation and p values for Correlations among the Food Availability Estimates and Mean Height Use and Vertical Group Spread

Table 2.16. Spearman’s Rank Correlation and p Values for Correlations among the Food Availability Estimates and Habitat Type Use

Table 2.17. The Maintenance Activity Patterns among the Cercocebus Species

Table 2.18. The Percentage of Total Time Spent Traveling, Home Range Size, and Group Size among Cercocebus Species

Table 2.19. The Amount of Time Spent in each Height Class among the Cercocebus Species

Table 3.1. The Diets of Known Species of Cercocebus and Mandrillus

Table 3.2. All of the Foods Identified During the Study Period from 2008 – 2009

Table 3.3. The Food Species Eaten by C. torquatus During the February – December 2008 Habituation Period and their Frequencies of Observation

Table 3.4. The Number of Observations of Each Food Species by Month for the Prehabituation Period (February – December 2008)

Table 3.5. Total Number of Records of Each Food Species and the Contribution to Overall Diet from May – September 2009

Table 3.6. Monthly Summary of the Number of Records of Each Food Species Eaten from May – September 2009

Table 3.7. Contribution of Each Food Type by Month from May – September 2009

Table 3.8. Food Crop Scores for May – September 2009

Table 3.9. Pearson’s Correlation Coefficients for Food Category Compared to Food Crop Score from May – September 2009

Table 3.10. The Average Shore Hardness Values and Standard Error for Foods which Registered on the Type A Durometer

xii

Table 3.11. The Average Shore Hardness Values and Standard Error for Foods which Registered on the Type D Durometer

Table 3.12. The Monthly Mean Shear Hardness Values from the Type A and Type D Durometers

Table 3.13. Monthly Summary of the Percent Contribution of Each Food Category to the C. torquatus Diet

Table 3.14. Pearson’s Correlation Coefficient Comparing Consumption of Each Food Property Type Category with Food Availability

Table 4.1. Summary of Known Ranging and Grouping Data for Cercocebus Species

Table 4.2. Summary of the Months Represented in the Phenology and Ranging Maps by Season

Table 4.3. The Total Number of 1-hectare Quadrants Used in Each Month of the Study and the Total Number of Days of Data Collection Each Month

Table 4.4. The Total Number of Days that C. torquatus were Observed as the Whole Group and as Subgroups Compared to Total Days of Observation for May to September 2009

Table 5.1. Total Number of Trees, Average Number of Trees by 0.1 ha, Average Tree Height, and Mean DBH for the Beach and Terra Firme Habitat Types

Table 5.2. The Number of Scans for Each Locomotor Behavior for all Age and Sex Classes Combined and the Overall Percentage of Scans

Table 5.3. The Total Number of Individuals Scanned of Each Age and Sex Category

Table 5.4. The Frequency of Each Type of Locomotion for Each Sex and Age Class and the Total Percent of Locomotion Observations by Sex and Age Class

Table 5.5. Overall Locomotor Frequencies by Activity and Total Percent of Each Activity Observed During Locomotion

Table 5.6. The Average Frequency of Individuals Observed at Each Height for all Scans Combined

Table 5.7. Frequencies of Locomotor Behaviors at Each Height Class in all Individuals and Percentage of Total Observations of Locomotion at Each Height Class

xiii

Table 5.8. Fisher’s Exact Comparisons of Locomotor Behaviors by Height between the Age Classes

Table 5.9. Locomotor Frequencies of Adults at Each Height Class

Table 5.10. Locomotor Frequencies of Juveniles at Each Height Class

Table 5.11. Locomotor Frequencies of Subadults at Each Height Class

Table 5.12. Total Number of Locomotion Individual Scans and their Frequencies by Tree Zone

Table 5.13. Frequency of Locomotor Behaviors by Tree Zone for all Ages and Sexes and Total Percentage of Locomotor Observations in Each Zone

Table 5.14. Frequency of Locomotor Behaviors of Adults by Tree Zone

Table 5.15. Frequency of Locomotor Behaviors of Juveniles by Tree Zone

Table 5.16. Frequency of Locomotor Behaviors of Subadults by Tree Zone

Table 5.17. Total Number of Locomotion Scans and their Frequencies by Support Size for all Ages and Sexes

Table 5.18. Frequency of Locomotor Behaviors by Support Type for all Ages and Sexes Combined and Total Percent of Observations During Locomotion on each Support Type

Table 5.19. The Frequency of Locomotor Behaviors on Vertical and Horizontal Tree Trunks for all Ages and Sexes Combined

Table 5.20. Frequency of Locomotor Behaviors by Support Type for Adults

Table 5.21. Frequency of Locomotor Behaviors by Support Type for Juveniles

Table 5.22. Frequency of Locomotor Behaviors by Support Type for Subadults

Table 5.23. Total Number of Locomotion Scans and their Frequencies by Habitat Type for all Ages and Sexes

Table 5.24. Frequency of Locomotor Behaviors by Habitat Type for all Ages and Sexes and the Total Percent of Locomotor Observations in Each Habitat Type

Table 5.25. Frequency of Locomotor Behaviors by Habitat Type and Total Percent Observations for Juveniles

xiv

Table 5.26. Frequency of Locomotor Behaviors by Habitat Type and Total Percent Observations for Subadults

Table 5.27. Locomotion of Lophocebus albigena from Kibale National Park, Uganda

Table 6.1. Number of Individual Records of Postures Observed and their Frequencies for all Age and Sex Categories Combined

Table 6.2. Posture Frequencies for Each Sex and Age Category

Table 6.3. The Frequency of Postures by Activity and the Total Percent of Each Activity Observed for all Ages and Sexes Combined

Table 6.4. The Frequency of Postures by Height and the Total Percent of Observations at Each Height for all Ages and Sexes Combined

Table 6.5. The Frequency of Postures by Height and the Total Percent of Observations at Each Height for Male and Female Adults Combined

Table 6.6. The Frequency of Postures by Height and the Total Percent of Observations at Each Height for Juveniles

Table 6.7. The Frequency of Postures by Height and the Total Percent of Observations at Each Height for Subadults

Table 6.8. Fisher’s Exact Comparison of Postures Used at Different Heights by Adults and Juveniles and Subadults and Juveniles

Table 6.9. The Frequency of Postures by Forest Zone and the Total Percent of Observations at Each Zone for all Ages and Sexes Combined

Table 6.10. The Frequency of Postures by Support Type and the Total Percent of Observations on Each Support for all Ages and Sexes Combined

Table 6.11. The Distribution of Maintenance Activities on Each Support Type During Non-locomotor Behaviors in C. torquatus

Table 6.12. Postures for all Age and Sex Classes by Habitat Type and the Percentage of Posture Observations for Each Habitat Type

Table 6.13. Cercocebus atys Postures Overall and by Resting, Social, and Feeding from Taï National Park, Cote d’Ivoire (Data from McGraw 1996a, 1998b)

List of Figures

Figure 1.1. An Illustration of Cercocebus torquatus (Courtesy of Stephen Nash)

Figure 1.2. The Distribution of C. torquatus in West Central Africa

Figure 1.3. The Current Papionin Phylogenetic Tree

Figure 1.4. Distribution of the Cercocebus Species in Africa

Figure 1.5. The Distribution of Mandrillus in Africa

Figure 1.6. The Molarized Premolars of Cercocebus and Mandrillus Compared to Lophocebus and Papio (From Fleagle and McGraw, 2002)

Figure 1.7. The Humerii of Several Papionins

Figure 1.8. The Proposed Dispersal Route and Evolutionary Trajectory for Cercocebus Species

Figure 2.1. The Location of Sette Cama, Gabon

Figure 2.2. The Distribution of the Different Habitat Types within the Sentier Nature Forest

Figure 2.3. The Flooded Mangrove Forest Fear the Edge of the Lagoon

Figure 2.4. A Section of the Mangrove Forest During the Dry Season

Figure 2.5. Terra Firme Habitat

Figure 2.6. Another View of the Terra Firme Habitat

Figure 2.7. Coastal Palm Forest

Figure 2.8. Another View of the Coastal Palm Forest

Figure 2.9. A Map of the Three Main Trails in the Sentier Nature Forest, Sette Cama, Gabon

Figure 2.10. The Inaccessible Swamp Zone that Borders the Mangrove Forest

Figure 2.11. Adult Male C. torquatus

xvi

Figure 2.12. Adult Female C. torquatus

Figure 2.13. Subadult C. torquatus

Figure 2.14. Tree Zones; 0=Ground (not marked), 1= Tree Trunk, 2= Interior Canopy Branches, 3=Terminal Branches, 4= Uppermost Canopy, 5=Areas Adjacent to Tree Trunk including Lianas and Treefalls

Figure 2.15. The Vegetation Plots Collected along the Three Main Trails in Sentier Nature

Figure 2.16. The Location of Phenology Trees in the Sentier Nature Forest

Figure 2.17. Average Maintenance Activity Budget for C. torquatus During the Months of May – September 2009

Figure 2.18. The Overall Average Height Class Distribution of C. torquatus

Figure 2.19. The Frequencies of Maintenance Activity within Each Height Class

Figure 2.20. The Monthly Vertical Group Distribution (Range 0 – 1) Compared to Food Availability for Each Month

Figure 2.21. Monthly Distribution of Scan Observations Over the Different Habitat Types (N=155)

Figure 2.22. One of the Crab Species (Cardisoma armatum) Eaten By C. torquatus in Sette Cama

Figure 2.23. The Distribution of Each Maintenance Activity by Habitat Type

Figure 2.24. Height Class Distribution within Each Habitat Type

Figure 2.25. The Number of Trees of Each DBH Class in the Sentier Nature Forest

Figure 2.26. C. torquatus Filling his Cheekpouches with Manilkara Fruits (Photo by BBC)

Figure 2.27. The Number of Tree Species with Fruit or Seeds by Month for January – September 2009

Figure 2.28. The Number of Individual Trees with Fruit or Seeds by Month for January – September 2009

Figure 2.29. Total Estimated Crop Production of Phenology Trees by Month

Figure 2.30. Scatterplot of the Relationship Between Travel Time and Home Range Size among African Papionins.

xvii

Figure 3.1. Stress-strain Curve Indicating Elastic Modulus and Yield Point

Figure 3.2. The Type A and Type D Asker Durometers (Photo Courtesy of J. Pampush and D. Daegling)

Figures 3.3 and 3.4. The Plunger of the Type A Durometer and the Type D Durometer (Photos Courtesy of J. Pampush and D. Daegling)

Figures 3.5 and 3.6. A Sacoglottis gabonensis endocarp and its cross-section (Photos Courtesy of J. Pampush and D. Daegling)

Figure 3.7. The Total Monthly Number of Food Species and Feeding Observations for the Prehabituation Study Period

Figure 3.8. Percentage of Foods by Category Observed from February – December 2008

Figure 3.9. Graphical Representation of the Foods Eaten and their Frequencies During the Februrary – December 2008 Habituation Period

Figure 3.10. Graphical Representation of the Frequency of Observation of each Food Species from May – September 2009

Figure 3.11. Total Number of Feeding or Foraging Records by Month and the Number of Different Food Species Recorded from May – September 2009

Figure 3.12. Diet Composition from May – September 2009 by Food Type

Figure 3.13. The Number of C. torquatus Foods Classified as Hard, Soft, or Cross-over Identified During the Study Period

Figure 3.14. C. torquatus Incising a Hard Palm Fruit. Photo Still from the BBC Film “Living with Monkeys”

Figure 3.15. Maxillary Dentition of a Deceased C. torquatus from Sette Cama, Gabon

Figure 4.1. The Distribution of Habitat Types within the Sentier Nature Forest, Sette Cama, Gabon

Figure 4.2. Total Number of GPS Points Collected for C. torquatus by Month and Year

Figure 4.3. The Cumulative Range Use of C. torquatus in 2008 and 2009 Calculated with the Grid Cell Method

xviii

Figure 4.4. The Cumulative Range Use of C. torquatus in 2008 and 2009 Calculated with the Minimum Convex Polygon Method

Figure 4.5. Grid Cell Maps for the 2008 Study Period

Figure 4.6. Grid Cell Maps for the 2009 Study Period

Figure 4.7. The Density of Observations by Quadrant During 2008-2009

Figure 4.8. The Location of Phenology Trees Compared to Habitat Use in 2008-2009

Figure 4.9. The Location of Guibortia and Sacoglottis Phenology Trees Compared to Habitat Use During 2008-2009

Figure 4.10. The Movements of C. torquatus Compared to Fruiting Trees During the Wet (March-April-May) Season of Data Collected During 2008

Figure 4.11. The Movements of C. torquatus Compared to Fruiting Trees During the dry (June-July) Season of Data Collected During 2008

Figure 4.12. The Movements of C. torquatus Compared to Fruiting Trees During the Wet (April-May) Season of Data Collected During 2009

Figure 4.13. The Movements of C. torquatus Compared to Fruiting Trees During the Dry (June-July-August) Seasons of Data Collected During 2009

Figure 4.14. The Total Number of Days C. torquatus were Observed as a Whole Group and as Subgroups Compared to the Number of Fruit Trees Available each Month for May to September 2009

Figure 5.1. A Comparison of Papionin Scapulae Reveals a Taller Suprascapular Fossa and Deeper Inferior Angle among Cercocebus and Mandrillus (From Fleagle and McGraw, 2002)

Figure 5.2. The Differences in Degree of Suborbital Fossa Depth among Different Mangabey Species (From McGraw and Fleagle, 2006)

Figure 5.3. The Similar Degree of Paranasal Ridging between C. torquatus and M. leucophaeus (From McGraw and Fleagle, 2006)

Figure 5.4. The Coastal Palm, or Beach, Forest of Sette Cama, Gabon

Figure 5.5. A Section of the “Main Trail,” or Terra Firme Forest of Sentier Nature

Figure 5.6. C. torquatus on the Ground of the Terra Firme Forest of Sette Cama, Gabon

xix

Figure 5.7. Vegetation Map of the Sentier Nature Forest

Figure 5.8. C. torquatus Quadrupedal Walk

Figure 5.9. C. torquatus Quadrupedal Run

Figure 5.10. Climb

Figure 5.11. Leap (Photo by CERCOPAN)

Figure 5.12. Descend Bottom First

Figure 5.13. Descend Head First (Photo by Lucy Keith)

Figure 5.14. Tree Zones; 0=Ground (not marked), 1= Tree Trunk, 2= Interior Canopy Branches, 3=Terminal Branches, 4= Uppermost Canopy, 5=Areas Adjacent to Tree Trunk including Lianas and Treefalls

Figure 5.15. The Hands of C. torquatus on the Largest Support Type, a Bough

Figure 5.16. Adult Female Sitting on a Branch

Figure 5.17. C. torquatus Gripping Twigs, or the Smallest Supports Available in an Arboreal Context

Figure 5.18. The Palm Trees Typical of the Beach Forest in Sette Cama

Figure 5.19. C. torquatus Eating a Palm Fruit in the Discontinuous Roots and Branches Associated with the Zone Nearest to the Lagoon

Figure 5.20. A Comparison of the Locomotor Profiles of all Individuals of C. torquatus and C. atys from Taï National Park, Côte d’Ivoire

Figure 5.21. The Locomotor Profiles of Adult C. torquatus (N=155) and C. atys (N=466)

Figure 5.22. The Strata Use of Adult C. torquatus Compared to C. atys

Figure 5.23. Support Use During Locomotion for Adult C. torquatus and C. atys

Figure 5.24. A Comparison of C. torquatus (G3) and C. atys (2106) Scapulae

Figure 6.1. C. torquatus Sitting with Feet and Hands Propped on Substrates

Figure 6.2. Quadrupedal Stand (Photo by Lucy Keith)

Figure 6.3. Sit

Figure 6.4. Lie

Figure 6.5. Droop (Photo Courtesy of CERCOPAN, Witzens)

Figure 6.6. Supported Stand

Figure 6.7. The Distribution of Support Use among C. torquatus and C. atys During Postural Behaviors (Data From McGraw 1996a, 1998b)

Figure 6.8. Postures of Lophocebus albigena During Feeding from Kibale National Park, Uganda

Figure 7.1. A Red-capped Mangabey Print Left Along the Ocean Coast

Figure 7.2. A Red-capped Mangabey Crossing the Grassy Open Area between Two Forested Areas of the Sentier Nature Forest

Figure 7.3. C. torquatus killed by a python along the beach (Photo by Tanguy Mahanga)

Figure 7.4. The Modern Distribution of Cercocebus Species and the Proposed Dispersal Route of Grubb (1978, 1982) and McGraw and Fleagle (2006). (Illustration Courtesy of W. Scott McGraw)

Figure 7.5. The C. atys-M. sphinx hybrid from Brookfield Zoo (Photo by Michelle Rodrigues)

Figure 7.6. The Current Papionin Phylogenetic Tree with Molecular Divergence Dates Added (Dates were Based on TSPY Protein Divergence Times; Tosi et al., 2003)

Figure 7.7. Another Hypothesis for the Radiation and Dispersal of Cercocebus Mangabeys that Incorporates Extinct Taxa

xxi

Chapter One: Introduction

1.1 Introduction

This chapter serves as a general overview of the Cercocebus-Mandrillus clade.

First, I introduce the study species, Cercocebus torquatus, the red-capped mangabey,

and what is known about its behavior and ecology. Next, I discuss the phylogeny and

taxonomic revisions of African papionins followed by a summary of what is known about

the distribution, ecology, and social behavior of each species. Finally, I present the

morphological features that define the Cercocebus and Mandrillus genera and the

scenarios proposed for the evolution of these features. This information will be useful

for the upcoming chapters and for understanding the place of C. torquatus in the

evolution and radiation of the Cercocebus-Mandrillus clade.

1.2 Species Profile: Cercocebus torquatus torquatus Kerr (1792)

Classification

C. torquatus is a member of the cercopthecine tribe Papionini. The sooty

mangabey, C. atys, was previously considered a subspecies of C. torquatus (Groves,

1978); however, phenotypical differences between the two species were identified and each variant now has species status (Kingdon, 1997; Groves, 2001; Grubb et al., 2003).

There is debate as to the status of another mangabey, C. lunulatus (the white-napped

mangabey). Most argue that C. lunulatus should be considered a subspecies of C. atys

whereas others suggest C. lunulatus is more similar to C. torquatus (Grubb et al., 2003).

Nevertheless, it is generally accepted that C. lunulatus is a subspecies of C. atys. C. torquatus is listed as vulnerable with decreasing population numbers and has Appendix

II CITES status (www.iucnredlist.org).

Geographic Distribution and Habitat Preference

C. torquatus is found along coastal regions in Western and Central Africa (Figure

1.2). C. torquatus ranges from Western Nigeria (from west of Cross River; Igangan

Forest Reserve), through Cameroon (east as far as East Dja Reserve) and Equatorial

Guinea (Rio Muni), to the coast of Gabon (Ehardt, forthcoming; Happold, 1973; Kingdon,

1997). The distribution of C. torquatus in Gabon was reported to end at Sette Cama

(Ehardt, forthcoming; Groves, 2001); however, C. torquatus is found as far south as

Mayumba National Park, which borders the Republic of Congo (Maisels et al., 2007).

The distribution and estimated number of C. torquatus present in Gabon is unknown (Maisels et al., 2007). The majority of primate field studies in this country are either from Lopé National Park (Abernethy et al., 2002; Tutin et al., 1991; Tutin et al.,

1997), which is outside the range of C. torquatus, or focused on great ape populations

(Boesch et al., 2009; Furuichi et al., 1997; Tutin and Fernandez, 1993). Nevertheless, because of its low human population density and extensive remaining forested regions

(Lahm, 2001), Gabon is probably the last population stronghold for C. torquatus.

Ancedotal reports suggest that C. torquatus can also be found in unprotected inland

2 forests in northern Gabon and Moukalaba-Doudou National Park in southwestern

Gabon (WWF, pers. comm.) As late as 2000, C. torquatus was also seen in Conkuati-

Douli National Park in the Republic of Congo, although rarely (Maisels et al., 2007).

C. torquatus faces hunting pressure throughout its range and it is becoming increasingly rare in Nigeria and Cameroon (Happold, 1973; Kingdon, 1997; Tooze, 1994).

C. torquatus are medium-sized primates that have conspicuous vocalizations, making them easy targets for poachers. They also may get ensnared in wire traps set for other small, terrestrial mammals (Maisels et al., 2007). To that end, census data from Korup

National Park in southwestern Cameroon found a decline in C. torquatus populations because of hunting and logging in the region (Waltert et al., 2002). Presumably, the distribution and number of C. torquatus is currently even less than previously reported.

Reports on the distribution of C. torquatus indicate that they are mostly restricted to coastal, wet forests, inland swamp forests with extensive mangrove roots and littoral forest (Jones and Sabater Pi, 1968). This matches the forest habitats encountered in Sette Cama and southwestern Gabon.

Physical Description and Locomotion

The pelage of C. torquatus ranges from chestnut brown to dark grey with the underside and inner surfaces of limbs white in color (Groves, 2001; Kingdon, 1997;

Figure 1.1). The white coloration reaches the chin and the sides of the neck and cheeks with a white patch of hair on the backside of the head. The top of the head is maroon in color and the ears and muzzle are dark grey to black. The eyelids are white and the tail

3 tip has a white tuft of fur. The tail carriage is “…either extended nearly straight behind, often bowed and with a slight curl at the tip, or arched over the back with the tip dangling above the head or shoulders” (Jones and Sabater Pi, 1968:103). Both the eyelids and tail aid in communication through the dense understory. For example, in

Sette Cama, the tail was often used in the above the head position when C. torquatus was on alert or alarm calling (pers. observ). C. torquatus also raises its eyebrows to expose the white eyelids during threat gestures (Field, 2007).

The sexes are dimorphic in size. Body mass for males has been reported from 7-

12.5 kg and female weight ranges from 5 – 8 kg (average= 9.47 kg for males and 5.5 kg for females, Smith and Jungers, 1997) (Kingdon, 1997; Smith and Jungers 1997). Fleagle

(1999) reports IMI of 83. There are geographical variations in skull size and length of white on the tail (Groves, 2001).

C. torquatus are semi-terrestrial (Jones and Sabater Pi, 1968; Kingdon, 1997;

Mitani, 1989). Their movement in the trees is described as slow and cautious. They are also characterized by their climbing abilities on both small vines and roots and large tree trunks. “Ascent is accomplished by head-first, hand-over-hand action and descent is made by backing down with similar hand-over-hand movements” (Jones and Sabater Pi,

1968: 104).

Previous studies in the wild and in captivity

The majority of studies on C. torquatus occurred in captivity. They have been the focus of cognition experiments that range from investigations of patterns of object

manipulation (Torigoe, 1985), emotional response and eye preference (de Latude et al.,

2009), hand preference and manual laterality (Blois-Heulin et al., 2006), to studies of

anxiety and stress related behaviors associated with different types of enclosures

(Reamer et al., 2010).

Relatively little is known about C. torquatus behavior in the wild. The earliest

observational reports present information on the distribution and habitat preference of

C. torquatus in Equatorial Guinea and other areas of West Africa (Malbrant and

Maclatchy, 1949; Jones and Sabater Pi, 1968). Jones and Sabater Pi (1968) provided a

brief overview of C. torquatus ecology and social behavior, but the only long-term study

on C. torquatus was conducted by Mitani (1989) in Campo, Cameroon.

Social and Behavioral Ecology

Mitani (1989) provided information on the diet, home range, habitat use, and

grouping patterns of C. torquatus in Campo, Cameroon. The home range in Campo was

247 ha and Mitani observed five C. torquatus groups in the area (Mitani, 1989; 1991).

Groups were composed of multiple males and females, and average group size was 25

individuals. Jones and Sabater Pi (1968) observed C. torquatus groups of 14 – 23

animals in their survey of West African primates. C. torquatus ate predominantly fruits/seeds (80% of diet) but also were observed eating monocotyledonous grasses, leaves, flowers, and animal prey (such as eggs). In Campo, C. torquatus shifted their

ranging patterns in response to several key fruiting species (Mitani, 1989). The vertical

distribution of C. torquatus was also related to available fruiting species. Travel, rest,

and social behaviors occurred most often on the ground (around 65 - 70% of scans) but

feeding was most common in the tree canopy (25-30 meters; 40% of scans).

Both Mitani (1989) and Jones and Sabater Pi (1968) remarked on the tendency of

C. torquatus to splinter into smaller groups that would rejoin later. “It seems that the

large groups of C. torquatus may be composed of subgroups or troops…” (Jones and

Sabater Pi, 1968:107). Mitani (1989) observed a similar phenomenon among the C.

torquatus population at Campo. The mean foraging group size was 21.11 ± 2.55

individuals. Mitani (1989) suggested that C. torquatus regulates foraging group size to

increase per capita foraging efficiency according to the availability and distribution of

fruits.

C. torquatus are reported to engage in mono and polyspecific associations with a number of species. Polyspecific associations can serve multiple purposes among primates including increasing foraging efficiency or protection from predators (McGraw and Zuberbühler, 2008; Noë and Bshary, 1997). In Sette Cama, Gabon, C. torquatus were often found with Cercopithecus cephus (Cooke, 2005). C. torquatus associated with several species in Campo Reserve, Cameroon including C. cephus, Cercopithecus pogonias, Cercopithecus nictitans, Lophocebus albigena, and Mandrillus sphinx (Mitani,

1991), and these associations varied seasonally. More recently, C. torquatus was observed in association with another close relative, Mandrillus leucophaeus (drills), in

Korup National Park, Cameroon (Astaras et al., 2011). The frequency of these non- random associations was surprising given the niche similarity of C. torquatus and drills.

C. torquatus uses the ground less often when in association with drills. Astaras et al.

(2011) propose that both drills and C. torquatus gain an advantage in predator detection by association.

1.3 Background on the Cercocebus-Mandrillus clade

Mangabey phylogeny

The tribe Papionini includes macaques, baboons, mandrills, drills, geladas, and mangabeys (Fleagle, 1999). Macaques are considered the primitive papionin group and serve as the outgroup for most molecular and morphological studies on African papionins. For many years, the African papionins were divided into two groups: baboons (baboons, mandrills, drills, and geladas) and mangabeys (Fleagle and McGraw,

2002). The baboon group included the larger, predominantly terrestrial species, and the remaining African papionins were placed in the mangabey group because of their shared medium size, long limbs and tails, hollow cheeks, and white upper eyelids.

Mangabeys also have several similar features of their dentition including large incisors, similar molar wear patterns, thick dental enamel, and laterally flaring cusps (Kay, 1981;

Shellis and Hiiemae, 1986; Szalay and Delson, 1979; Thornington and Groves, 1970).

Mangabeys were classified as possessing teeth adapted to crushing and feeding on obdurate foods (Kinzey and Norconk, 1990).

Because of their phenotypic similarities, the mangabeys were lumped into one genus, Cercocebus, and then separated into two species groups based on differences in substrate preference and morphological features (Fleagle, 1999; Groves, 2000; Napier,

1981; Schwartz, 1928; Thornington and Groves, 1970). The arboreal albigena-aterrimus

group featured more pronounced maxillary fossae, concave nasal bones, and larger

incisors (Szalay and Delson, 1979). The other group contained galeritus, torquatus, atys,

agilis, chrysogaster, and sanjei because of their shared semi-terrestriality, straight nasal

bones, a narrower braincase, and larger teeth for their skull sizes (Fleagle, 1999; Groves,

2000; Napier, 1981; Schwartz, 1928; Thornington and Groves, 1970). Molecular and

anatomical studies eventually revealed that mangabey taxonomy was more complex

than previously recognized and that mangabeys were not a monophyletic clade (Cronin and Sarich, 1976; Disotell, 1994; Disotell, 1996; Hewett-Emmett and Cook, 1978).

Therefore, the similarities among Lophocebus and Cercocebus species appear to be a result of convergence, and homoplasy is now recognized as being prominent among papionins (Collard and O’Higgins, 2001; Collard and Wood, 2001; McGraw et al., 2011).

Most authorities currently place albigena and atterimus in the genus Lophocebus and the remaining semi-terrestrial mangabeys in the genus Cercocebus (Groves, 2000;

Fleagle and McGraw, 1999). The discovery of a new primate species, Rungwecebus kipunji, further complicated the mangabey classification scheme. Initially, kipunji was placed in the genus Lophocebus because of similarities in substrate use and skeletal features (Jones et al., 2005). It was then placed in a new genus, Rungwecebus, based upon more detailed investigation into kipunji’s molecular and morphological features

(Davenport et al., 2006). Researchers now propose that this species represents a hybrid between Papio and Lophocebus (Burrell et al., 2009).

The distinctions between Cercocebus and Lophocebus mangabeys were initially discovered when immunological investigations detected differences in the alpha and beta hemoglobin chains of the arboreal and terrestrial mangabeys (Barnicot and

Hewett-Emmett, 1972). Further studies of blood proteins and cranio-dental

characteristics supported the division of mangabeys into two genera (Cronin and Sarich,

1976; Hewett-Emmett and Cook, 1978; Groves, 1978). In addition, the postcranial

skeleton reflects morphological differences between Lophocebus and Cercocebus based

on substrate preference (Nakatsukasa 1994, 1996). For example, the humerus of the

arboreal albigena group features a reduced greater tuberosity, weak muscular

insertions on the humeral shaft, a thinner diaphysis, and less retroflexed medial

epicondyle compared to the semi-terrestrial species (Nakatsukasa, 1994, 1996).

Further molecular and genetic studies indicate that Lophocebus and Cercocebus

mangabeys are not even each other’s closest relatives. These analyses indicate that

Cercocebus mangabeys are more closely related to mandrills and drills (of the genus

Mandrillus), while the Lophocebus mangabeys are more properly allied with baboons

and geladas (Canedo et al., 2010; Disotell, 1994; Disotell, 1996; Disotell et al., 1992;

Harris and Disotell, 1998; Harris, 2000). Fleagle and McGraw (1999, 2002) identified a

suite of dental and postcranial features among Cercocebus and Mandrillus related to a

shared terrestrial hard-object foraging niche. These features include enlarged P4s, a

short and deep scapula, expanded deltoid tuberosities, broad brachialis flanges, and

proximally extended and laterally widened supinator crests. These similarities provide

further support for the molecular phylogeny uniting Cercocebus and Mandrillus to the

9 exclusion of other papionins. Additional morphological studies documented differences in the craniomandibular morphology of African papionins that reaffirm the molecular phylogeny such as the shape of the temporal and nuchal lines, the position of the nasal bones, and the position of the lingual mental foramina (McGraw and Fleagle, 2006;

Gilbert, 2007; Gilbert et al., 2009). Figure 1.3 illustrates the current phylogeny of papionins.

Cercocebus-Mandrillus Distribution

The genus Cercocebus includes six species that range from western to eastern

Africa (Groves, 2001; Kingdon, 1997; McGraw and Fleagle, 2006; Figure 1.4). Cercocebus atys (sooty mangabey) has two subspecies (atys and lunulatus) and ranges from Côte d’Ivoire to Guinea. Cercocebus torquatus (red-capped mangabey) ranges from western

Nigeria to the coast of Gabon and northern Congo. Cercocebus agilis (agile mangabey) is found in southeastern Cameroon, northeastern Gabon, southwestern Central African

Republic, and northern Congo to eastern Democratic Republic of Congo. Cercocebus chrysogaster (golden bellied mangabey) occupies the lower Congo River basin. The

Tana River mangabey (Cercocebus galeritus) is found in the gallery forest of Kenya’s

Tana River. Cercocebus sanjei (Sanje mangabey) has the most restricted distribution and is found on the eastern slopes of the Udzungwa Mountains in Tanzania.

The genus Mandrillus is much less widespread than Cercocebus (Figure 1.5).

Mandrillus sphinx (mandrill) is located in Cameroon, Gabon, and the Congo. Drills

(Mandrillus leucophaeus) are found in southeastern Nigeria, northwestern Cameroon,

and on Bioko Island. In some areas, Cercocebus species are sympatric with Mandrillus

species. The most notable distinction, apart from overall body size, between

Cercocebus and Mandrillus is the extraordinary secondary sexual characteristics of

Mandrillus males. Both Mandrillus species exhibit elaborate coloration and extreme sexual dimorphism.

Cercocebus-Mandrillus Feeding Ecology

Cercocebus and Mandrillus are some of the least studied primate genera because their habitat preference (dense, mangrove forest) and semi-terrestrial nature make them difficult to observe and habituate. However, researchers are beginning to piece together aspects of the feeding and behavioral ecology of several species (mandrills and drills: Caldecott et al., 1996, Hoshino, 1985, Lahm, 1986, Rogers et al., 1996, Abernethy et al., 2002, Astaras et al., 2011; C. agilis: Shah, 2003, Devreese, 2010; C. atys: McGraw,

1996a, Range and Noë, 2002, Range, 2004, McGraw et al., 2011; C. galeritus:

Homewood, 1978, Kinnaird, 1990, Wieczkowski, 2004, Wieczkowski, 2005, Mbora et al.,

2009; C. sanjei: Mwawende, 2009; C. torquatus: Mitani, 1989, 1991, Cooke et al.,

2009). These studies suggest that Cercocebus and Mandrillus species show a wide range

of variation in diet and their responses to seasonal food fluctuations. They also have

variable group sizes and home ranges.

Cercocebus and Mandrillus are often described as frugivorous seed predators

(Caldecott et al., 1996; Hoshino, 1985; Lahm, 1986; McGraw, 1996a; Rogers et al., 1996;

Shah, 2003), but they also feed on insects, mushrooms, small prey, and terrestrial

herbaceous vegetation that occur in small, dispersed clumps. Table 1.1 lists the diets of

different clade members. Several studies combined fruits and seeds into the same

category so exact numbers for seed-eating are not available for all species. However,

seed-eating was reported separately as 36.2% for Sanje mangabeys and 46.5% for Tana

River mangabeys (Wieckowski and Ehardt, 2009). Researchers still do not have

accurate data on the dietary composition of Mandrillus species so the values listed

represent estimations.

The dietary composition of each species differs in the amount of fruits, seeds, and invertebrates. Some species, such as C. atys, are heavily reliant upon seeds and

invertebrates (80% of diet; McGraw et al., 2011) whereas other species, such as C.

torquatus in Cameroon appear to be more frugivorous (60% of diet; Mitani, 1989). The

variation in diets among members of this clade may relate to differences in their

reliance on terrestrial foraging (Table 1.2). Anecdotal evidence suggests that mandrills

and drills are highly terrestrial (Caldecott et al., 1996; Abernethy et al., 2002; Astaras et

al., 2011) whereas the members of Cercocebus vary in degree of terrestriality.

Nevertheless, we should expect that more arboreal species are consuming more fruits

than the more terrestrial species.

When diet and terrestriality are compared, there are several instances where seed

eating increases with time spent on the ground (Table 1.2). The diet of C. atys contains

the most seeds (60%), and they are the most terrestrial of the mangabey species (67%)

(McGraw, 1996a; McGraw et al., 2011). C. galeritus have the second highest percentage

of seeds in their diets (32-42%) and spend around 50% of their time on the ground

(Kinnaird, 1990; Devreese, 2010). It will be interesting to compare the amount of seeds

in the Mandrillus diet with terrestriality once the data become available. In addition,

the consumption of invertebrates, fungi, and terrestrial vegetation may relate to time

spent on the ground for each species.

Degree of terrestriality also appears to change seasonally, at least in one mangabey

species. Shah (2003) notes that C. agilis, in Mondika, Central African Republic, spends

more time on the ground during periods of fruit scarcity. This shift towards terrestriality

may have continued in the other Cercocebus species in response to resource fluctuations leading to a higher degree of terrestriality among certain species. Each of the Cercocebus species appears to react differently in terms of feeding and travel times and ranging patterns during off seasons (see below). This may reflect different degrees of reliance on less preferred food types and local variability during periods of scarcity.

Despite differences in dietary composition and extent of arboreality, all

Cercocebus and Mandrillus species are characterized by their ability to feed on terrestrial hard-object foods to varying degrees. These foods tend to be unavailable and inaccessible to other primates. In her study comparing the feeding ecology of C. agilis and L. albigena in Central African Republic, Shah (2003) found differences in the

consumption of hard seeds and nuts between these genera. C. agilis also spent a

significantly larger portion of their time on the ground during feeding compared to L.

albigena. C. atys in the Taï Forest, Côte d’Ivoire, are able to eat Sacoglottis gabonensis

seeds for which chimpanzees use tools to access (McGraw et al., 2011). C. galeritus and

C. sanjei also feed on Diospyros mespiliformes and Parinari excelsa seeds, which have

13 some of the highest seed strengths in East Africa (Wieczkowski, 2009; Wieczkowski and

Ehardt, 2009).

These observations, along with morphological studies, have led researchers to propose that “the ability to subsist on hard seeds and nuts gleaned from the forest floor is a key adaptation for the Cercocebus-Mandrillus clade” (Fleagle and McGraw

2002:267). However, researchers differ in their interpretation of the evolution of this adaptation. Some argue that durophagy is a fallback strategy among mangabeys

(Lambert et al., 2004; Wieczkowski and Ehardt, 2009). Fallback feeding has multiple definitions and interpretations, but it is generally used to refer to foods eaten during periods of low food availability (Marshall and Wrangham, 2007). These foods usually require some physiological adaptations of the dentition or gastrointestinal tract because they are difficult to process. Some suggested adaptations for processing fallback foods include increased dental enamel and tooth size or increased gut passage rates (Marshall and Wrangham, 2007). On the other hand, preferred foods are expected to select for behavioral adaptations related to food harvesting such as an increased cognitive capacity or different positional behaviors.

Among mangabeys, it is proposed that the thick dental enamel and strong jaws of both Cercocebus and Lophocebus evolved as a consequence of reliance on bark and seeds during certain times of food shortage, or as a fallback food (Lambert et al., 2004;

Wieczkowski and Ehardt, 2009). Other researchers suggest that obdurate feeding is a habitual and regular occurrence among Cercocebus species and it does not fit the definition of fallback feeding outlined above (Cooke et al., 2009; McGraw et al., 2011;

McGraw and Daegling, 2012). For example, C. atys at Taï National Park, Côte d’Ivoire routinely eat hard-objects all year round (McGraw et al., 2011). Thus, in order to understand how and why Cercocebus and Mandrillus species evolved a hard-object

feeding niche, we must identify the role of obdurate foods in their diet and also how

Cercocebus and Mandrillus species adapt to food seasonality.

Cercocebus-Mandrillus Behavioral Ecology

Home range sizes vary greatly among Cercocebus species, and, in general,

species with larger group sizes occupy larger home ranges (Table 1.3). As group size

increases, the home range size should also increase to ensure adequate resources for all

group members and to help mitigate intragroup feeding competition. C. galeritus

populations reside in only 17-53 hectares (Homewood, 1978; Kinnaird, 1990). C. agilis,

C. sanjei, and C. torquatus home ranges are as large as 300 ha (Mitani, 1989, 1991; Shah,

2003; Cooke and McGraw, 2007; Mwawende, 2009) whereas C. atys ranges over 800 ha

(Range and Noë, 2002). Mandrills occupy extremely large home ranges (up to 18,200 ha) compared to Cercocebus species (White et al., 2010). Day ranges tend to increase with increases in overall home range.

Several mangabey species show shifts in ranging associated with low fruiting periods. When food availability decreased, C. galeritus increased its dietary diversity, total distance moved, and total area searched for food (Homewood, 1978). Mwawende

(2009) observed that C. sanjei ranged farther and moved faster during the dry season.

C. torquatus, in Campo, Cameroon, displayed seasonal shifts in their home range associated with the availability of four high quality fruiting species including S.

15 gabonensis and Anthonontha cladantha (Mitani, 1989, 1991). C. agilis devoted less time to travel during periods of fruit scarcity but ranged farther due to an increased reliance on terrestrial food items (Shah, 2003).

Many Cercocebus species live in groups of 17 to 50 individuals (Table 1.3), but C. atys lives in groups as large as 100+ individuals (Range and Noë, 2002; McGraw et al.,

2011), and at one site in Central African Republic, C. agilis forms groups of 230 individuals (Devreese, 2010). Mandrills have been observed in massive groupings, or hordes, that contain over 800 members and are the largest known groups of any non- human primate (Abernethy et al., 2002). This behavior has not yet been observed in wild drill populations. Mandrills and drills generally tend to disperse widely during foraging and search for scattered food sources (Caldecott et al., 1996). The larger home ranges occupied by these species enables them to maintain larger group sizes. The ability to feed on both arboreal and terrestrial foods also increases vertical and horizontal group spread and may facilitate larger group sizes, as seen in C. atys, C. agilis, and mandrill hordes.

Several species of Cercocebus, including agilis, atys, galeritus, torquatus and mandrills have been reported to break into subgroups (Homewood, 1978; Jones and

Sabater Pi, 1968; Mitani, 1989; Quris, 1975; Range, 2004; Shah, 2003). Mitani (1991) identified at least two adult males in the C. torquatus and mandrill subgroups but the composition of subgroups has not been studied in any species. The reasons for the proclivity towards subgrouping and possibly supergrouping among this clade are unclear. For example, the relationship between subgrouping patterns and food

availability in Cercocebus has not been systematically documented. Nevertheless, C.

atys tends to only subgroup during the dry season (Range, 2004; Shah, 2003). Typically

the dry season is a period of lowered food availability, and subgrouping may be a means

of reducing intragroup feeding competition.

Evidence from C. galeritus and mandrills suggest that supergrouping occurs

when food resources are abundant and evenly distributed (Abernethy et al., 2002;

Homewood, 1978). Devreese (2010) suggests that C. agilis in Bai Hoku, Central African

Republic maintain their large group size because it is more efficient when feeding on

slowly accumulating resources. Feeding as a large group prevents individuals from

returning to depleted patches before food sources are again available. It is expected

that when Cercocebus and Mandrillus feed on slowly accruing, evenly distributed hard-

object foods, it may also facilitate supergrouping through reduced intergroup feeding

competition (Jolly, 2007). Conversely, these species should split into subgroups when

feeding on more patchily distributed and clumped resources. Apparently this clade has

a phylogenetic tendency to form large groups; however, ecological constraints within

each habitat may prevent the maintenance of these groups year round (Jolly, 2007).

Cercocebus-Mandrillus social behavior

Little is known about the social structure and behavior of Cercocebus in the wild.

C. atys is the only Cercocebus species that has been studied in depth in its natural habitat (Range and Noë, 2002; Range, 2004), but information is becoming available about the social behaviors of other species such as C. sanjei (Mwawende, 2009). There

17 also have been multiple studies of C. atys social behavior in captivity at the Yerkes

Primate Research Center (Bernstein, 1976; Ehardt, 1988; Gust and Gordon, 1993; Gust and Gordon, 1994; Gust, 1995; Gust et al., 1998). These studies can help illuminate possible social behaviors in other Cercocebus species.

Cercocebus live in multi-male, multi-female groups and both sexes form linear dominance hierarchies (Mwawende, 2009; Range and Noë, 2002). Captive studies of social behavior among sooty mangabeys suggest that dominance is acquired rather than ascribed, as seen among free ranging C. atys (Ehardt, 1988; Gust, 1995; Range, 2006).

Outside of captivity, dominance is not based on size or age (except in older males) among C. atys, and dominance follows a pattern similar to that found among matrilineal primates (Range, 2004). A female’s rank is closely related to her mother’s rank and tends to remain stable throughout her life. From a young age sooty mangabeys recognize their place within the dominance hierarchy and solicit aid from higher ranking allies (Range, 2006). Juvenile females also showed a preference towards interacting with close maternal kin (Range, 2004).

In captivity, sooty mangabeys exhibit differences in dominance patterns and affiliations. Dominance is acquired rather than passed on by lineage, and there is no preferential affiliation among kin (Ehardt, 1988; Gust, 1995; Range, 2006). An individual’s rank is determined by matriline for the first few years of life (Gust and

Gordon; 1994; Gust, 1995). However, by around age 3, both male and female juveniles usually rank above their mothers. Juveniles challenge higher ranking individuals for a

18 higher position in the hierarchy. These data suggest that in the wild, C. atys has a matrilineal social structure but rank becomes individualistic in captivity.

Like most cercopithecines, Cercocebus mangabeys are female philopatric, with males emigrating to other groups (Range and Noë, 2002; Range, 2004). Male members of the Taï populations of C. atys can be either full-time or part-time group residents.

Researchers have also reported solitary males in both C. atys and C. torquatus (Mitani,

1989; Range and Noë, 2002). Data are not available as to the success of this part-time or peripheral mating strategy, but C. atys females were able to differentiate between the vocalizations of group male and non-group male calls indicating a possible reaction to the threat of infanticide by unfamiliar males (Range, 2004). Paternity studies in a captive group of C. atys found that male dominance rank usually predicts reproductive success; however, females do not have offspring with the same males from year to year

(Gust et al., 1998). This may reflect an interest among females in different males as a means of infanticide avoidance.

More is known about the social behavior of mandrills from semi-captive and wild studies. Mandrills and drills exhibit a diversity of social organizations including multimale-multifemale groups, groups of females and offspring, and one male groups

(Gartlan, 1970; Hoshino et al., 1984; Harrison, 1988; Setchell, 2005). In Lopé, Gabon, mandrills live in huge hordes of up to 800 individuals composed of females and dependant offspring (Abernethy et al., 2002).

The majority of research on mandrills and drills focuses on the evolutionary

importance of the secondary sexual characteristics of males, sexual selection, and mating strategies. Males form linear dominance hierarchies but tend to avoid direct aggressive contact (Setchell and Wickings, 2005). However, they go through intense competitions and fights during mating season for access to females (Jolly, 2007). The coloration of males serves as a badge of status to other males as a measure fighting abilities and rank (Setchell and Wickings, 2005; Marty et al., 2009). It was also shown that male reproductive success correlates with dominance and coloration, and males

tend to preferentially mate guard higher ranking females (Setchell and Wickings, 2006).

Jolly (2007) proposed a hypothetical scenario for the socioecological evolution of Mandrillus and Cercocebus related to their niche of foraging from the forest floor. He suggests that mandrill social behavior represents an extreme on a continuum of male residency and mating patterns beginning with C. atys. Because these genera feed on slowly accumulating resources, “The large home range of Cercocebus troops, the even larger range of mandrill foraging groups, and the fact that females and juveniles travel the circuit as a single, large party enable each area’s resources to recover to a harvestable level between visits” (Jolly, 2007:245). Mandrill males spend most of their time separate from the group. Males benefit from occupying smaller home ranges than the females, and therefore, males can conserve their energy for mating and maintaining their energetically expensive secondary sexual characteristics (Setchell and Wickings,

2005). The presence of this “resident/non-resident male” mating strategy within other

members of the clade is unknown, but sightings of solitary males among C. torquatus

suggest that it may characterize other Cercocebus species.

1.4 Cercocebus-Mandrillus Morphology and Hard-object Feeding Adaptations

Since the reclassification of mangabeys, researchers have been examining

Cercocebus and Mandrillus morphology for characteristics that unite these genera to the

exclusion of Lophocebus. Many of the cranio-dental and postcranial features found

among Cercocebus and Mandrillus species are functionally related to their terrestrial,

hard-object feeding strategy (Fleagle and McGraw, 1999, 2002). More specifically, the

complex of osteological features found in Cercocebus and Mandrillus are proposed as an

adaptation that allows them to glean hard nuts and seeds from the forest floor that are

available year-round and are inaccessible to other sympatric primates.

Most descriptions of mandrill and mangabey tooth and jaw morphology (in both

Cercocebus and Lophocebus) stress that they possess adaptations related to the processing of hard-object foods. Specifically, they have been described as having thick dental enamel, powerful jaws, and a facial configuration that enables them to produce large occlusal forces (Hylander, 1975; Kay, 1981; Shellis and Hiiemae, 1986; Fleagle and

McGraw, 1999, 2002; Singleton, 2002; Daegling and McGraw, 2007; McGraw et al.,

2012). Both Lophocebus and Cercocebus mangabeys have some of the thickest dental

enamel of all extant primates (McGraw et al., 2012). C. torquatus, in particular, was

shown to have the thickest enamel of the Cercocebus species analyzed.

Cercocebus, Mandrillus, and Lophocebus also have exceptionally large incisors

relative to other cercopithecid genera (Fleagle and McGraw, 1999, 2002; Shellis and

Hiiemae, 1986). As noted by Swindler (2002), “The endurance of a tooth can be

extended by having thicker enamel or increasing the size of the tooth” (17). Larger incisors and premolars are more resistant to wear than smaller incisors and are often associated with tough or hard foods that require processing before movement to the posterior teeth.

Based on their dentition, Kay (1981) classified mangabeys as “sclerocarpic

harvesters” similar to the New World genus Chiropotes (saki monkeys). Chiropotes use their incisors and canines to puncture unripe fruit husks and access nutritious seeds

(Kinzey and Norconk, 1990). Field studies indicate that both mangabey genera exploit obdurate foods. For example, L. albigena populations in Kibale National Park, Uganda, switch to eating bark and seeds during periods of fruit scarcity which were presumed to have high hardness values (Lambert et al., 2004). Sympatric populations of L. albigena and C. agilis were both observed eating seeds and nuts (Shah, 2003).

It is now recognized, however, that the cranio-dental similarities among

Lophocebus and the members of the Cercocebus-Mandrillus clade are due to convergence and homoplasy (Collard and O’Higgins, 2001; Collard and Wood, 2001;

Lockwood and Fleagle, 1999). Homoplastic characters are similarities between taxa that are not from a common ancestor (Lockwood and Fleagle, 1999). Cladograms created from masticatory characters among papionins consistently revealed incongruent

relationships compared to the established molecular cladograms (Collard and Wood,

2001). This suggests that both groups of mangabeys developed adaptations to hard-

object feeding (such as thick enamel, powerful jaws, enlarged incisors) independently.

However, Cercocebus and Mandrillus also have larger premolars than Lophocebus which

may indicate differences in how these monkeys process and use obdurate foods.

Indeed, Daegling and McGraw (2007) suggest that Cercocebus and Lophocebus

differ in the hardness of foods eaten and the method of mastication of these foods.

Compared to Lophocebus, Cercocebus and Mandrillus have enlarged premolars that exhibit extreme wear (Fleagle and McGraw, 1999, 2002; Figure 1.6). These molarized premolars aid in “frequent and powerful crushing by the postcanine dentition of hard nuts and seeds gleaned from the forest floor” (Daegling and McGraw 2007:50).

Lophocebus has smaller posterior dentition compared to both Cercocebus and the basal papionin, Macaca (Fleagle and McGraw, 1999, 2001). Lophocebus species are not believed to be capable of producing a strong crushing force with their posterior teeth like the Cercocebus species.

Studies of the feeding behavior in several mangabey species support the hypothesis of Daegling and McGraw (2007) that Cercocebus and Lophocebus process obdurate foods differently. In her comparison of the feeding ecology of C. agilis and L. albigena, Shah (2003) noted that the masticatory behavior of C. agilis was characterized by postcanine crushing more often than L. albigena. Additionally, “agile mangabeys crunched open much harder seeds than grey-cheeked [Lophocebus] mangabeys…. Agile

mangabeys often ate very old hard seeds… which they found on the forest floor…”

(Shah, 2003:41). McGraw et al. (2011) conducted the first study to directly test the

relationship between premolar expansion and durophagy among Cercocebus. They

identified what dental regions were used to process different food items in C. atys at Taï

National Park. Although incisal processing and mastication were the dominant actions,

McGraw et al. found that C. atys uses postcanine crushing behaviors to eat two of the hardest foods found in Taï, S. gabonensis and Coula edulis. Indeed, S. gabonensis is the most commonly eaten food among Taï mangabeys.

Overall, the masticatory complex of Cercocebus and Mandrillus has multiple adaptations for processing hard-object foods. The large incisors of Cercocebus are used to pierce tough fruit skins and the enlarged premolars, unique to this clade, indicate that these species use them as tools to crack open and crush hard-food objects. Even the earliest potential representative of the Cercocebus genus, Procercocebus antiquus, displays enlarged premolars compared to Parapapio suggesting an early shift toward hard-object feeding and postcanine crushing (Gilbert, 2007). These dental adaptations are necessary to initiate cracks in highly fracture resistant foods and also to ensure a long tooth life when relying on durophagous foods.

Cercocebus and Mandrillus also share a suite of postcranial characteristics, to the exclusion of Lophocebus, that aid in the acquisition of nuts and seeds from the forest floor and vertical climbing to access fruits. “The features shared by Cercocebus and

Mandrillus are functionally related to specific feeding and locomotor behaviors that

include aggressive manual foraging, the processing of hard-object foods, and the

climbing of vertical trunks” (Fleagle and McGraw 2002:267).

The forelimbs of Cercocebus and Mandrillus appear adapted for habitual

pronation/supination and flexion/extension movements (Fleagle and McGraw, 1999,

2002). The humerus features an expanded deltoid tuberosity, broad brachialis flange,

and proximally extended and laterally widened supinator crests (Figure 1.7). The

forelimb also has pronounced crest development that indicates prominent wrist or digit

flexor musculature. These characteristics allow for extensive manual and forelimb

dexterity that would be required to obtain seeds and nuts hidden on the forest floor and

also to forage for terrestrial herbaceous vegetation and invertebrates (Fleagle and

McGraw, 1999; Fleagle and McGraw, 2002). Evidence has shown that during foraging,

mandrills and C. atys obtain terrestrial food sources by aggressively pawing through the leaf litter and ripping apart logs for arthropods and mushrooms (Hoshino, 1985;

McGraw, 1996a; McGraw et al., 2011). C. sanjei has also been reported to dig into the

forest floor in search of tubers and Parinari excelsa nuts (Wieczkowski and Ehardt,

2009).

Not only is this clade adapted for terrestrial foraging, but its members also have scapular, pelvic, and lower limb characteristics associated with vertical climbing (Fleagle and McGraw, 1999, 2002). Cercocebus and Mandrillus possess a short and deep scapula, which increases the lever arm of teres major, an extensor of the humerus.

These features are found in species that use vertical climbing on tree trunks.

Furthermore, “…it seems likely that vertical climbing up tree trunks could select for a

robust ilium, a relatively more prominent medial patellar margin and a more rounded

tibial shaft” (Fleagle and McGraw 2002:280). Altogether, Cercocebus and Mandrillus

have skeletal features designed for extensive forelimb movements and vertical climbing

up large tree trunks. This foraging niche is considered a key adaptation of this clade that

impacts not only locomotion but also ranging and grouping patterns.

1.5 Cercocebus-Mandrillus Biogeography and Evolution

Researchers have tried to elucidate the evolutionary history and radiation of the

Cercocebus-Mandrillus clade by comparing the distribution of morphological

characteristics with the biogeographical distribution of each clade member (Dobroruka

and Baladec, 1966; McGraw and Fleagle, 2006; Gilbert, 2007). McGraw and Fleagle

(2006) identified a morphocline in several facial characteristics among Cercocebus and

mandrills. They found that C. torquatus, out of all Cercocebus species, most closely resembled Mandrillus in the degree of paranasal ridging and shallow suborbital fossae on the crania. C. agilis most closely resembled Lophocebus in its deep maxillary fossae

and weakly developed nasal ridging (McGraw and Fleagle, 2006). These cranial data fit

with the proposed dispersal route from central to eastern and western Africa of this

clade (Dobroruka and Baladec, 1966; Grubb 1978, 1982).

At one stage in their history… the mangabey (C. agilis) dispersed from Central to West Africa, forming presumably continuous populations across the continent… C. atys differentiated when these continuous distributions were interrupted. Subsequently… the westernmost species gave rise to eastward dispersing animals, C. torquatus (dispersing down the coast to Gabon). The discreteness of these species was emphasized once again by a break in distributions, the Volta River and Dahomey gap for Cercocebus. Intermediate populations between C.

atys and C. torquatus, assigned subspecifically to the more western and ancestral species… as C. a. lunulatus… replace the nominate races in Ivory Coast and Ghana (Grubb 1978:544-545; McGraw and Fleagle, 2006; Figure 1.8).

The morphocline in cranial characteristics, as well as the proposed biogeographic history of this clade, led to the hypothesis that C. torquatus is the sister taxon to mandrills and drills and that C. agilis represents the ancestral Cercocebus population

(McGraw and Fleagle, 2006). C. torquatus and Mandrillus are similar in maxillary fossa depth, nasal ridge development, and temporal line morphology (McGraw and Fleagle,

2006; Gilbert, 2007). They also are sympatric, or were sympatric in the past, in much of west Central Africa. C. torquatus males feature extremely large canines, a condition seen among male Mandrillus species (McGraw and Fleagle, 2006). Furthermore, mandrills and C. torquatus have even been known to hybridize in captivity, and they share strains of the SIV virus in the wild (Telfer et al., 2003; McGraw and Fleagle, 2006).

This suggests a close phylogenetic relationship between these Mandrillus and C. torquatus.

The evolutionary history of Mandrillus is less complex than that of Cercocebus.

Grubb (1973) proposes that the differences in phenotypes among mandrills and drills may be the result of independent evolution in isolated geographical regions.

Similarly, differences among the Cercocebus species are likely the result of local adaptation and isolation. If this adaptation involved an increased dependence on terrestrial food items, an increase in degree of terrestriality would be expected in the direction of the divergence of Cercocebus. The available data only somewhat support this trend (with C. agilis displaying the least terrestrial behavior, excluding the new

study from Bai Hoku, Cameroon). Thus, according to this divergence scenario, C.

torquatus should be the most terrestrial of all the Cercocebus species, but C. atys is the

most terrestrial of the Cercocebus species studied. However, we are lacking clear

information on the degree of terrestriality of C. torquatus throughout its distribution

and in areas where it is not sympatric with Mandrillus.

A re-evaluation of Papionin fossil evidence suggests that C. torquatus retains the most morphological similarities with the earliest representative of the Cercocebus taxa,

Procercocebus antiquus (Gilbert, 2007). Procercocebus from Taung, South Africa dates back to 1.5 – 2 million years ago. Gilbert argues that, “Rather than radiating east and west from the low latitudes of central Africa, a scenario must be considered where the genus arose in either western or southern Africa and dispersed north, south, and east from these regions occupied by P. antiquus and C. torquatus” (2007:85). Therefore, researchers disagree as to the status of C. torquatus within the Cercocebus-Mandrillus clade. Either C. torquatus is the most derived of the Cercocebus species, and the sister taxon to Mandrillus, or it is the most primitive of the Cercocebus species. McGraw and

Fleagle (2006) also note that the cranial evidence supporting the sister taxon hypothesis has not been substantiated by molecular studies.

The Cercocebus-Mandrillus clade has been defined both morphologically and behaviorally by its unique foraging strategy, and it results in many similarities between these two genera. The differences in Cercocebus and Mandrillus feeding, ranging, and grouping behaviors may be related to their varying reliance on and adaptation to terrestriality. Furthermore, each group has followed its own evolutionary trajectory due

to differences in local environments. The collection of more data on both of these genera will help further clarify their relationships.

1.6 Cercocebus-Mandrillus: The impact of obdurate feeding?

Despite the growing database of information on these species, Cercocebus and

Mandrillus remain some of the least studied primates. Therefore, researchers are left

with questions regarding the adaptations that characterize this clade. Assuming the

importance of hard-object feeding to Cercocebus and Mandrillus, the critical data for understanding the observed variability in the feeding and behavioral ecology of this clade are the distribution, availability, and reliance on hard foods. It is also important to understand how they obtain and process obdurate foods and the impact on locomotion and substrate use. The positional behaviors associated with foraging and processing food items have only been quantified for one member of this clade, C. atys (McGraw,

1996a, 1998a, 1998b; McGraw et al., 2011). Therefore, any information can increase our understanding of these monkeys.

The terrestrial, hard-object feeding niche has also been associated with distinctive grouping behaviors in the Cercocebus-Mandrillus clade. Flexibility in foraging behaviors may enable Cercocebus to maintain group sizes and dietary quality during periods of food scarcity or maximize group size during periods of food superabundance.

Current evidence suggests that these genera are highly adaptable and respond in a variety of ways to different environments. However, we lack information on the relationship between subgrouping and/or supergrouping to food availability and seasonality.

1.7 Research Questions

Although the available morphological evidence suggests that Cercocebus and

Mandrillus are adapted to hard-object feeding, the attempts to explain the evolution of

this foraging niche suffer from a paucity of ecological and behavioral data on the lesser

known Cercocebus species and drills (McGraw and Fleagle, 2006). Because of its

similarity to the earliest members of the genus and its location in west Central Africa, C.

torquatus occupies a pivotal position for understanding the behavioral and morphological adaptations associated with hard-object foraging. In order to address the

morphological and behavioral impact of durophagy on the Cercocebus-Mandrillus clade,

hypotheses based on the following questions were tested on a group of C. torquatus

from Sette Cama, Gabon: 1) What is the diet of C. torquatus? 2) What are the

mechanical properties of the foods they eat? 3) What is the spatio-temporal

distribution of foods? 4) Does the distribution of obdurate foods impact ranging

patterns of C. torquatus? 5) How does C. torquatus positional behavior compare to

other Cercocebus species and Lophocebus? and 6) Is C. torquatus the most likely sister

taxon to Mandrillus?

Researchers are now beginning to understand the importance of hard-object

foods to this clade and its evolutionary trajectory. The goal of this study is to combine

multiple lines of information to understand the place of C. torquatus among the

Cercocebus-Mandrillus clade and the impact of durophagy on their behavioral ecology.

1.8 Organization of dissertation

The dissertation is divided into seven chapters. Five of the chapters each cover a

separate aspect of the study. Because the topics discussed are disparate, yet

interconnected, each chapter features a brief literature review on the subject followed

by the presentation of the results of that portion of the study. The goal of this project

was to incorporate multiple elements in order to understand both the evolutionary

history and modern behavioral ecology of red-capped mangabeys. Each of these parts

will be synthesized in the final, concluding chapter.

Chapter one introduced Cercocebus torquatus and summarized the current

knowledge of both this species and its fellow clade members. I also discussed some of

the larger issues in understanding the evolution and adaptation of these monkeys

including the taxonomic and classification revisions, the dental and skeletal features

that characterize this clade, and the importance of obdurate feeding.

Chapter two provides an overview of the study site of the Sentier Nature forest

in Sette Cama, Gabon, and the methods used for basic behavioral data collection. The

maintenance activity patterns, height use, and habitat use are presented along with a

phenological and vegetation profile of the Sentier Nature forest. I also present the

results of the vegetation and phenology surveys and compare the seasonal trends of

Sentier Nature to several other West African field sites.

Chapter three presents feeding data and the role of obdurate feeding in the C. torquatus diet. This section also includes data on the material properties of C. torquatus

foods and addresses the suggestion that the morphological adaptations of the

Cercocebus genus are directly related to fallback feeding.

Chapter four discusses the ranging behavior of C. torquatus and compares patterns of ranging over each month of the study period. I also discuss the relationship between ranging and the spatio-temporal availability of key C. torquatus foods.

Chapters five and six cover the positional behavior of C. torquatus compared to its fellow clade members and Lophocebus species. These data are necessary to understand how C. torquatus acquires its foods and utilizes its environment. More specifically, chapter five presents the locomotor behaviors of C. torquatus and compares locomotion across age, sex, habitat, and substrate types. These data are also used to examine differences in terrestrial and semi-terrestrial primates.

Chapter six discusses the postural behaviors of red-capped mangabeys. The role of postural activities in shaping primate lives and adaptations is often underappreciated.

Postural behaviors occur during feeding, foraging, and resting and allow a primate to more efficiently use its environment.

The last chapter serves as a review and integration of the behavioral and morphological data collected in order to assess the phylogenetic position and adaptive radiation of C. torquatus and the members of the Cercocebus-Mandrillus clade. I also discuss some future directions for the study of C. torquatus and the adaptations of its clade.

Figure 1.1: An illustration of Cercocebus torquatus. (Courtesy of Stephen Nash).

Figure 1.2: The distribution of C. torquatus in west central Africa. (Map by Richard Moussopo).

Figure 1.3: The current papionin phylogenetic tree. (Reprinted with permission from Gilbert et al., 2009).

Figure 1.4: Distribution of the Cercocebus species in Africa. (From McGraw and Fleagle, 2006).

Figure 1.5: The distribution of Mandrillus in Africa. (From McGraw and Fleagle, 2006).

Species Fruit Fruit Seeds Structural1 Flowers/ Animal Other Site2 + Leaves Seeds C. agilis -- 75 -- 16 -- 5 4 Mondika, CAR C. agilis -- 67.6 -- 20.8 -- 6.2 4.5 Bai Hokou, CAR

C. atys Taï, Côte d’Ivoire C. galeritus -- 76 -- 12 5 2 5 Tana River, Kenya

C. galeritus 34 -- 42 7 5 11 -- Tana River, Kenya C. galeritus 44 -- 32 ------Tana River, Kenya C. sanjei -- 47 -- 15 9 29 -- Udzungwa, Tanzania C. torquatus 60 -- 20 ------Campo, Cameroon M. 58 -- -- 16 -- 26 -- Bioko, leucophaeus Equatorial Guinea M. sphinx 84 ------8 -- Campo, Cameroon M. sphinx 47 -- 34 -- 7 5 -- Lope, Gabon

Table 1.1: The diets of known species of Cercocebus and Mandrillus.

1This category includes bark, twigs, pith, and sap

2Sources in order by species: Shah, 2003; Devreese, 2010; McGraw et al., 2011; Homewood, 1976; Kinnaird, 1990; Wieczkowski and Butynski, in press; Mwawende, 2009; Mitani, 1991; Swedell, 2011; Hoshino, 1985; Tutin et al., 1997.

Species Terrestriality % Seeds in Site Source Diet C. agilis 22 -- Mondika, CAR Shah, 2003 C. agilis 72 -- Bai Hoku, CAR Devreese, 2010 C. atys 67.24 60 Taï, Côte McGraw, 1996a d’Ivoire C. galeritus 51 42 Tana River, Homewood, 1976 Kenya C. torquatus1 30 202 Korup, Astaras et al., 2011; Cameroon Mitani, 1989 M. leucophaeus1 62 -- Korup, Astaras et al., 2011 Cameroon

Table 1.2: The overall amount of time spent on the ground for several Cercocebus species and drills. 1Data represent the percentage of observations at 3 meters and below. 2The estimate of seeds in diet is from another site in Cameroon.

Species Group Size Day Range Home Range Site Source (meters) (hectares) C. agilis 21-22 1155 303 Mondika, Shah, 2003 CAR C. agilis 230 3086 1000 Bai Hokou, Devreese, 2010 CAR C. atys 100+ N/A 700-800 Taï, Côte McGraw et al., d’Ivoire 2011 C. galeritus 36 1165 17 Tana River, Homewood, Kenya 1976; Kinnaird, 1990 C. galeritus 17 1184 19 Tana River, Kinnaird, 1990 Kenya C. galeritus 50 1395 47 Tana River, Wieczkowski, Kenya 2005 C. sanjei 62 1760 300 Udzungwa, Mwawende, Tanzania 2009 C. torquatus 70+ 1000-1100 200-300 Sette Cama, Cooke and Gabon McGraw, 2007 C. torquatus 25 N/A 250 Campo, Mitani, 1989, Cameroon 1991 M. 52.3 N/A N/A Bioko, Astaras et al., leucophaeus Equatorial 2008 Guinea M. sphinx 15-95 N/A 500-2800 Campo, Hoshino, 1985 Cameroon M. sphinx 600-800 N/A 18,200 Lope, Gabon Abernethy et al., 2002; White et al., 2010

Table 1.3: The group sizes, day ranges (in meters), and home ranges (in hectares) for Cercocebus and Mandrillus species.

Figure 1.6: The molarized premolars of Cercocebus and Mandrillus compared to Lophocebus and Papio. (From McGraw and Fleagle, 2002).

Mandrillus Papio

Figure 1.7: The humerii of several Papionins. Note the enlarged deltoid plane of Mandrillus and Cercocebus compared to Lophocebus and Papio. (From Fleagle and McGraw, 2002).

Figure 1.8: The proposed dispersal route and evolutionary trajectory for Cercocebus species. (From McGraw and Fleagle, 2006).

Chapter Two: General Methods and Basic Data

2.1 Introduction

This chapter provides background on the study site, methodology, and some

basic behavioral data for C. torquatus in Sette Cama, Gabon. The methods for the behavioral and locomotor sections of this study are outlined, and baseline behavioral data such as activity budget, strata use, and habitat use are discussed. Both qualitative and quantitative descriptions of the forest composition and architecture for each of the microhabitats in Sette Cama are presented. Data are also given on the spatio-temporal

availability of some important C. torquatus foods. These data will be used in the

upcoming chapters discussing diet and food hardness, ranging patterns, and the

influence of habitat on positional behavior. Finally, C. torquatus are compared to other

Cercocebus species in order to gain an understanding of the behavioral diversity within this genus.

2.2 Background

Activity patterns among primates

When studying primates, it is necessary to understand the most basic aspects of their lives including activity patterns, diet, strata use, and ranging. Activity patterns include how a primate spends it day (or night) and divides its time among activities such as feeding, traveling, and social behaviors (Fleagle, 1999). Activity patterns are highly

42 dependent upon diet and habitat structure (Altmann, 1974). The potential energy provided by foods and food location influences the amount of time devoted to and available for foraging. This, in turn, impacts the energy available for other activities such as grooming or mating (Kinnaird, 1990). For example, the primarily folivorous howler monkeys (Alouatta spp) devote most of their days to resting rather than traveling because they occupy small home ranges and need time to digest their low quality diet

(Milton, 1980).

Group size can also impact activity patterns. In general, as group size increases, home range size also expands because more area is needed to ensure an adequate food supply for all group members (Chapman, 1990; Terborgh, 1983; Wrangham et al., 1993;

Chapman et al., 1995; Janson and Goldsmith, 1995). A larger home range entails more travel time, either through increased daily path lengths or an increase in the overall percentage of time the group devotes to traveling. Wrangham et al. (1993) found a positive correlation between group size and day range length among both primates and carnivores. Among most frugivorous primates, daily path ranges increase with group size because of the increase in foraging costs through indirect feeding competition

(Janson and Goldsmith, 1995).

Habitat use among primates

Primates face competition from other sympatric species for access to space and resources. Primate species usually occupy different niches to minimize the negative effects of species coexistence. Aspects of niche separation between primate species can include dietary variations or differences in activity patterning and substrate use

(Schreler, 2009). The use of different forest heights, or strata, by various primates is

one of the most common adaptations associated with niche partitioning to avoid

competition (Fleagle and Mittermeier, 1980; McGraw, 1996a; Schreler et al., 2009). For

example, McGraw (1996) found that the six sympatric monkey species in Taï National

Park, Côte d’Ivoire tended to sort themselves vertically and used different forest heights

during different maintenance activities. In general, C. polykomos was found at the

greatest heights followed by C. badius, while C. atys was consistently located on the

forest floor. The guenons at Taï also partitioned themselves by both strata and diet

(Buzzard, 2006).

A species may also exhibit site specific diversity in its strata use depending upon

sympatric species present or variations in resources. Association with other primate

species often results in one of the species using levels of the forest not typically

frequented. Goeldi’s monkeys (Callimico goeldii) in Bolivia were observed more often in the lower and middle forest canopy when in association with Saguinus groups (Porter,

2001). Several populations of bearded Saki monkeys (Chiropotes satanas utahicki) occupied different forest levels at different sites depending on both the sympatric species present and the availability of alternative food sources (Bobadilla and Ferrari,

2000). The ability to exploit different levels of the forest enables a primate to be highly adaptable to a myriad of circumstances.

Cercocebus mangabeys are characterized as semi-terrestrial, frugivorous species

that prefer riverine and swamp habitats (Kingdon, 1997; Fleagle, 1999). They are able to

occupy areas of their habitats unavailable to other primate species such thorny

brambles and flooded areas as well as all the layers of the tree canopy. This gives

Cercocebus mangabeys an advantage over other primate species that are more limited

by forest strata. Because of their flexibility and adaptability in habitat use, Cercocebus

species should show site specific differences in strata use. Strata use is influenced by

food availability and abundance and the presence of other competing species. For

example, sooty mangabeys in the Taï National Forest, Côte d’Ivoire, share their habitat

with six other cercopithecoids. Sooty mangabeys are the most terrestrial of all

Cercocebus species, and they regularly exploit seeds and insects located on the ground.

Forest composition: Vegetation surveys and phenology

As mentioned previously, diet is a primary influence on primate behavioral ecology. Diet impacts how a primate divides its time, how and where it moves, and its type of social grouping. Therefore, knowing the distribution and availability of foods eaten by a primate species is critical to understanding how it adapts to its environment.

The majority of primates are found in tropical forests because of the abundance of

fruiting trees and other food sources (Fleagle, 1999). Tropical forests are highly

dynamic, and the production and availability of fruits, flowers, and young leaves in

tropical forests varies seasonally (Tutin and Fernandez, 1993; Newbery et al., 1998;

Tutin et al., 1997; van Schaik and Pfannes, 2005). Therefore, primates must behaviorally

adjust to fluctuating resources and the cyclical nature of tropical forest productivity.

Multiple factors influence plant reproductive cycles including rainfall, temperature, intensity of solar radiation, and altitude. Peak fruiting is often assumed to occur in the wet season in tropical climates, however, this trend does not hold up for all

habitat types (van Schaik and Pfannes, 2005). For example, in Kibale National Park,

Uganda, fruiting was highest at the beginning of the dry season (Chapman et al., 1999).

Fruit production can potentially vary within different areas of a forest and among

species within the same forest (Newbery et al., 1998; Chapman et al., 1999). The

quantity and nutritive value of fruits may also differ within a single tree (Houle et al.,

2007). Therefore, it is important to know the fruiting, flowering, and leafing patterns of

a primate species’ particular habitat as well as the distribution of major vegetation

types. The two most common methods for estimating a forest’s composition and

productivity are vegetation surveys and phenological monitoring (Chapman et al., 1994).

Vegetation surveys provide a snapshot of a forest’s composition. Several

measures can inform researchers of a forest’s potential productivity and biomass

including tree species density (Chapman et al., 1994) and fruit tree diameter at breast

height (DBH). Research suggests that DBH is an accurate estimator of fruit biomass,

with larger trees producing more fruit (Chapman et al., 1992; Chapman et al., 1994;

Leighton and Leighton, 1982; Wieczkowski, 2005).

Phenology studies are the most standard method for estimating seasonal variations in food availability (Chapman et al., 1994). In a phenology study, trees are monitored monthly and the amount of young and mature leaves, ripe and immature fruits, and flowers are measured on scale of percent abundance from zero to one hundred. Ideally, a forest’s phenology is recorded over a period of many years to gauge trends in food and fruit production. Nevertheless, shorter phenology studies combined

with socio-ecological data can be informative of the contemporaneous effects of food

availability.

Although phenology is site-specific, data from similar forest types can help

elucidate some patterns of food availability among geographic regions. Long term

phenology data are available for at least one site in Gabon (Tutin and Fernandez, 1993;

Tutin et al., 1997). Researchers at Lopé National Park, located north of the equator in

central Gabon, monitored the fruiting and flowering patterns of trees over a period of

ten years. The forest in Lopé is likely similar to the terra firme habitat of the site of this

study, the Sentier Nature forest in Sette Cama, Gabon. Both forests are characterized

by an herbaceous understory and many species of the Marantaceae family. Indeed,

many of the tree and plant species in Sentier Nature were identified using a plant and

tree guide from Lopé (White and Abernethy, 1997). Both areas feature a three-month

dry season from June – August with temperature lows during this time. Temperatures

are relatively stable year-round in Lopé with daytime highs between 27 and 31˚ C and night-time lows of 20 - 22˚ C (White and Abernethy, 1997).

In Lopé, fruit was scarce during the dry season and crop failures sometimes led

to food shortages for up to eight months (Tutin et al., 1997). “The year at Lopé can thus be divided into three periods with respect to the availability of ripe fruit: June – August

when it is consistently scarce, October – December when it is always abundant, and

February – May when it is usually abundant…” (Tutin and White, 1998). Tutin and colleagues also observed inter-annual variation in crop production, possibly because of

failure to meet the minimum temperature of 19˚C required for many trees to start

flowering (Tutin and Fernandez, 1993).

2.3 Research Questions

In this chapter, I present information on the project study site and the C.

torquatus group. I also include baseline behavioral data such as activity patterns, height use, group spread, and habitat use for C. torquatus. These data are then compared to the spatio-temporal availability of foods. The goal of this chapter is to answer the following questions:

1. How does C. torquatus compare to other members of its genus in its use of time,

space, and habitat types?

2. How are C. torquatus behaviors impacted by the spatio-temporal availability of

foods?

3. How does the productivity and vegetation of the Sentier Nature forest of Sette

Cama, Gabon compare to other sites?

2.4 Methods

Study site

The Sentier Nature forest (2˚29’30” to 2˚30’58.7”S and 9˚43’24.3”E to

9˚44’56.2”E) is a protected area located in the Gamba Park Complex in southwestern

Gabon (Figure 2.1). The Gamba Complex encompasses two national parks, Loango

(1,500 km2) and Moukalaba-Doudou (5,000 km2). Sette Cama is the nearest village to

the Sentier Nature forest. Sette Cama lies on the southern edge of Loango National

Park. Approximately 132 people inhabit Sette Cama (Thibault 2001), and hunting is

purportedly contained to a forested area near the village. The WWF maintains a

research facility at the Sentier Nature forest that was constructed in 1997. The facility

houses researchers and employees of the Brigade des Eaux et Forêts. Two tourist lodges, Sette Cama Safaris and Camp Missala, separate the Sentier Nature forest from

the village and Loango Park. Therefore, the Sentier Nature forest represents a semi-

isolated habitat outside of Loango Park. The area of the Sentier Nature forest is 254 ha.

The available temperature and rainfall data are for Gamba, a coastal town

located 40 km south of Sette Cama. The annual temperature is 24˚-28˚ C, and there are

two dry seasons from June to September and January to February (Lee et al., 2006).

Annual rainfall is 2093 mm (Lee et al., 2006).

The forests of this region of Gabon are broadly classified as lowland, evergreen

forest (Campbell et al., 2006). Sentier Nature is secondary forest that features extensive

undergrowth and areas of thickets with dense liana growth. The canopy cover shifts

from closed to broken to open coverage as the forest becomes more coastal. Like

Loango Park, the Sentier Nature forest features a mosaic of habitats. However, these

habitats are not evenly distributed. The forest was divided into 3 zones based on

habitat type: beach forest, terra firme forest, and mangrove forest. Figure 2.2

illustrates the limits of each habitat type in Sentier Nature. The following is a brief

description of each habitat type:

Mangrove Habitat (Figures 2.3 and 2.4): The forest from Ndogou Lagoon to the

non-flooded terra firme forest. This region is typified by tree root outgrowths and

thickets near the lagoon to large tree stands less than 7 meters apart closer to the main

trail. During the rainy season, this area becomes flooded and is nearly impassible by

foot. The canopy is closed to semi-closed, and there are many lianas and fallen trees.

The mangrove forest also includes several swamp zones that are permanently flooded

and filled with thorny undergrowth.

Terra Firme Habitat (Figures 2.5 and 2.6): The terra firme zone is the habitat

between the coastal forest and flooded forest areas next to the swamp and mangrove

forest. The majority of the forest is terra firme forest. The undergrowth is thick and

there is less than 5 meters between many of the trees. This area features many trees

but also significant liana growth. The canopy varies from closed to open.

Beach Habitat (2.7 and 2.8): This is the forest located between the Atlantic

Ocean and terra firme forest. The area features open spaces of grassland and expanses

of Chrysobalanus icacao shrubs making up the understory. The soil is sandy and the

canopy is open. The trees are widely spaced, and there are a significant amount of tree

falls due to elephant traffic.

Loango National Park and the Sentier Nature forest contain an exceptional range

of wildlife including hippopotamuses, marine turtles, and several species of duiker.

These forests also have one of the highest densities of forest elephants in Africa

(Morgan, 2007). Several primates listed as vulnerable or endangered by the IUCN occupy the area including Gorilla gorilla and Pan troglodytes. The other primate species found in the Gamba Complex are Cercocebus torquatus, Cercopithecus nictitans, C. cephus, and Lophocebus albigena. However, the only primates observed in the Sentier

Nature forest during this study were C. torquatus, C. nictitans, C. cephus, and P.

troglodytes. C. torquatus were observed foraging for fruits with several other non- primate species including sitatungas, two species of duiker, and the water chevrotain.

The potential C. torquatus predators in Sentier Nature are leopards, crowned-hawk eagles, and pythons; however, traces of these species were only observed indirectly.

Three trails, cleared from pre-existing elephant trails, ran through each of the

major habitat types (mangrove forest, terra firme forest, and coastal forest) in a section

of the mangabey home range (Figure 2.9). The trails were mapped using a GPS and

marked every 100 m to facilitate tracking the C. torquatus group. The mangabey range

also included a swamp area filled with thorny thickets that was inaccessible year-round

(Figure 2.10). The park conservator did not give permission to cut new trails or use the

forest near the tourist lodges on either end of the Sentier Nature Forest boundaries.

Therefore, access to the entire mangabey home range was severely restricted by several

factors.

Study group

Data were collected on one group of red-capped mangabeys (Cercocebus

torquatus). Habituation of the study group began in February 2008. The habituation

period was interrupted by construction of a treehouse in the forest and the filming of a

documentary by the BBC during November 2008 – February 2009. Systematic

behavioral sampling began in May 2009 and continued until September 2009.

The C. torquatus group was composed of at least 70 individuals. The best

estimates of group count come from the occasions when the whole group was together

and crossing from one section of the forest to another. For example, on July 25, my

assistant and I counted 74 individuals. However, it was never possible to get an exact

count because of the lack of visibility in Sentier Nature and because of the frequent

subgrouping among C. torquatus. A year-long census of large mammals in Loango

National Park estimated that C. torquatus were found at a density of 15-17 individuals

per km2, the highest density for any of the large mammals surveyed (Morgan, 2007).

C. torquatus are notoriously difficult animals to study. Indeed, it was remarked,

“When disturbed, animals always took refuge in the swamp forests by escaping through the canopy, on the ground, or through the tangles of mangrove roots” (Jones and

Sabater Pi, 1968:108). The only other long-term study on C. torquatus, in Cameroon, also suffered from lack of visibility of animals and problems tracking study subjects

(Mitani, 1989). Range et al. (2007) had difficulties in identifying C. atys individuals because of their large group size and tendency to subgroup. Upon being startled, the initial reaction of C. torquatus in Sentier Nature was to run away on the ground or climb into the trees and find a place to hide. For the first five months of study, C. torquatus would hide behind mangrove roots and thickets and watch the researchers. This tendency to flee to the inaccessible swamp zone when startled continued throughout the study period to varying degrees. Shah (2003) observed a similar behavioral pattern among agile mangabeys in Mondika, Central African Republic. She noted that the mangabeys often employed the tactic of “…hiding silently and immobile in a viney tangle for hours on end… [often] when individual mangabeys felt ‘trapped’ by the observers during the habituation process” (108).

It is estimated that the group included at least five adult males, seven adult females, twenty-two subadults, and sixteen juveniles. This is based on the greatest number of individuals observed within each category during the group scans. Several infants were born into the group during the study period; females were observed with infants during each of the behavioral sampling months. One solitary male was seen in the study area, and he often was found peripheral to the group. The group had at least three males that gave the “whoop” long call (they would contact one another when the group was split).

Behavioral data

Data collection occurred in two phases: the habituation period from February

2008 – March 2009 and the period of systematic behavioral data collection from May –

September 2009. “Habituation is the process by which animals become accustomed to human presence and eventually accept a human observer as a neutral element in their environment” (Doran-Sheehy et al., 2007:1354). Habituation is usually considered a means to an end and is achieved when researchers can collect systematic focal data

(Williamson and Feistner, 2003; Doran-Sheehy et al., 2007). Different primate groups vary in the amount of time required for habituation from one month in most lemurs and several years to a decade for some great ape species (Williamson and Feistner, 2003).

Information about the habituation of Cercocebus mangabeys indicates that it takes at least three years for groups to be fully comfortable around researchers. Shah

(2003) spent three years habituating her group of agile mangabeys in Mondika, CAR.

Another study on agile mangabeys in Bai Hoku, CAR was conducted on a group

considered partially habituated (Devreese, 2010). This group had been studied since

2004. Some factors that may contribute to difficulty of habituating mangabeys include

their proclivity toward subgrouping, their dense, thick habitat, and large home ranges

(Williamson and Feistner, 2003). The lack of adequate habituation for the Sette Cama C.

torquatus study group definitely hampered efforts at data collection and contact time with the mangabeys.

During habituation, my assistants and I attempted to locate the mangabeys beginning at 7 A.M. We were in the forest at least five days each week. For every group encounter, I recorded the location, habitat type (beach, terra firme, mangrove), number of individuals sighted, height and activity of the first individual spotted, an approximate number of how many individuals were present, group composition (whole or subgroup), and any foods eaten. GPS points were also taken at 10 minute intervals during contact periods to estimate ranging patterns. Habituation levels were monitored with each encounter by noting the observer’s distance from the group and duration of contact. By the end of the study, this group of C. torquatus were approachable up to 10 meters but could still only be considered semi-habituated.

Systematic behavioral data were collected on the group of C. torquatus from

May 2009 to September 2009. Follows occurred five days a week (not always consecutive) and began at 7:00-7:15 AM and continued until 12:00 PM. We re-entered the forest at 2:30 PM until 5:30 PM because, typically, the mangabey group spent the mid-day hours in the inaccessible swamp zone. Our movements and time in the forest were limited by the presence of forest elephants (Loxodonta africana). The forest

elephants tended to remain in the thick forest until around 16:00 h when they moved to

the more coastal habitats (Morgan and Lee, 2007). Therefore, we could not use the

traditional methodology of locating the C. torquatus group each day using its resting

place from the previous night. We had to re-locate the group every day, which hindered

data collection and contact time with the mangabeys.

The original data collection plan was to take five minute group scans (Altmann,

1974) every 20 minutes and 10 minute focal scans (with instantaneous samples every

two minutes) between group scans (similar to Shah, 2003). However, visibility in Sentier

Nature was very poor because of the extensive lianas and undergrowth. Therefore, if no

focal individuals were available after the group scan, another group scan began after ten

minutes. This pattern was continued if no focal individuals were available.

The variables noted during each scan were derived from Shah (2003) and

McGraw (1996) in order to facilitate comparisons with C. agilis and C. atys. During each

group scan, for each individual seen, the data collected were: sex, age class (adult,

subadult, juvenile), activity, height (visually estimated in meters), positional behavior,

forest zone, and support size. Any polyspecific associations, habitat type (beach, terra

firme, mangrove) and group composition (whole group, subgroup) were noted for each

group scan. The sex of subadults and juveniles were not noted because of visibility

issues. The same data were collected during focal animal scans. The hardness value of

C. torquatus foods were also measured using Asker portable handheld durometers (see chapter 3).

The sexes and different age classes were identified using the following criteria:

Males have large body size, a continuous ischial callosity pad, are more thickset in the

chest area, and have stouter body proportions (Field, 2007; Figure 2.11). Females are

20% smaller than males, have separated ischial callosity pads, and most females were

either nursing or carrying infants which made them easier to identify (Figure 2.12).

Subadults tend to have a smaller body size than adults, the head is disproportionately

bigger than limbs and body size, vocalizations are higher pitched, and they display more curiosity and tend to hang around the edges of the group (Figure 2.13). Juveniles have the smallest body size besides infants (not pictured).

The maintenance activities recorded were: travel (TR), feed (FE), feed cheek- pouch (FECP), forage (FO), rest (R), and socio-sexual (SS) (Shah, 2003). Travel included movement from one area to another, both within and between trees. Feeding was the chewing and ingestion of food items or drinking water. Feeding also included the processing of food items with the hands, teeth, or lips (for example, opening the seed cover of old Sacoglottis gabonensis fruits with the posterior dentition or scraping the pulp from fruits with the incisors). Cheek-pouch feeding was used for when C. torquatus put foods into their cheek pouches or fed from foods stored in the cheek pouch from any posture. If C. torquatus was seen eating a fruit species far from any of that fruit trees, it was scored as cheek-pouch feeding. Foraging included searching the ground and trees for food items or rifling through the leaf litter to search for seeds. During feeding scans, the food species, part eaten, and ripeness (if applicable) was noted. FE,

FECP, and FO were combined for analysis because it was very difficult to observe C.

torquatus foraging because of their preference for areas with extensive undergrowth.

Rest included stationary behaviors such as sleeping or standing. The socio-sexual

category was used for vocalizations and interactions with conspecifics such as playing,

grooming, fighting, and mating.

For each scan the forest stratum was not recorded but instead the height in meters was estimated for each observation. The heights were grouped into height classes that include: 0 meters, 1-5 meters, 6-10 meters, 11-20 meters, 21-30 meters,

and 31+ meters. These categories roughly correspond to the ground, understory, lower

canopy, middle canopy, upper middle canopy, and emergent canopy layer.

In addition, the mangabey’s location within the tree was recorded to determine

how the different tree zones are used during positional behaviors (McGraw, 1996a).

The forest was broken down into 6 zones (Figure 2.14). The ground was delineated as

zone 0. Zone 1 included the tree trunk and any branches immediately adjacent to the

tree trunk. Zone 2 was the area between Zone 1 and the terminal branches of Zone 3.

Zone 4 is the uppermost layer of the tree. Zone 5 includes areas outside of the tree

such as lianas, tree falls, or small trees and shrubs.

During each positional behavior, the support size was also noted. Definitions of

support size are taken from Fleagle (1976) and McGraw (1996). Large supports, or

boughs, are tree trunks, tree limbs, lianas or fallen trees that are larger than 10 cm and

cannot be grasped by the hands or feet. Medium sized supports, or branches, are limbs

and lianas that can be grasped by the hands or feet. The smallest sized supports are

twigs, and they are found at the terminal end of branches and are less than 3 cm. Small

sized lianas were also included in the category of twigs.

Data were transcribed from notebooks into Microsoft Excel. Excel was used to

calculate basic statistics, and data were further analyzed using SPSS software.

Vegetation

Vegetation samples

In order to determine the densities and distributions of tree species in Sentier

Nature, 13- 100m x 10m vegetation transects were placed along the three main trails.

One transect was placed on the other side of the swamp zone that is only accessible by

boat (Figure 2.15). Each transect was spaced 200 m apart. We were denied permission

to paint trees or to cut new trails to access other parts of the forest not included in the

pre-existing elephant trails. A total of 1.3 ha were surveyed by the vegetation sampling.

More extensive vegetation surveys have been conducted in Loango National Park

(Campbell et al., 2006), and the goal of this small survey was to get a snapshot of the

composition of the Sentier Nature Forest.

All trees and lianas with stems located inside each transect were identified, the

DBH (diameter at breast height in cm) was measured using a DBH tape, and the height was estimated visually in meters. Species were only included if the DBH was greater than 10 cm. Each stem of multi-stemmed trees were measured and the average taken.

If a tree had buttressing at breast height, the measurement was taken immediately above the buttress. Dead trees and lianas were not included in the survey.

The tree and liana species were identified using field guides and local informants

(Raponda and Sillans, 1995; White and Abernethy, 1999). Any unknown species were

tagged, photographed, and leaf and bark samples were brought to the chief of Sette

Cama for identification. The chief provided the local Balumbu name, and then the

species was found from a list of common and scientific tree names compiled by the

agents of Eaux et Forêts (Table 2.1 lists some common local plants in Balumbu). Despite

this system, the names of several tree species were never identified.

Data are presented separately for each habitat type. The swamp zone plot was

lumped with the mangrove plots because of proximity and similarity in species

composition and forest architecture. The Shannon-Weaver Index was calculated for

each habitat type to measure the biodiversity of the Sentier Nature forest. Unknown

trees were not included for this anaylsis. The Kruskal-Wallis test was used to test for

differences in the median DBH by habitat type.

Phenology

Five individuals of the ten most commonly eaten fruit species by the mangabeys

were chosen for phenological monitoring. This was based on feeding observations from

February – December 2008. The five representatives of each tree species were chosen because they were frequently fed on by the mangabeys, or because they were near the

movements of the group. Each tree species was represented by a letter and a number

was given to each individual of a species (example: Manilkara tree= A, the first

Manilkara tree= A01). Trees were marked with flagging tape and the GPS location,

height, and DBH of each tree was noted. Table 2.2 lists all the species included in the

phenological monitoring and the height and DBH of each tree. Only one member of the

Pycnanthus angolensis species was monitored because there is only a single Pycnanthus

tree in the Sentier Nature forest. Figure 2.16 shows the location of the phenology trees

in the Sentier Nature forest. The majority of the trees were located near Ndogou

Lagoon.

Phenology data were collected for two days during the third week of every

month from January – September 2009. For each tree, the presence of mature and immature leaves, mature and immature fruits, and flowers or buds was recorded. Since mangabeys also feed off the ground, the presence or absence of fruits and seeds on the

ground were noted. The areas directly under the tree and under the terminal branches

were scanned for fruits and seeds. If the seeds were eaten, the relative amount eaten to available was noted. Each category was given a score of 0 – 2 (White and Edwards,

2001) with 0 indicating none, 1 indicating <75% of the canopy or ground, and 2 indicating >75% coverage.

Although ripe and unripe fruits were distinguished during monitoring, they are combined for the data analysis because the mangabeys often consumed both ripe and unripe fruits. Since the mangabeys of Sentier Nature were never observed eating flowers, only fruits and seeds are included in the analysis of temporal food availability

(although this does not discount that C. torquatus eat flowers). Many of the mangabey fruits are found on shrubs or lianas, and therefore, the fruit availability by month may be underestimated because it does not include these food sources. Several food species were not included in the analysis because their importance wasn’t known at the

beginning of the monitoring. The palm tree, Hyphaene guineensis, has fruits that are

eaten by C. torquatus during certain months; however, the tree fruits consistently throughout the year. C. torquatus also rely upon the seeds of Chrysobalanus icacao

shrubs during fruit scarce periods which are available several times a year (pers. obs).

2.5 Data Analyses

Behavioral scans

Because the number of individuals varied in every scan (from 1-36) and the

different age and sex classes were not equally represented, the individual records were

averaged for each scan (Devreese, 2010; Porter, 2001; Shah, 2003). This helps to

prevent any bias towards individuals displaying more conspicuous behaviors, or those

individuals that were more habituated than others. This method of analysis is useful

when the number of individuals observed in each scan is inconsistent and when the

behavior of a few individuals of the group is likely representative of the rest of the group

(Devreese, 2010). The average proportions for each scan were then averaged for each

month and an overall average was taken for all group estimates.

The number of days of data and the number of scans per day also varied within

each month. Therefore, the averaging of behaviors over all the months should provide

equal weight to all scans (Shah, 2003). For example, overall activity budget was

calculated by averaging the maintenance activities for every scan within a month. The

average of the scan averages were then calculated and compared to the other monthly

averages.

The Kruskal-Wallis test was used to test for differences in the amount of time

spent in each activity and the amount of time at each height class between the age and

sex classes. Kruskal-Wallis is a non-parametric statistic that tests whether two or more

observations are equally as large (Madrigal, 1998).

Synchrony of height class use was also calculated to test whether vertical group

spread varied by month. For each scan with two or more individuals, I calculated the

Simpson’s sample-size corrected index of diversity (Devreese, 2010; Krebs, 1989; Shah,

2003). Simpson’s index ranges from 0 (low diversity, or all individuals were found at the

same height class) to 1 (high diversity, or all individuals were occupying different height

classes) (Krebs, 1989).

The equation for Simpson’s index of diversity is:

s D = 1 – Σ [ ni (ni – 1) ] i N(N – 1)

where s = the total number of different height classes used in the scan, N = the number of total individuals observed in the scan sample, and ni is the number of

individuals occupying height class i in the scan sample.

Vegetation analysis

The overall density of tree and liana species for the Sentier Nature forest was

calculated using the total number of individual stems counted divided by total hectares

sampled. For each habitat type, the fruit abundance or productivity was determined by

summing the DBH of all trees producing fruit (Chapman et al., 1994). Kruskal Wallis

62 tests were performed to determine if there are any significant differences between median DBH of each habitat type.

The Shannon Weaver Biodiversity Index was also calculated for each habitat zone to determine the relative diversity (Krebs, 1989). The Shannon Weaver formula is:

H’ = -Σ pi ln(pi)

where pi = the relative abundance of each tree species

A higher number indicates higher species diversity.

Phenology

Since the project was terminated early, phenology data are only available for nine months. Several of the individual trees never produced fruit so fruit availability may be underestimated. These data also do not include foods from lianas and shrubs that may have been important in certain months (ex: Landolphia sp., Phoenix reclinata).

This estimate also does not include non-fruit species which may have formed an important component of the C. torquatus diet (crabs, invertebrates, fungi, etc.).

Following Shah (2003), I calculated three monthly estimates of fruit availability from the phenology data: 1) the number of phenology species with fruit; 2) the number of individual trees with fruit; and 3) total estimated crop production. Several methods are available to estimate the total fruit crop available in a forest (Chapman et al., 1995;

Wieczkowski and Ehardt, 2009). I chose the method used by Shah (2003) where crop production is estimated as the sum of the DBH’s of all trees producing foods eaten by C. torquatus each month (Chapman et al., 1995). Trees were included if fruits or seeds were found in the canopy or on the ground. For this study, I only have monthly data for

63 those food species that were used for the phenology analysis, and therefore, it may underestimate total overall food availability. I also compared the ranging data with food availability to determine if fruit production influences C. torquatus ranging patterns in

Sette Cama (see chapter 4).

The different estimates of food availability were then tested for correlations using Spearman’s rank correlation (rs) with a significance value of p=0.05. Spearman’s rank correlation is a non-parametric test used to test the null hypothesis that there is no association between two variables (Madrigal, 1998).

2.6 Results

Behavioral scans

These data represent the results of the systematic behavioral scans from May –

September 2009. A total of 155 group scans were collected over 37 days (Table 2.3).

There were several days each month when we searched for the mangabeys but never successfully located the group. I collected 76 focal animal scans (21 adult female, 55 adult male; Table 2.4). However, these data were not included in the overall analysis.

I collected a total of 1529 individual records (Table 2.3). The number of monkeys observed in each group scan ranged from 1-36 (with a mean of 9.85 individuals per scan;

Table 2.3). The average number of juveniles (3.9) and subadults (2.7) observed during each group scan exceeded that of adult females (1.2) and adult males (1.5). Unequal habituation levels made it possible that some individuals were more likely to avoid the observer, and therefore, certain individuals were not sampled as regularly as others.

During many scans, part of the group was not visible, and therefore, it was impossible to

observe every group member. The mangabeys also frequently formed subgroups so the

entire group was not together for most of the scans. Furthermore, many scans were

made during periods of travel, and it is possible individuals were missed because of their

quick movements.

Activity budget

The monthly averages for time devoted to each maintenance activity are

presented in Table 2.5. C. torquatus spent the most time traveling (65.9%), followed by feeding (15.3%), resting (13.2%), social behavior (3.7%), and foraging (1.4%) (Figure

2.17). The time devoted to feeding and foraging is likely underestimated due to difficulties of observation in the dense undergrowth and the lack of full habituation of this group. Cercocebus species tend to forage and eat while moving (McGraw, 1996a).

They use quick movements to grab items such as insects or fungi off the forest floor as they travel. Therefore, periods of foraging may have been erroneously characterized as traveling due to poor visibility.

Adult males, adult females, and subadults had similar frequencies of each maintenance activity (Table 2.6). Traveling was the most common activity for each of the sex and age classes, but juveniles were observed traveling at the highest frequency

(80.6% of their activities). Juveniles engaged in social behaviors the least of all groups

(1.2%). Foraging was the least common activity observed for every sex and age class.

Activity budget does not differ significantly across the sex or age classes (Kruskal Wallis, p=.392 for every maintenance activity).

Height use

The monthly averages for height class use are presented in Table 2.7. C.

torquatus spent the most time on the ground (39.4%) followed by the understory (1-5 m, 30.1%) (Figure 2.18). C. torquatus was never observed in the emergent canopy layer

(31+ m) but was in the lower, middle, and upper middle tree canopy for 30.5% of the time.

Juveniles (33.9%) and subadults (45%) were observed on the ground less often than adults (females= 57.9%, males= 50.4%; Table 2.8). Juveniles and subadults were located in the trees more than adults. Nevertheless, there are no significant differences in the amount of time spent in every height class for all sex and age classes (Kruskal

Wallis, p=.392 for every height class). Adults and subadults were found most often on the ground, which suggests an overall preference for terrestrial substrates among these age groups in C. torquatus. Adults and subadults may be more limited in their ability to exploit the different sized arboreal substrates (such as small branches or twigs).

Juveniles were observed most often in the understory (1-5 m, 36.9%) compared to the other groups. They were frequently seen climbing the thin lianas that are abundant in this part of the forest.

Overall, C. torquatus distributes their activities throughout all forest strata

(except the emergent canopy), but the ground and understory are the most common levels to find C. torquatus. Indeed, the highest percentage of maintenance activity time was spent either on the ground or in the understory (Figure 2.19). Traveling (45.1%), feeding (50.8%), and foraging (100%) occurred most frequently on the ground. Resting

and social activities were observed most often in the understory (1-5 m). 27.6% of

feeding and 22.4% of traveling occurred within the tree canopy.

The complete concentration of foraging observations on the ground is probably

due to sampling error. Foraging by C. torquatus in the tree canopy may have been

confused for traveIing. Since C. torquatus relies on both foods on the ground and in the

trees, foraging will occur in both forest levels. The only type of primate that would be

observed foraging on the ground 100% of the time is a completely terrestrial primate.

Other Cercocebus species forage and feed on the ground, in the understory, and in the

trees (Devreese, 2010; McGraw, 1996a; Mitani, 1989; Shah, 2003). In Campo

Cameroon, Mitani (1989) observed C. torquatus feeding most often in the middle

canopy followed by the ground.1 C. atys were seen foraging in the understory most

frequently, at an average height of 2.12 meters.

Group spread

The Simpson’s index of diversity was calculated for each month and then averaged (Table 2.9). The diversity index serves as a measure of vertical group spread.

As group size increases, the use of different forest strata may lessen intragroup feeding competition.

The overall mean vertical distribution for C. torquatus was 0.47. This indicates that at any time, almost half of the group used different forest strata. The vertical distribution of the group was highest in July (0.52), the month with the highest number

1 Mitani (1989) did not delineate between feeding and foraging for his study so it is assumed that these activities were combined during his observations.

of tree species with fruit (Figure 2.20). However, group spread was higher, in general,

during the months with the least number of individual trees fruiting (May, June, and

July). This suggests that C. torquatus are using different strata when fruits are less

available. Vertical distribution decreased in the months with the most individuals

fruiting (August and September). During these months, the primary food source for C.

torquatus was Sacoglottis gabonensis fruits that they largely obtain from the ground.

Studies of C. agilis in Central African Republic also measured the mean diversity index of vertical distribution. The mean diversity indices were 0.5 at Mondika (Shah,

2003) and 0.3 at Bai Hoku (Devreese, 2010). Interestingly, the larger Bai Hoku group

(N=230) had a lower mean vertical distribution, but they have a large home range (1000 ha). C. torquatus is most similar to the smaller C. agilis group (N=22) in vertical

distribution, and they also have similar home range sizes (~300 ha). Perhaps Cercocebus

groups adapt to smaller home ranges by increasing vertical distribution at any given

time.

Overall habitat use, maintenance activity by habitat type, and height use by habitat

type

C. torquatus was observed most frequently in the mangrove section of their habitat (N=97) followed by the terra firme zone (N=39) and coastal forest zone (N=19)

(Figure 2.21). The most observations occurred in the mangrove zone in every month except May and June. This is not surprising given the suggestion that Cercocebus

species prefer riverine or swampy habitats (Jones and Sabater Pi, 1968; Kingdon, 1997).

Although it wasn’t possible to follow the mangabeys into the inaccessible swamp zone,

this area was probably their most frequented area. Every day after eating, they would

retreat into this swamp zone, and they also headed to this zone when startled or

frightened (pers. obs).

The number of observations in each habitat varied monthly (Figure 2.21).

Observations were most common at the coastal forest area during May and June.

During these months, C. torquatus frequently fed on foods located by the beach including palm fruits, Chrysobalanus icacao fruit and seeds, and crabs (pers. obs; Figure

2.22). These foods are available most of the year, but C. torquatus ate them predominantly during periods of lower fruit availability (pers. obs). The number of observations in the coastal habitat was also negatively affected by our ability to track C. torquatus effectively during peak elephant season (March – September). Observations in the terra firme and mangrove habitats increased from July to September. This coincides with the peak fruiting period of many of the tree species in these habitat types.

C. torquatus was observed traveling, feeding, foraging, resting and socializing in all of the habitat types but at different frequencies (Figure 2.23). They traveled the most in the mangrove habitat (74.7%), but the frequencies among habitat types do not differ greatly (terra firme=67%, beach=58.7%). Compared to the other habitat types, feeding was most common within the terra firme habitat (17.2%), and this coincides with the high number of fruiting trees in this habitat type. Resting occurred most frequently in the beach habitat (23.3%), and social behaviors were observed most often in the mangroves compared to other habitat types.

In general, C. torquatus spent most of their time in the beach habitat at heights of 6 meters or higher (6-10 m=30%, 11-20 m=22%, 21-30 m=10%) (Figure 2.24). This

may be due to the relatively open understory in this zone which offers less predator

protection than in other zones. C. torquatus were found most often on the ground in

the terra firme habitat (49.3%), but they were also frequently observed on the ground in

the mangroves (47.1%). C. torquatus spent less time in the trees in the mangrove

habitat compared to the other habitat types.

Vegetation of the Sentier Nature Forest

A total of 713 stems (unknown=46) were measured in the Sentier Nature forest

representing 19 different species (and at least 5 unknown species) over the 1.3 hectares

sampled (Table 2.10). Table 2.11 lists all the tree and liana species identified in the

vegetation plots and the mean DBH by species. The DBH of stems ranged from 10 cm to

188 cm (Figure 2.25). The majority of stems measured between 10-20 cm (N=132) and

31-40 cm (N= 104). This suggests a relatively young age for this forest or recent

disturbance in selected areas. The total stem density for the Sentier Nature forest is

estimated at 550 trees per hectare. The density of food trees is 430 trees per hectare.

The forests of this region feature extreme variation in habitat types. Therefore,

each habitat type will be presented individually and general trends in biodiversity, DBH,

and fruit tree density (total number of individual trees of fruiting species [regardless of

the overall contribution to diet] divided by the total area sampled) are discussed

(Chapman et al., 1995; Shah, 2003).

Summary of biodiversity, tree species, and fruit abundance by habitat type

Beach: The coastal forest was the least diverse in terms of tree species (Table

2.10). This zone also had the lowest number of tree stems (193). Only two species were observed (Hyphaene guineensis and Manilkara fouilloyara), and the diversity index is the lowest of all three habitat types (1.97).

The mean DBH of all trees (33.5 cm) was higher than for the mangrove habitat

(Table 2.10). However, none of the trees measured higher than 70 cm in diameter

(Figure 2.25). The average food tree density was 148.5/ha and the total DBH of fruit trees (6462.4 cm) was higher than the terra firme habitat (Table 2.10). Both tree species in this habitat provide fruits for C. torquatus. H. guineensis fruit year-round but these fruits are only consumed by C. torquatus when overall fruit abundance is low (pers. obs).

The Manilkara trees fruit from January – March. During this time, C. torquatus fills their cheek pouches full of Manilkara fruits and spends long periods in the beach habitat

(Figure 2.26). Therefore, the potential for fruit abundance is high along the beach but only during certain times of the year.

Terra Firme: The terra firme habitat featured the most species diversity

(Shannon Weaver Index of 7.5) but less stems than the mangrove habitat (Table 2.10).

There were 16 different tree and liana species identified (Table 2.10). Of these species,

14 provide fruits for C. torquatus. The three most common trees were: Scytopetalum pierranum, Dialium pachyphyllum, and Sindora klaineana. Each of these species were also important fruiting trees for C. torquatus.

The average DBH (37.5 cm) was higher for this habitat than the averages for the beach and mangrove habitats (Table 2.10). The average DBH for fruit tree species was

36.2 cm and the total fruit tree DBH was 6219.4 (cm). The largest number of stems had a DBH of 10 – 20 cm (Figure 2.24) but this habitat had a more even distribution of stems in each DBH class. This habitat also had trees with the highest DBH measures (for example, a Sacoglottis gabonensis tree with a DBH of 188 cm). Food tree density was the same as in the mangroves (143.1/ha).

Mangrove: The mangrove habitat had a lower Shannon Weaver Diversity Index

(6.2) than the terra firme habitat (Table 2.10), but the most tree stems (315) were counted in this area. 12 species were identified; 10 of which provided fruits for C. torquatus (Table 2.12). The three most common species were: Anthostema aubrynum,

Macrolobium sp, and Sindora klaineana. The top three fruit species were: S. klaineana,

Scytopetalum sp, and Lecanodiscus cupanoides.

The average DBH of all species (31.7 cm) was the lowest of all the habitats (Table

2.10). Fruiting species had an average DBH of 30.56 cm. The total food tree DBH

(7067.1 cm) was highest in this zone but the food species density was the same as in the terra firme habitat (143.1/ha). Although no trees were measured with a DBH above 120 cm, the high productivity of this zone can be attributed to the higher number of individual trees and lianas found here.

Comparison of productivity among habitat types

The mean DBHs for each habitat type are significantly different (Kruskal-Wallis test, p=0.<005). Based on the assumption that DBH is a good measure of fruit

productivity (Leighton and Leighton, 1982; Chapman et al., 1995), the mangrove habitat

was the most productive. The terra firme habitat contained the most C. torquatus food

species but had the lowest overall total DBH. C. torquatus were also most frequently

observed in the mangrove habitat. These estimates provide a guide for the spatial

distribution of C. torquatus foods, but their movements are also influenced by the temporal distribution and availability of foods. Therefore, it is also necessary to discuss the variation in food availability and productivity over time in the Sentier Nature forest.

Phenology: Food availability by month

Number of phenology species with fruit and seeds and number of individual

trees with fruit or seeds

February was the month with the lowest number of phenology species in fruit (2

species) and the highest number of species with fruit was in July (9 species) (Figure

2.27). The highest number of individual trees with fruit (37 individuals) was in

September whereas the lowest number of trees fruiting was in February and March (8

individuals) (Figure 2.28).

The months with the lowest numbers of species and individual trees with fruit

coincide with the small dry season (December – February). In contrast, the period of high fruit availability in both number of species fruiting and number of individual trees with fruit (May – August), is during the months of the long dry season.

It should be noted that old S. gabonensis seeds were available on the forest floor every month of the phenology study. The percentage of seeds was lowest toward the end of the dry season (July, August, and September) because they were exploited more

heavily in the previous months. This period of S. gabonensis seed decline coincided with the time of peak S. gabonensis fruiting. Therefore, S. gabonensis seeds appear to be most abundant a few months after fruiting when a new “crop” of seeds have had time to mature on the ground (December – May).

Total monthly estimated crop production

The estimated crop production of phenology trees varied monthly (Figure 2.29).

The lowest crop production was in February and March. At this time, C. torquatus eat mostly Manilkara fruits and supplement their diets with crabs and palm fruits (pers. obs). The highest crop production occurred from July – September.

Correlations among estimates of food availability

The estimates of food availability (diversity, number of trees, and crop production) are significantly correlated (Table 2.13). Shah (2003) found a similar relationship among agile mangabey foods in Mondika.

Behavioral changes in response to temporal fluctuations in food availability

The proportion of time spent in the different maintenance activities, mean height use, vertical group distribution, and habitat type were compared to the three estimates of food availability: number of fruiting species, number of individual fruiting trees, and crop production. The goal was to determine if food availability influences behaviors. However, these data only consist of the five months of systematic behavioral data (May – September).

Fruit availability and maintenance activities

None of the three estimates of fruit availability were significantly related to monthly maintenance activities (Table 2.14). This does not mean, however, that fruit availability does not impact activity budget in the months not included in the analysis.

Shah (2003) observed that agile mangabeys reduced their travel time and intensified their foraging behaviors during periods of fruit scarcity. If C. torquatus reacts similarly to diminished fruit availability, they should also increase foraging and decrease time devoted to traveling. This would suggest a more rigorous use of their habitat during the rainy season when fruit is generally less abundant. It is expected C. torquatus would supplement their diets with more terrestrial foods that require intensive foraging such as fungi, shoots, or insects. It must also be reiterated, however, that the activity data for this group may not accurately reflect C. torquatus behaviors due to their lack of full habituation.

Fruit availability and mean height and vertical distribution

There are no significant relationships among average monthly height use, vertical distribution, and fruit availability (Table 2.15). In contrast, Shah (2003) found that agile mangabeys used the ground more often during periods of low fruit abundance.

Fruit availability and habitat use

There are no significant correlations among fruit availability and the use of the beach and terra firme habitat types (Table 2.16). However, as the number of individual trees in fruit and crop production increases, C. torquatus uses the mangrove habitat

more often (trees in fruit: rs=1, p=0.01; crop production: rs=1, p=0.01). This is likely

related to the increase in productivity within this habitat type during the dry season.

2.7 Discussion

This study represents the first long-term study of C. torquatus in Gabon and

presents some baseline behavioral data for this species. These data are compared to

other members of this genus to determine if C. torquatus activity patterns, terrestriality,

habitat use, and site productivity are comparable to other Cercocebus species.

Maintenance activity patterns of C. torquatus and comparison to other Cercocebus

species

Data on activity budgets are relatively scarce among Cercocebus species, and this

study presents the first estimate of C. torquatus activity patterns in Gabon. The available data on Cercocebus species suggest significant variation in time devoted to travel, feeding, and foraging among these species (Table 2.17). Socio-sexual behaviors are observed the least often in all species. Both populations of C. agilis travel more than the other species, but all Cercocebus species (with the possible exception of C. torquatus) devote almost half of their time to feeding and foraging for food. The high percentage of time spent foraging and feeding corresponds to the hard-object terrestrial feeding strategy of this clade that requires extensive searching through leaf- litter for fallen seeds and nuts (Fleagle and McGraw, 1999, 2002; Shah, 2003).

The time devoted to various maintenance activities by C. torquatus in Sette

Cama differs from that observed in other Cercocebus species (Table 2.17). Locomotion

is the most common maintenance activity, followed by feeding and resting among C.

torquatus. All other species spend more time in feeding and foraging combined than in locomotion. It is expected that populations with larger group sizes should travel more than populations with smaller group sizes (Janson and Goldsmith, 1995), but C. torquatus traveled substantially more often than the more numerous C. atys and C. agilis populations (Table 2.18). Furthermore, C. torquatus traveled more than C. agilis in

Mondika, which occupies a similarly sized home range (Table 2.18). The relatively low amount of time devoted to traveling among C. atys (which has both a large home range and a large group size) is perplexing. Perhaps C. atys practices subgrouping or wide vertical group spread while foraging on its terrestrial resources and once a patch is depleted the entire group moves to the next patch. This could lead to a decrease in daily path length but an overall increase in home range size.

C. torquatus in Sette Cama travel much more often than other Cercocebus species. Figure 2.30 shows a scatterplot of home range size compared to travel times among African papionins. Although the relationship between group size and travel time is not significant among African papionins (p=0.366), the position of C. torquatus in relation to the other species does indicate a problem with the value.2 C. torquatus falls

well outside all the other data points, which suggests that the amount of travel among

this population may be artificially high. One reason for the inflated rates of travel could

2 The lack of a significant relationship between group size and travel times among these African papionines may be attributed to the terrestrial species and the low number of data points. Janson and Goldsmith (1995) found that folivores and primarily terrestrial primates do not necessarily fit into the predictions for group size and travel times.

be the lack of full habituation of the C. torquatus group. Species, such as western lowland gorillas, have shown increased daily path lengths during the process of habituation compared to after habituation (Cipolletta, 2003; Blom et al., 2004). Also, because of poor visibility in the undergrowth, foraging may have been erroneously categorized as traveling. This leads to the possibility that a significant portion of the red-capped mangabey’s time was devoted to travel rather than other activities. The group was probably moving more, not out of necessity to forage more, but because it was trying to distance itself from the observers.

There also does not appear to be a correlation between activity patterns and group size among Cercocebus species. C. agilis (in Bai Hoku average group size is 230) and C. atys (N=120) have the largest group sizes of this genus (McGraw, 1996a;

Devreese, 2010). C. atys travels much less often than this C. agilis population and C. atys devotes more time to feeding, foraging, resting and socio-sexual behaviors.

However, C. agilis in Bai Hoku occupy a much larger home range which may necessitate more traveling than for C. atys. The species with smaller group sizes (C. agilis in

Mondika, C. galeritus) of around 25 individuals also have different maintenance activity budgets from one another. C. torquatus group composition is more similar to the larger group sizes (N=70), but their activity budget is much different. Again, this illuminates the need for further study among this group after fully habituated, but these comparisons among species highlight the wide range of behavioral diversity that seems to be characteristic of this genus.

Terrestriality of C. torquatus and comparison to other Cercocebus species

In general, Cercocebus are considered semi-terrestrial, but anatomical studies suggest that they should spend the majority of their time on the ground (Nakatsukasa

1994, 1996). C. torquatus, in particular, was proposed as the most terrestrial of all

Cercocebus species. Intrageneric comparisons reveal that some Cercocebus species are more terrestrial than others, and there is a range of variation in terrestriality among species. More importantly, though, C. torquatus is not as terrestrial as predicted by their skeletal morphology (refer also to chapter five).

The data from different populations place C. agilis as either the most or least terrestrial Cercocebus species (Table 2.19). C. torquatus is the second least terrestrial and uses the tree canopy more often than all populations except C. agilis in Mondika

(Shah, 2003). Anecdotal evidence from Campo, Cameroon also suggests that C. torquatus spend a considerable amount of time in the trees (Mitani, 1989). C. atys is highly terrestrial (67% of the time) and C. galeritus is found on the forest floor for around 51% of its time (Homewood, 1978; McGraw, 1998).

There are several possible reasons for the differences in height preference among Cercocebus mangabeys. First, the density and number of competing species varies by site. C. agilis in Mondika shares the forest with the more “arboreal” mangabey genus, Lophocebus, and seven other primate species (Shah, 2003). Yet, this species is the least terrestrial of all Cercocebus mangabeys. If Cercocebus uses terrestrial feeding as a strategy to help mitigate feeding competition, it would be expected that they would

increase the time spent on the ground when more competing species are present.

Perhaps there are other primate species in Mondika that occupy the terrestrial niche.

C. atys is highly terrestrial and shares the Taï Forest with six other cercopithecoid

species (McGraw, 1996a). C. torquatus in Sette Cama is more arboreal than C. atys at

Taï. This population is usually only found with one other primate species, C. cephus,

which may allow C. torquatus to utilize the forest levels more evenly. The differences in forest height use within the Cercocebus genus may reflect niche partitioning among the

various species in these forest communities.

Finally, the vertical distribution of food resources can largely impact a species’ height preferences in the forest. Most Cercocebus species are highly frugivorous (see chapter 1) but still rely upon seeds and terrestrial vegetation in their diets. C. torquatus

in Sette Cama eat primarily seeds (54%), but approximately 38% of their diet is fruits

(see chapter 4). The amount of time spent on the ground and in the trees is similar in

this population. The vertical distribution of C. torquatus in Campo was strongly

correlated with the abundance of fruits from 20-30 meters in the forest canopy (Mitani,

1989). C. atys is the least frugivorous of all the Cercocebus species (diet comprised of

~60% seeds and invertebrates), and with the exception of the C. agilis Bai Hoku population, C. atys are the most terrestrial (McGraw et al., 2011). This highlights the flexibility of Cercocebus species and their ability to exploit different strata.

Vertical distribution of C. torquatus during maintenance activities and comparison to other Cercocebus species

Data from Campo, Cameroon suggest a difference in the vertical distribution of

C. torquatus at that site compared to Sette Cama (Mitani, 1989). While traveling and resting/social activities occurred most frequently on the ground (around 60% of observations, respectively) in Campo, feeding was most common from 25-30 meters. In contrast, feeding was most common on the ground among C. torquatus at Sette Cama.

Mitani (1989) found a positive correlation between feeding height and the

distribution of fruit within the forest canopy. In Campo, the foods eaten most by C.

torquatus were located from 20 – 30 meters in the canopy. The distinctions in preferred feeding heights between C. torquatus sites may be related to dietary differences. C.

torquatus in Sette Cama eat more seeds (54%) and fruits obtained from the ground than

Campo C. torquatus (seeds comprise 20% of the diet) (Mitani, 1989). Therefore, C. torquatus in Sette Cama were observed feeding more often on the ground than the

Campo population.

There is also a wide range of variation in the vertical distribution during maintenance activites of the different Cercocebus species. Data are available on the feeding heights of C. agilis from Mondika, CAR (Shah, 2003). This population was less terrestrial overall compared to C. torquatus and other Cercocebus species. The agile

mangabey fed most often on the ground (25%), followed by 6-10 m (20%), and the

understory (19%). Around 33% of feeding among C. agilis occurred at heights of 11

meters or above. C. agilis at this site are also only found on the ground for a total of

22% of the time.

C. atys fed more often in the understory than on the ground (McGraw, 1996a).

The mean height for all activities (except for social behaviors) was around 2 meters, or

in the understory.

The sooty mangabey generally feeds and rests at higher altitudes while foraging and travel takes place closer to and including the forest floor. This trend is in accord with the tendency for mangabeys to forage on the ground and then bring selected food items to low trees where they are eaten (McGraw, 1996a: 115).

McGraw also notes that C. atys rarely travels in the trees (10.9% of travel),

whereas C. torquatus was observed traveling in the tree canopy for 22.4% of travel time.

Overall, the sooty mangabey is more terrestrial than C. torquatus, and the diet of C. atys

includes a substantial amount of seeds (around 60%) (McGraw et al., 2011).

Differential habitat use in C. torquatus and comparison to other Cercocebus species

One of the more common generalizations regarding the Cercocebus genus is its

preference for riverine, swamp, or seasonally inundated forests (Kingdon 1997; Gautier-

Hion et al., 1999; Shah, 2003). This study, and the known distribution of C. torquatus

throughout Gabon, suggests that this species does prefer wetter habitat types. C.

torquatus in Sette Cama was observed most often in the mangrove section of its habitat.

However, they were also seen quite frequently in the terra firme habitat and also in the coastal palm habitat. Indeed, other Cercocebus species, such as C. agilis in Mondika and

C. atys at Taï are found in predominantly terra firme habitats (McGraw, 1996a; Shah,

2003).

Shah (2003) proposes that Cercocebus species are not limited to swampy habitats although they may prefer this type of environment. More specifically, “…it may be more fitting to think of Cercocebus mangabeys as adapted to forest habitats with

82 dense undergrowth, broken canopies, and an abundance of shoots and other new growth, rather than necessarily restricted to water-dependent forests” (Shah,

2003:111). The semi-terrestrial adaption of Cercocebus allows it to exploit both terrestrial and arboreal food sources to varying degrees depending upon site conditions.

Therefore, when considering conservation and reintroduction efforts for Cercocebus mangabeys (such as those by organizations like CERCOPAN), the semi-terrestrial nature of Cercocebus may be a larger factor in determining habitat suitability than the need for a specific habitat category (such as swamp forest compared to a drier forest).

Food tree density and productivity in Sette Cama compared to other sites in Africa

The overall food tree density at Sentier Nature, Sette Cama is similar to other sites where similar measures were made. For example, Kibale National Park in Uganda features a range of 59.4 food trees per hectare in logged forest and 145.6 food trees per hectare in unlogged forest (Chapman et al., 1995). This forest supports a larger number of primate species (five) than Sette Cama (four, at different times of the year) and is much larger in overall size.

The average DBH for food trees and crop production by month is higher in the

Sentier Nature forest compared to Mondika, Central African Republic (Shah, 2003). In

Mondika, food trees averaged a DBH of 28.8 cm and crop production values ranging from 800-1800 a month. The average DBH of fruit trees in Sentier Nature is 33.41 cm and the crop production values range from 950-2556 a month. These numbers are lower, though, compared to Kibale National Park (Chapman et al., 1995).

The higher relative productivity of the Sentier Nature forest may partially explain

how C. torquatus can obtain such a large group size without a large home range (only around 300 ha). C. atys are the most comparable in overall group size, but they occupy a home range that is 2.5 times larger than C. torquatus in Sette Cama (McGraw et al.,

2011). The lack of feeding competition, high abundance of foods, the vertical distribution of the group, and frequent subgrouping may allow for the higher population size at this site compared to other C. torquatus sites (Mitani, 1989).

Phenological differences between sites in Gabon

The period of high fruit availability varies by region in Gabon. The fruiting patterns are more traditional in the more centrally located, inland forest of Lopé. Fruit availability is typically lowest during the long dry season (June – September). In contrast, in the Sentier Nature forest, the dry season is a period of high fruit availability.

The months of October – December were not included in the Sentier Nature forest sample, but personal observation from previous years suggest that these months feature smaller numbers of species in fruit compared to June – September. It should also be noted that for this study, I chose trees that were important to C. torquatus for phenological monitoring so it may not adequately represent overall forest productivity.

Despite these caveats, the fruiting patterns in Sette Cama are probably influenced by its coastal position and variety of habitat types, and therefore, differences in productivity should be expected compared to Lopé. More importantly, we cannot assume that the dry season is a “lean” period for all primate species. In Sette Cama, the months with the least fruits available for C. torquatus were during the major rainy

season. If C. torquatus do rely upon hard-object foods as a fallback resource, the

consumption of these foods should be highest during this period.

2.8 Conclusions

C. torquatus of Sette Cama, Gabon behave differently from other Cercocebus

species. In general, they are observed traveling more often, and C. torquatus are one of the most arboreal Cercocebus mangabeys. C. torquatus does not appear to be affected by the seasonal availability of fruit production in its habitat. C. torquatus are typical of their genus in their preference for swampy, mangrove habitat types, but they also frequent the coastal palm and terra firme portions of their habitat.

The large group size and relatively small home range of this C. torquatus population may be related to the unusual nature of its habitat. The Sentier Nature forest is bound on both sides by tourist lodges which restrict C. torquatus to a small segment of forest (~300 ha). However, based on the limited data of this study, this forest is highly productive and offers relatively little feeding competition for the few primate species that live there. C. torquatus, and Cercocebus species in general, appear to be highly adaptable. For example, C. torquatus adjusts its habitat use in response to fruit availability. They also utilize a wide vertical distribution in the forest and divide into subgroups. These behavioral adjustments have allowed this population of C. torquatus to thrive.

It must be emphasized, again, that the results of this study only represent a portion of C. torquatus yearly behaviors. The level of habituation most likely impacted

85 the results of overall activity patterns, but we now have a basic idea of C. torquatus behavior in this large population.

Figure 2.1: The location of Sette Cama, Gabon. (Map by Richard Moussopo Ibessa).

Figure 2.2: The distribution of the different habitat types within the Sentier Nature forest.

Figure 2.3: The flooded mangrove forest near the edge of the lagoon.

Figure 2.4: A section of the mangrove forest during the dry season.

Figure 2.5: Terra firme habitat.

Figure 2.6: Another view of the terra firme habitat.

Figures 2.7: Coastal palm forest.

Figure 2.8: Another view of the coastal palm forest.

Figure 2.9: A map of the three main trails in the Sentier Nature forest, Sette Cama, Gabon. (Map by Richard Moussopo).

Figure 2.10: The inaccessible swamp zone that borders the mangrove forest.

Figure 2.11: Adult male C. torquatus.

Figure 2.12: Adult female C. torquatus.

Figure 2.13: Subadult C. torquatus.

Figure 2.14: Tree zones; 0=ground (not marked), 1= tree trunk, 2= interior canopy branches, 3= terminal branches, 4=uppermost canopy, 5=areas adjacent to the tree trunk including lianas and treefalls.

Figure 2.15: The vegetation plots used to collect botanical data along the three main trails in Sentier Nature.

BALUMBU NAME SCIENTIFIC NAME FAMILY DILOLOU Antodrophragha congoense MELIACEES GOYAVE Psidium guineensis MYRTACEES Poechevalierodendron ICOLE stephanii CESALPINIOIDEES KEVAZINGO, OBAKO Guibortia ebie CESALPINIOIDEES MBILINGA Nauclea didirichi RUBIACEES MOABI Baillonella toxisperma SAPOTACEES MOUFOUM Ceiba pentadra BOMBACACEES MOUKOUMI Aucoumea klaineana BURSERACEES MOUKUISSE Costus albus ZINGIBERACEES MOULOMBE Pycnanthus angolensis MYRISTICACEES MOUMBOUDZINI Alchornea cordifolia EUPHORBIACEES MOUNDZIADZI Anthostema aubryanum EUPHORBIACEES MOUNDZOUNGOUBALI Pseudos pondias ANACARDIACEES MOUNIOGUE, OZOUGA Sacoglottis gabonensis HUMIRIACEE MOUTSAFOU Dacryodes edulis BURSERACEES MOUTSIETSIENDI Macaranga barteri EUPHORBIACEES Distemonanthus MOUVENGUI benthamianus CESALPINIOIDEES MUGAU Phoenix reclinata PALMAE MUMBUNDJĒNI Alchornea cordifolia EUPHORIACEES NGOM Sindora klaineana LEGUMINOCEES NZIATSI Lympia adouinsis UNKNOWN TOBU, BAYA Mitragyna ciliata RUBIACEES TODOU Staudtia gabonensis MYRISTICACEES

Table 2.1: Some common plant names in the local Balumbu language.

Species Name Number Height DBH Manilkara fouilloyara A01 20 39 Manilkara fouilloyara A02 25 58 Manilkara fouilloyara A03 25 50 Manilkara fouilloyara A04 20 49 Manilkara fouilloyara A05 30 70 Scytopetalum pierranum B01 20 27 Scytopetalum pierranum B02 30 48.5 Scytopetalum pierranum B03 20 31.5 Scytopetalum pierranum B04 25 42.5 Scytopetalum pierranum B05 27 51.5 Syzygium guineense C01 20 37 Syzygium guineense C02 30 51 Syzygium guineense C03 30 71 Syzygium guineense C04 30 65 Syzygium guineense C05 30 112.5 Sindora klaineana D01 35 83 Sindora klaineana D02 30 53.5 Sindora klaineana D03 20 43 Sindora klaineana D04 30 106 Sindora klaineana D05 25 62 Dialium pachyphyllum E01 25 101.5 Dialium pachyphyllum E02 20 133 Dialium pachyphyllum E03 20 47 Dialium pachyphyllum E04 25 41 Dialium pachyphyllum E05 25 58 Sacoglottis gabonensis F01 25 136 Sacoglottis gabonensis F02 45 179 Sacoglottis gabonensis F03 40 110 Sacoglottis gabonensis F04 45 131 Sacoglottis gabonensis F05 45 119 Vitex doniana G01 25 63.5 Vitex doniana G02 20 85 Vitex doniana G03 30 100 Vitex doniana G04 35 99.5 Vitex doniana G05 20 56 Continued

Table 2.2: List of the Phenology Species, Identification Labels, Height (in meters), and DBH

Table 2.2: Continued

Species Name Number Height DBH Guibortia tessmannii H01 20 35 Guibortia tessmannii H02 30 82.5 Guibortia tessmannii H03 30 54 Guibortia tessmannii H04 25 62 Guibortia tessmannii H05 35 92.5 Pycnanthus angolensis I01 45 108 Lecanodiscus cupanoides J01 10 14 Lecanodiscus cupanoides J02 12 14 Lecanodiscus cupanoides J03 15 12.5 Lecanodiscus cupanoides J04 12 12.3 Lecanodiscus cupanoides J05 15 13.5

Figure 2.16: The location of phenology trees in the Sentier Nature forest.

Month Days Scans Indiv Avg # Male Female Juvenile Subadult Unkn Indiv May 4 12 63 5.25 15 10 16 11 11 June 10 29 252 8.6 31 34 106 74 7 July 6 23 227 9.8 37 33 85 71 1 August 11 57 547 9.5 81 61 159 227 19 September 6 34 438 12.8 72 46 253 41 27

Total 37 155 1529 236 184 619 424 65 Avg/Scan 9.85 1.5 1.18 3.99 2.73 0.41

Table 2.3: Sample sizes for group scans and the total and average number of individuals observed each month by age class.

# Focal Scans # Adult Female # Adult Male Scans Scans May 13 4 9 June 12 4 8 July 17 4 13 August 18 3 15 September 16 6 10

Total 76 21 55

Table 2.4: The number of focal animal scans by month and sex class.

100

TRAVEL REST FEED FORAGE SOCIAL May 68 14.2 13.4 0 0 June 58.2 20.6 14 3.3 6.2 July 63.5 15.6 17.7 1.3 1.9 August 68.4 8.6 17.5 1.6 3.9 September 71.2 7.1 14.1 0.9 6.7

Total 65.86 13.22 15.34 1.42 3.74

Table 2.5: Monthly averages for each maintenance activity.

Activity Budget for C. torquatus (N=155)

1.4% 3.7%

15.3% TRAVEL REST

13.2% FEED FORAGE 65.9% SOCIAL

Figure 2.17: Average maintenance activity budget for C. torquatus during the months of May – September 2009.

101

TR FE FO R SS Adult Female 64.9 15.1 2.7 12.4 4.9 Adult Male 66.5 14.8 1.7 11.9 5.1 Juvenile 80.6 6.9 0.7 10.6 1.2 Subadult 69 14.2 1.3 9.9 5.7

Table 2.6: Maintenance activities for all sexes and age classes.

Height Class Use (N=155)

31+ m

21-30 m

11-20 m

6-10 m

1-5 m

0 m

0 10 20 30 40 50

Figure 2.18: The overall average height class distribution for all observations of C. torquatus.

102

Month 0 1-5 6-10 11-20 21-30 31+ May 37.9 29.5 10.8 7.6 14.2 0 June 36.8 19.1 17.2 19.1 7.7 0 July 32.1 32.1 10.5 11.4 13.9 0 August 45.1 33.3 6.2 11.4 3.9 0 September 45.1 36.4 7.3 7.7 3.5 0

Total 39.4 30.08 10.4 11.44 8.64 0

Table 2.7: The monthly averages for height class use.

0 1 - 5 6 - 10 11 - 20 21 - 30 31 + Adult Female 57.8 27 3.8 3.8 7.6 0 Adult Male 50.4 23.3 6.4 11.4 4.4 0 Juvenile 33.9 36.9 11.8 12.3 5.2 0 Subadult 45 34.7 6.8 9.1 4.4 0

Table 2.8: Average height class use for every sex and age class.

103

Maintenance Activity by Height

Social

Rest 31+ 21-30

Forage 11-20 6-10 1-5 Feed 0

Travel

0 20 40 60 80 100

Figure 2.19: The frequencies of maintenance activity within each height class.

Month Diversity Index Min Max May 0.48084 0 1 June 0.50415 0 1 July 0.52371 0 1 August 0.3963 0 1 September 0.47731 0 0.83333

Average 0.47646

Table 2.9: Simpson’s Diversity index as a measure of vertical group spread by month.

104

Vertical distribution compared to food availability by month 40 35 30 25 Species with Fruit or 20 Seeds 15 Trees with Fruits or 10 Seeds 5 0.48 0.50 0.52 0.39 0.47 Vertical Distribution 0 May June July August Sept

Figure 2.20: The monthly vertical group distribution (range 0 – 1) compared to food availability for each month.

Number of scans each month by habitat type 40 35 30

25 20 Beach

# Scans 15 Terra Firme 10 Mangrove 5 0

Figure 2.21: Monthly distribution of scan observations over the different habitat types (N=155).

105

Figure 2.22: Remains of one of the crab species (Cardisoma armatum) eaten by C. torquatus in Sette Cama.

Maintenance Activity by Habitat Type

Social

Rest Mangrove Forage Terra Firme Beach Feed

Travel

0 10 20 30 40 50 60 70 80

Figure 2.23: The distribution of each maintenance activity by habitat type.

106

% time at each height class within each habitat type

31+

21-30

11-20 Mangrove

6-10 Terra Firme Beach 1-5

0 10 20 30 40 50 60

Figure 2.24: Height class distribution within each habitat type.

Habitat Sp Total # Mean Shannon- Total DBH of food Food tree of DBH Weaver food trees (cm) density Stems trees Terra 16 205 37.48 7.46 181 6219.35 143.1/ha Firme Beach 2 193 33.48 1.97 193 6462.4 148.5/ha Mangrove 12 315 31.73 6.19 186 7067.1 143.1/ha

Table 2.10: The summary of vegetation and vegetation analyses by habitat type.

107

Species Mean DBH Anthostema aubryanum 21.05 Chrysobalanus ellipticus 35.25 Cola carcifolia 11.97 Dialium 34.9 Guibortia tessmannii 50.09 Hyphaene guineensis 37.13 Lecanodiscus cupanoides 15.66 Macrolobium spp 28.57 Manilkara 23.14 Mareyopsis longifolia 17.05 Newtonia leucocarpa 27.4 Pachylobus spp 13 Sacoglottis gabonensis 42.65 Scytopetalum spp 28.53 Sindora klaineana 55.67 Syzygium spp 58.29 Vitex doniana 53.83 Xylopia spp 15.7 Unknown 27.61

Table 2.11: Summary of all the tree and liana species identified within the Sentier Nature forest and the mean DBH.

108

DBH of trees in Sentier Nature Forest 140 120

100 80 60 #Trees 40 Beach 20 Main 0 Lagoon 10 - 20 21 - 30 31 - 40 41 - 50 51 - 60 61 - 70 71 - 80 81 - 90 91 - 100 101 110 - 111 120 - 121 130 - 131 140 - 141 150 - 151 160 - 161 170 - 171 180 - 181 190 - DBH (cm)

Figure 2.25: The number of trees of each DBH class in the Sentier Nature forest.

Fruit Species Sampled in Vegetation Plots Main Lagoon Beach

Chrysobalanus ellipticus X X Cola carcifolia X X Dialium X X Guibortia tessmannii X X Hyphaene guineensis X Lecanodiscus cupanoides X X Manilkara spp X X X Newtonia leucocarpa X Pachylobus spp X Sacoglottis gabonensis X X Scytopetalum spp X X Sindora klaineana X X Syzygium spp X Vitex doniana X X Xylopia spp X

Table 2.12: The C. torquatus fruit trees sampled within the vegetation plots and the habitats they are found in.

109

Figure 2.26: C. torquatus filling his cheekpouches with Manilkara fruits. (Photo by BBC).

Number of phenology species with fruit or seeds by month for January-September 2009

10 9 8 7 6 5 4 3 2 1 0

Figure 2.27: The number of tree species with fruit or seeds by month for January – September 2009.

110

Number of individual trees with fruits or seeds by month for January-September 2009

40 35 30 25 20 15 10 5 0

Figure 2.28: The number of individual trees with fruit or seeds by month for January – September 2009. These numbers represent the number of trees for each species included in the phenological monitoring.

Crop Production by Month (DBH) 3000

2500

2000

1500

1000

500

Figure 2.29: Total estimated crop production of phenology trees by month.

111

# Fruit # Fruit Crop Species trees Production # Fruit Species X 0.865* 0.783** # Fruit Trees X 0.946*** Crop X Production

Table 2.13: Spearman’s rank correlation values for correlations between the three estimates of fruit availability based on phenological monitoring. Significance levels *0.003, **0.013, ***0.001

TR p R p FD p FO p SO p Fruit -0.35 0.55 0.35 0.55 0.70 0.18 0 1 -0.35 0.55 Species Fruit 0.7 0.18 -0.7 0.18 0.6 0.28 0.1 0.87 0.7 0.18 Trees Crop 0.7 0.18 -0.7 0.18 0.6 0.28 0.1 0.87 0.7 0.18 Prod

Table 2.14: Spearman’s rank correlation and p values for correlations among the food availability estimates and maintenance behaviors. There are no significant relationships among these variables.

Height p-value Grp Spd p-value Fruit Species 0 1 0.707 0.182 Fruit Trees -0.8 0.104 -0.5 0.391 Crop -0.8 0.104 -0.5 0.391 Production

Table 2.15: Spearman’s rank correlation and p values for correlations among the food availability estimates and mean height use and vertical group spread. There are no significant relationships among these variables.

112

Beach p-value Main p-value Mangrove p-value Fruit Species 0 1 0 1 0 1 Fruit Trees -0.9 0.037 -0.6 0.285 1 0.01 Crop -0.9 0.037 -0.6 0.285 1 0.01 Production

Table 2.16: Spearman’s rank correlation and p values for correlations among the food availability estimates and habitat type use. The only significant relationship was found between the number of individual trees fruiting and total crop production and the use of the mangrove habitat.

Species Site Travel Feed Forage Rest Socio- Other Source sex C. agilis Mondika, 31 33 8 13 10 5 Shah, 2003 CAR C. agilis Bai Hoku, 42 24.5 15 9.8 5.9 2.5 Devreese, CAR 2010 C. atys Taï, Côte 10 39 25 19 8 NA McGraw, d'Ivoire 1998 C. Tana 15 35 14 14 11 11 Homewood galeritus1 River, 1978 Kenya C. Tana 27 36 6 16 NA NA Homewood galeritus1 River, 1978 Kenya C. Sette 66 15.3 1.4 13.2 3.7 NA This study torquatus2 Cama, Gabon

Table 2.17: The maintenance activity patterns among the Cercocebus species. NA= data are not available. 1These data are for two groups at the same site. 2The activities for C. torquatus are rounded to compare to other genera.

113

Species % Travel Home Range (ha) Group Size C. agilis1 31 303 21-22 C. agilis2 42 1000 230 C. atys3 10 700-800 120 C. galeritus4 27 17 36 C. torquatus5 66 254 70

Table 2.18: The percentage of total time spent traveling, home range size, and group size among Cercocebus species. 1Shah, 2003; 2Devreese, 2010; 3McGraw, 1998; 4Homewood, 1978; 5this study.

0 1-5 6-10 11-20 21-30 +31 Site C. agilis 22 19 26 18 15 <1 Mondika, CAR1 C. agilis 72 10 8 8 2 <1 Bai Hoku, CAR2 C. atys 67.24 19.1 10.6 3 NA NA Taï, Côte d'Ivoire3 C. galeritus 51 NA NA NA NA NA Tana River, Kenya4 C. torquatus 39.4 30.08 10.4 11.44 8.64 0 This study

Table 2.19: The amount of time spent in each height class among the Cercocebus species. NA=data are not available or they were not found at these heights. 1Shah, 2003; 2Devreese, 2010; 3McGraw, 1998; 4Homewood, 1978

114

Figure 2.30: Scatterplot of the relationship between travel time and home range size among African papionins. All data (except C. torquatus) were taken from Swedell, 2011.

115

Chapter Three: Diet and Food Hardness

3.1 Introduction

A study of dietary specializations in primates would at best assemble information about three factors: 1. The structure and other attributes of the specialized characteristic itself (for example, a tooth’s dimensions and the rate and manner in which it wears down with use); 2. The diet of primates with that characteristic; and 3. The actual manner in which that characteristic helps to process dietary items (for example, how finely a particular kind of tooth grinds up a particular food). Richard 1985:189

There is also a fourth, vital component to any dietary study: the physical properties of foods, or the behavior of food materials under applied stress (Lucas et al.,

2008). The mechanical properties of foods are recognized as important selective pressures for adaptive change in dental and jaw morphology (Kinzey and Norconk, 1990;

Rosenberger, 1992; Yamashita, 1996). In particular, the consumption of obdurate foods is often associated with dental characteristics such as thick enamel, low, rounded molar cusps, or enlarged tooth area (e.g. Cebus, Kay, 1981; Rosenberger and Kinzey, 1976; L. albigena, Lambert et al., 2004; Paranthropus spp., Grine, 1988; Ungar et al., 2008;

Pithecia, Kinzey and Norconk, 1990). Studies have begun incorporating the material properties of food items eaten by primates and how these relate to dental anatomy and food processing techniques (Happel, 1988; Kinzey and Norconk, 1990; Yamashita, 1996;

Strait, 1997; Lambert et al., 2004; Wright, 2005; Teaford et al., 2006; Vogel et al., 2008;

Wieczkowski and Ehardt, 2009; McGraw et al., 2011; McGraw and Daegling, 2012).

116

Cercocebus and Mandrillus species are characterized by their enlarged

premolars, strong jaws, and limb adaptations for aggressive terrestrial manual foraging

(Fleagle and McGraw, 1999, 2002). These features are associated with a specialized, hard-object feeding niche that allows these species to compete with other sympatric primates. Two contrasting explanations have been proposed to describe the evolution of this skeleto-dental complex among Cercocebus and Mandrillus species. The first argues that durophagy is a fallback feeding strategy, and mangabeys (both Cerocebus and Lophocebus) only eat hard-object foods (such as bark or seeds) when preferred foods (fruits) are unavailable (Lambert et al., 2004; Wieczkowski and Ehardt, 2009).

Other researchers suggest that obdurate feeding is a habitual and regular occurrence among Cercocebus mangabeys and is one of the hallmarks of the Cercocebus-Mandrillus

clade (Cooke et al., 2009; McGraw et al., 2011; McGraw and Daegling, 2012). In order to

address these competing explanations, and also gain a greater understanding of the diet

and adaptations of C. torquatus, this study focuses on the following questions:

• What is the diet of C. torquatus? How does the C. torquatus diet compare to

other members of the Cercocebus genus?

• What are the physical properties of C. torquatus foods? How much of the C.

torquatus diet is comprised of obdurate foods?

• Is hard-object feeding a fallback strategy for C. torquatus and other Cercocebus

species?

Finally, I make some predictions regarding the oral processing behaviors of C.

117

torquatus based on preliminary research from Sette Cama and research conducted on C. atys, the sooty mangabey, at Taï National Park, Côte d’Ivoire (Daegling et al., 2010;

McGraw et al., 2011; McGraw and Daegling, 2012).

3.2 Background

Diet is a critical component in understanding a primate species and its adaptations. Primates are often classified based on gross dietary generalizations, such as folivores, frugivores, insectivores etc. The characterization of a primate’s diet into one category obscures the dietary complexity or variation that can occur both within and across populations (Chapman and Chapman, 1990; Chapman et al., 2002). For example, colobines are broadly classified as folivores, but research indicates that seeds comprise the majority of the diet for several colobine species including Colobus polykomos (western black and white colobus) and Procolobus badius (western red colobus) (Daegling and McGraw, 2001; Davies and Oates, 1994). Therefore, researchers are expanding beyond broad dietary characterizations to include these variations.

What a primate eats is based on a myriad of factors including anatomy and physiology, habitat type, interspecific competition, food availability, and individual preference (Lucas et al., 2003). Certain foods, such as mature leaves, require anatomical specializations for processing and digesting. For example, both howler monkeys and colobines have slow digestive rates to maximize leaf nutrient intake

(Milton, 1984). Additionally, colobines evolved a multi-chambered stomach that aids in leaf digestion (Chivers and Hladik, 1980; Lambert, 1998). Howler monkeys also adapt

118

behaviorally to their low-energy diet by spending most of their time resting (Milton,

1984). These adaptations allow them to eat foods other primates cannot.

Most primates also experience seasonality in food availability or periods when foods are scarce due to seasonal variation in the fruiting and leafing of tropical plants

(van Schaik et al., 2003). “Phenological variation at the level of the forest community affects primary consumers who respond by dietary switching, seasonal breeding, changes in range use, or migration” (van Schaik et al., 2003: 353). A primate’s reaction to food variability is limited by its behavioral, functional, and morphological constraints

(Chapman and Chapman, 1990). Therefore, some primates in a forest community, such as capuchins, turn to hard palm nuts during periods of low food availability, but they have thick dental enamel to facilitate this switch in food sources (Wright, 2005). Other species, such as squirrel monkeys or spider monkeys, may increase insect or leaf consumption during periods of scarcity because they lack the anatomical adaptations to process hard nuts (Terborgh, 1983).

Because of seasonal and overall variation in primate diets, researchers are now

focusing on how primates evolved to deal with a shifting feeding environment. These

adaptations may have shaped both primate behaviors (ranging and grouping

adaptations) and morphology (cranio-dental and gastro-intestinal adaptations).

I discuss two of the major feeding variables proposed to impact the morphology

of C. torquatus: the physical properties of food and dietary switching (or reliance on

fallback foods). An understanding of how C. torquatus has adapted to these variables

will aid in our understanding of extant form-function relationships within the entire

119 clade, and this information provides a valuable guide for reconstructing the diets and behaviors of extinct primates (such as Procercocebus antiquus) and hominins that feature similar morphological adaptations.

Before addressing the study results, the next section includes a review of the mechanical properties of foods, dental adaptations for processing hard foods, previous studies on hard-object feeding, and the concept of fallback feeding. These topics are then applied to the known information for the Cercocebus-Mandrillus clade. The next chapter will deal with any possible impacts of hard-object feeding and seasonal food availability on the ranging behaviors of C. torquatus.

Mechanical Properties of food

Primates make feeding decisions based on food characteristics such as texture, color, smell, size, and shape (Maas and Dumont, 1999; Lucas et al., 2003; Yamashita,

2003). Food choice is a compromise between ensuring adequate nutritional intake and minimizing the costs of obtaining those nutrients (whether it is avoiding toxins and mechanical defenses of plants or minimizing the time it takes to physically access or process a food) (Altmann, 2009). The so-called “packaging problem” or “…commingling of costs and benefits in accessing foods and other vital resources” has influenced both behavioral and physiological adaptations among primates for processing and obtaining foods (Altmann, 2009:615).

One of the least understood aspects of food choice are the mechanical properties of the foods themselves. In general, ripe fruit pulp is usually soft, easy to access, and simple to digest (Lucas et al., 2008). Seeds, which tend to be high in fats

120

and proteins, are often protected by a durable, lignified outer shell that is designed to

resist fracture (Peters, 1987; Kinzey and Norconk, 1997; Lucas et al., 2008). Different

cranio-dental adaptations are required for fragmenting more physically protected foods such as seeds, nuts, or unripe fruits compared to softer food items (Agrawal et al., 1997;

Strait and Vincent, 1998).

There are three main physical food properties that can be measured: toughness

(R), Young’s (or elastic) modulus (E), and hardness (H) (Yamashita, 1996; Lucas et al.,

2003; Yamashita, 2003; Lucas et al., 2008; Lucas et al., 2009). Most foods feature

different values for each food property (for example a food can be both hard and tough

or tough but soft), and thus, using one value to describe a food is an oversimplification

(Strait, 1997). Nevertheless, each property must be dealt with separately when

understanding the overall material properties of foods.

Toughness is the energy required to propagate a crack in a solid over a given

area (Yamashita, 1996; Strait, 1997; Yamashita, 2003; Williams et al., 2005; Lucas et al.,

2008; Williams et al., 2008; Lucas et al., 2012). Scissor or wedge tests are used to

determine the energy (force) required to propagate a crack (displacement) throughout

the material (Lucas et al., 2003; Williams et al., 2005; Lucas et al., 2012). Toughness is

usually associated with the structure and strength of cell walls, and foods that “can

withstand high strains before crack propagation are termed displacement-limited

foods…” (Wright et al., 2008: 1457). Leaves are the most commonly eaten

displacement-limited foods among primates.

121

Young’s (or elastic) modulus refers to the stiffness of an object (Strait, 1997;

Yamashita, 2003; Pampush et al., 2011). “The elastic modulus describes the rigidity of

an object through the ratio of stress (force/unit area over which it acts) to

corresponding strain (increase in length/original length) along the linear proportion of

the stress-strain curve” (Figure 3.1; Williams et al., 2005:332). In other words, the

higher the elastic modulus of a material, the stiffer it is. Stiffer foods require a higher

stress concentration buildup to initiate cracks that lead to fragmentation (Strait, 1997;

Yamashita, 2003). Any applied force prior to the yield point (point of permanent

deformation) will result in the solid returning to its original state. Forces beyond the

yield point lead to plasticity, or permanent damage to the material. Therefore, in order

for a primate to process foods with a high elastic modulus, it must be able to generate

enough force to reach the point of fragmentation.

The terms toughness and hardness have often been used interchangeably

despite them referring to different physical properties (Lucas et al., 2009). Hardness is

not a real material property, in itself, but a group of properties (Strait, 1997). Hardness

refers to the resistance of a material to indentation, and it is measured by calculating

the force of indentation required to leave a mark on a material (Tabor, 1951; Strait,

1997; Lucas et al., 2009). Foods that fracture under high stress but low strain are

considered hard (stress-limited) whereas foods that fracture easily are soft (Strait, 1997;

Lucas et al., 2003; Yamashita, 2003; Lucas et al., 2009; Daegling et al., 2011). Hard foods require high bite forces to initiate breakage. Hardness measurements are considered a

122 good approximation of the interaction between food particles and teeth, and therefore, primate foods are often measured for hardness (Yamashita, 1996; Lucas et al., 2003).

Shore hardness (MPa) is a commonly used value to represent the hardness of materials (Qi et al., 2003). Shore hardness does not give a direct measurement of the stress-strain relationship of materials, but the measurements roughly correspond with

Young’s modulus (Qi et al., 2003; Figure 3.1). In general, the higher the hardness value, the higher the Young’s modulus, and the more force required to cause permanent deformation of an object. However, the relationship between hardness and Young’s modulus varies depending upon the conversion equation used, and the hardness of softer foods tends to correspond less closely with elastic modulus (Qi et al., 2003;

Pampush et al., 2011). The mathematical calculations required to convert Shore hardness into Young’s modulus are beyond the scope of this study, but Shore hardness, in itself, provides researchers a reliable quantitative scale from which to compare foods across field sites and studies. Most researchers suggest that it is the harder foods that will impact the masticatory anatomy of food processing (Lambert et al., 2004;

Wrangham and Marshall, 2007; Marshall et al., 2009; Pampush et al., 2011).

Anatomical features related to physical properties of foods

Multiple factors combine to give teeth their particular properties and characteristics including enamel thickness, enamel structure, tooth size, and tooth morphology (Hillson, 1996; Maas and Dumont, 1999). A tooth is composed of a crown and a root (Hillson, 1996). Dentine forms the inner bulk of the crown and is covered by enamel. Although enamel is the hardest biological tissue, it is not replaced when lost

123

(except among aye-ayes) (Teaford, 2007). The inner part of the tooth, the root, is

covered by a layer of cement. Because enamel comes into direct contact with foods, it

is potentially impacted by wear (or dental attrition) related to the processing of dietary

items.

Wear is damaging to a primate’s fitness because it poses a threat to the integrity of a tooth. Wear occurs when fragments of the tooth are lost because of contact with

either food objects or other teeth (Lucas 2004). An object’s hardness is not the principle

cause for wear, but indentation (as measured by hardness) contributes to surface loss.

Wear is also likely caused by a combination of other factors including toughness and

Young’s modulus of the material being masticated. Because wear changes tooth shape

and erodes the surface, extreme wear is potentially fatal for the individual, either

directly or indirectly (Lucas, 2004; Elgart, 2010). For example, dental senescence was

associated with increased infant mortality during years with low rainfall among Milne-

Edwards’ sifakas due to decreased maternal nutrition (King et al., 2005).

Tooth durability and resistance to wear can be enhanced either by increasing the enamel thickness or overall tooth size (Shellis et al., 1998; Lucas, 2004; Ungar et al.,

2008). Indeed, enamel thickness and tooth size are two of the most discussed dental traits that impact feeding behaviors among primates.

Enamel Thickness

In general, the amount and distribution of enamel on teeth is a gross indicator of diet and dietary properties (Kay, 1981; Shellis et al., 1998; McGraw et al., 2012). Among most mammals, thicker enamel is associated with hard-object feeding (Kay, 1981;

124

Dumont, 1995; Ungar, 2008). For example, sea otters that feed on mollusks and crabs have thicker enamel than sea otters that rely on fish (Ewer, 1973 in Kay, 1981). Enamel acts as a tooth’s first line of defense against abrasive food particles, crushing stress, and wear (Shellis et al., 1998).

Two explanations have been proposed for variation in enamel thickness among mammals: “First, thick enamel may prolong tooth lifetime where chewing causes progressive surface loss. Second, it may enhance resistance to fracture from biting on hard objects” (Lucas et al., 2008:374). Multiple studies suggest that primates that feed on hard-object foods tend to have thicker enamel than other primates (Kay, 1981;

Dumont, 1995; Strait, 1997; Swindler, 2002; Lucas et al., 2008; McGraw et al., 2012), and therefore, enhanced enamel thickness provides a “buffer” against high occlusal forces (Ungar, 2007).

Among primates, thick enamel is considered an adaptation for a durophagous diet because thick enamel strengthens the tooth crown and delays tooth senescence

(Kay, 1981; Lucas, 2004; Vogel et al., 2008). For example, Cebus apella has among the thickest dental enamel of all primates, and they subsist on hard palm nuts (Kay, 1981;

Shellis et al., 1998). In contrast, thin enamel is associated with soft fruits or leaves. Thin enamel forms edges or crests that help in slicing or shearing actions (Happel, 1988;

Lucas, 2004). In their comparison of enamel thickness and fallback feeding among hominoids, Vogel et al. (2008) found that the thinner enameled chimpanzee species relied more often on leaves during periods of fruit scarcity compared to the thicker enameled orangutans which ate consistently ate harder and tougher foods. In this case,

125

orangutans routinely process foods (such as seeds) of higher hardness values than

chimpanzees, and orangutans do not only rely upon hard foods as a fallback resource.

Nevertheless, enamel thickness is not always a prerequisite for hard-object feeding. Certain populations of ring-tailed lemurs consume hard tamarind fruits despite having thin enamel (Cuozzo and Sauther, 2006; Sauther and Cuozzo, 2009). These lemurs experience extreme tooth wear and antemortem tooth loss. This reliance on tamarinds as a “fallback food” is associated with the extreme anthropogenic disturbances of their habitat.

Tooth size

Enlarged tooth or cusp size should also prolong the life of a tooth in the face of wear and use (Grine, 1988; Strait, 1997; Lucas, 2004; Ungar et al., 2008). The robust australopithecines, or Paranthropus spp., are characterized by huge posterior dentition with flat occlusal surfaces and thick enamel (Grine, 1988; Ungar et al., 2008). This tooth morphology is hypothesized as an adaptation for the consumption of either hard or abrasive foods (Grine, 1988; Ungar et al., 2008). Among mantled howler monkeys

(Alouatta palliata) on Barro Colorado Island, a study on molar size and fitness found that individuals with smaller molars suffered higher mortality rates at weaning than those with larger molars (DeGusta et al., 2003). Therefore, it is predicted that primates eating harder foods (which presumably suffer higher chance of wear) should have larger posterior teeth than soft food feeders. However, Daegling and colleagues (2011) found that not all of the primate taxa with the highest P4/M1 ratios were obdurate feeders.

126

Several tooth designs aid in breaking down stiff (or hard) materials. Smaller primates that feed on hard-bodied insects benefit from having small, sharp cusps (Strait,

1997). This maximizes the force concentration for any given load. Smaller primates also have smaller jaw musculature which gives them less overall force producing capabilities.

Other primates, which feed on non-insect stiff materials, face a compromise between tooth integrity and tooth design (Strait, 1997). By increasing the cusp angle, more strain energy is generated, thus fracturing the solid. The wider cusp angle and tooth area reinforces the strength of the tooth and prevents breakage when facing repeated contact with stiff foods.

Given these properties, durophagous taxa are predicted to have molars with short, blunt cusps and large basins to induce crack initiation (Lucas, 1979; Yamashita,

1996). The larger surface area of the tooth allows more room for the occluding cusps to contact and potentially breakdown foods. The bilophodont molars of cercopithecines and several lemur species are also proposed as an adaptation for puncturing and crushing seeds by acting as wedges to fracture hard seed coats (Happel, 1988;

Yamashita, 1996). These tooth features represent diverse morphological solutions to the problem of eating hard foods.

Previous studies on hard-object feeding

Although researchers proposed a correlation between hard-object feeding and thick dental enamel and enlarged tooth size, most studies neglected to actually measure the properties of foods being eaten or define a “hard-object” food. Kinzey and Norconk

(1990) conducted one of the first investigations into the relationship between dental

127 morphology and food properties. They compared the puncture and crushing resistance of fruits and seeds eaten by sympatric black spider monkeys (Ateles paniscus) and bearded saki monkeys (Chiropotes satanas). Saki monkeys have divergent canines and procumbent lower incisors which were proposed adaptations for feeding and resource partitioning between these species. Indeed, Kinzey and Norconk (1990) observed sakis opening foods of higher puncture resistance such as unripe husks or fruits that spider monkeys ignored. They termed this style of feeding “…sclerocarpic harvesting or the preparation and ingestion of hard fruit” (Kinzey and Norconk 1990:13). The saki monkeys, however, did not eat seeds of especially high crushing resistance. By opening unripe husks and fruits, the sakis were able to access unripe seeds that contained fewer toxic chemicals.

Since the initial study by Kinzey and Norconk (1990) other researchers have examined the role of food properties in shaping dental adaptations and food choice.

Research suggests that there is a correlation between durophagy and dental characteristics such as thick enamel or enlarged tooth area among multiple primate taxa

(Lophocebus mangabeys: Lambert et al., 2004; Cebus apella: Wright, 2005; Orangutans:

Vogel et al., 2008; Harrison and Marshall, 2011). These features allow these species to choose “harder” foods not available to other primates during periods of preferred food scarcity. However, Yamashita (1996) found that durophagy occurred year-round in several species of lemurs and indrids and, for the most part, hardness did not impact food choice.

128

Many studies now suggest that dental adaptations evolved as a solution to

feeding on hard-objects as “fallback foods” (Lambert et al., 2004; Marshall and

Wrangham, 2007; Marshall et al., 2009). The concept of fallback feeding has also been

introduced as an explanation for the unique suite of characteristics found among the

Cercocebus-Mandrillus clade. Nevertheless, the definition of fallback foods and what it

means to rely on these resources remains unclear.

Fallback foods: redefining a nebulous concept

Researchers are more frequently using the term fallback foods in response to the

observed variation in primate diets. “Fallback foods are becoming increasingly invoked

as key selective forces that determine masticatory and digestive anatomy, influence

grouping and ranging behavior, and underlie fundamental evolutionary processes such

as speciation, extinction, and adaptation” (Marshall et al., 2009:603). In most cases,

researchers assume that fallback foods are physically harder or more difficult to process

than preferred foods (Lambert et al., 2004; Lucas et al., 2009). Despite the increased

usage of the term fallback foods, there are many different interpretations of what

constitutes and typifies a fallback food.

Many earlier studies referred to fallback foods as “keystone resources”

(Terborgh, 1986; Tutin et al., 1997; White, 1998). In ecological theory, keystone

resources are important foods for several species, and the loss of this food would cause

considerable ecological disruption (Paine, 1969; Terborgh, 1986). However, many

researchers have erroneously applied this term to primates in reference to foods eaten

during periods of scarcity. For example, Tutin and colleagues stressed the presence of

129

“keystone resources” for the primate community at Lopé, Gabon (1997). Keystone

foods, in their definition, were foods that were relied upon by frugivores during times of

fruit scarcity. “Compared to fruit, many alternate foods are less nutritious, harder to

digest, less easy to process and more time consuming to harvest” (Tutin and White,

1998:332). The choice of keystone foods was related to morphological constraints.

Several primate species, including L. albigena and M. sphinx, aided by their powerful

jaws, increased their intake of mechanically protected immature seeds of Pentaclethra

macrophylla during these fruit scarce periods. The soft P. macrophylla seeds are

surrounded by a durable pod that cannot be opened by guenons or apes.

In an attempt to clarify how the term fallback food is used and distinguish it from

keystone resources, Marshall and Wrangham (2007) developed a framework to identify

fallback feeding among primates. They define fallback foods as “…foods whose use is

negatively correlated with the availability of preferred foods” (Marshall and Wrangham,

2007: 1220). Preferred foods are those foods that are overselected relative to their

abundance. However, it is difficult to define preference in most studies because of

logistical limitations (length of study, biased sampling, etc.), and no single methodology

exists for calculating preference (Marshall and Wrangham, 2007).

The authors suggest that preferred and fallback foods select for different adaptations among primates (Marshall and Wrangham, 2007; Marshall et al., 2009).

Because preferred foods tend to be rarer and harder to locate, they select for harvesting adaptations in locomotion or cognition. Locomotor adaptations include efficient travel between food patches. Fallback foods, on the other hand, tend to be more abundant

130

and harder to process. Therefore, these foods are related to dental or physiological

adaptations associated with food processing. These features include thicker dental

enamel, such as that found among orangutans compared to other apes, or the

forestomach fermentation of colobines (Davies, 1994; Marshall and Wrangham, 2007;

Vogel et al., 2008).

Fallback foods are also divided into categories based on their dietary contribution (Marshall and Wrangham, 2007; Marshall et al., 2009). Staple fallback foods can seasonally serve as 100% of the diet whereas filler fallback foods account for the entire diet. This suggests that staple foods have more impact on adaptations than

filler foods.

Lambert (2007) also expands upon the definition of fallback feeding by

introducing the concept of fallback feeding strategies. She suggests that low-quality

fallback foods should select for anatomical strategies for processing (such as thick dental

enamel) whereas high quality fallback foods should select for behavioral strategies (such

as fission-fusion subgrouping). Lambert argues that these adaptations arise, not

because foods are consumed regularly, but instead, adaptations evolve during “critical”

periods of food shortage (2004, 2007). A critical period is a time “…of extreme food

scarcity, during which heightened resource competition imposes substantial mortality”

(Marshall et al., 2009:604). For example, the thick dental enamel of Lophocebus is

proposed as an adaptation for feeding on abundant, low-quality fallback foods (such as

bark) when ripe fruits are scarce. Therefore, rather than selection acting for preferred

131

foods, in this case, these adaptations serve as solution to highly seasonal food

availability.

The definition of fallback feeding proposed by Lambert (2007) compliments that

put forth by Marshall and Wrangham (2007). Both frameworks suggest that high-quality

foods are harder to find but easier to process, and, therefore, select for harvesting

adaptations, whereas low-quality foods are easier to find but require adaptations for processing (Lambert, 2007; Marshall and Wrangham, 2007; Harrison and Marshall,

2011). Nevertheless, this framework for fallback feeding is only beginning to be tested, and exceptions are starting to appear (orangutans: Harrison and Marshall, 2011).

Therefore, researchers also need to remain open to the idea that hard-object feeding

may not always be a fallback adaptation in all primate species, and it cannot always be

invoked to explain the evolution of cranio-dental adaptations for durophagy (McGraw et

al., 2011; McGraw and Daegling, 2012). Furthermore, fallback feeding may not always

match with dental features (as in the tamarind fruit feeding among thin-enameled ring-

tailed lemurs; Cuozzo and Sauther, 2006; Sauther and Cuozzo, 2009).

Morphological adaptions for durophagy in Cercocebus

The jaw morphology and dentition of Cercocebus and Mandrillus feature

adaptations for hard-object feeding (Fleagle and McGraw, 1999, 2002; Wieczkowski and

Ehardt, 2009; McGraw et al., 2011; McGraw and Daegling, 2012). Cercocebus (and the

genus Lophocebus) has frequently been described as having thick dental enamel (Kay,

1981; Dumont, 1995; McGraw et al., 2012), powerful jaws (Hylander, 1975), and a facial

configuration that enables them to produce large occlusal forces (primarily Lophocebus;

132

Daegling and McGraw, 2007; Singleton, 2005). In addition, Cercocebus and Mandrillus

possess molarized premolars and relatively large incisors (Fleagle and McGraw 1999,

2002). This constellation of features has led some researchers to suggest that hard-

objects are a fallback resource for mangabeys in general (Lambert et al., 2004;

Wieczkowski and Ehardt, 2009).

Both mangabey genera have extremely thick dental enamel compared to other

primates (McGraw et al., 2011; McGraw et al., 2012). In a comparison of M2 enamel

thickness among catarrhines, Kay (1981) found that L. albigena and C. torquatus had the highest relative enamel thickness values for all Old World species studied. C. torquatus was found to have a slightly higher level of enamel thickness than L. albigena.3 Further

studies on Cercocebus and Lophocebus taxa reveal that both genera feature high M2 enamel thickness compared to most other primate groups (McGraw et al., 2012), and dietary data indicate that both genera are obdurate feeders in some capacity (Chalmers,

1968; Tutin et al., 1997; Wahungu, 1998; Shah, 2003; Lambert et al., 2004; Wieczkowski,

2009; Cooke et al., 2009; McGraw et al., 2011). Regardless of which mangabey genus has the thickest enamel, this adaptation enables both genera to feed on hard-object foods.

Cercocebus and Mandrillus also possess exceptionally large incisors relative to other cercopithecid genera (Hylander, 1975; Shellis and Hiiemae, 1986). Large incisors

3 Dumont (1995) suggests that C. torquatus does not have thick enamel compared to L. albigena and attributes this to differences in dietary properties. Dumont (1995) erroneously classified C. torquatus as a soft-food specialist (McGraw et al., 2012) and newer investigations into the enamel thickness of Cercocebus and Lophocebus coincide with studies conducted by Kay (1981).

133

are associated with foods that require processing before movement to the posterior

teeth for mastication (Hylander, 1975). Thus, larger incisors are more resistant to wear

than smaller incisors. “…[I]ncisors are used in food preparation, providing access to

fruits of a range of hardness values” (Happel, 1988:320). This is illustrated by two

species of orangutans that use their incisors in different manners to process hard fruits

(Ungar, 1994). P. pygmaeus crushes hard fruits with their incisors while P. thomasi used incisal puncturing to remove hard shells in several pieces.

Cercocebus use their incisors to pierce fruit pericarps and endocarps (Happel,

1988; Shah, 2003; Cooke and McGraw, 2009; McGraw et al., 2011). Shah (2003) noted

“Strychnos aculeata, large, hard fruit that resemble small bowling balls, were hitherto thought to be opened only by elephants, but agile mangabeys are able to open them by scraping a hole using their incisors” (41). Happel (1988) suggested that mangabeys were limited in the pericarp hardness that could be processed with their incisors, but sooty mangabeys were observed using incisal processing on even their hardest food objects

(McGraw et al., 2011). Mandrills and drills were also observed using their incisors for food processing and were described as “strippers and pithers” (Caldecott et al.,

1996:83).

Cercocebus, Mandrillus, and Lophocebus share thick dental enamel and enlarged incisors. However, Cercocebus and Mandrillus feature expanded premolars, a trait not found among Lophocebus species (Fleagle and McGraw, 1999, 2002). Lophocebus mangabeys have smaller premolars than both Cercocebus and the papionin outgroup, macaques. On the other hand, Cercocebus species have the highest ratio of P4/M1

134

measurements compared to all other anthropoids (Daegling et al., 2011). Even the

earliest known member of this clade, Procercocebus antiquus, displays enlarged

premolars (Gilbert, 2007). These differences in premolar size suggest that Cercocebus

evolved to process obdurate foods differently than Lophocebus mangabeys. Therefore,

it is important to understand how the dental morphology of Cercocebus mangabeys

relates to the placement of food prior to mastication. This establishes a functional

relationship between dentition and food properties and helps to determine if molarized

premolars are an important adaptation for hard-object feeding.

The expansion of premolar size should enhance crushing abilities by increasing

the surface area on which to generate a force. This facilitates crack initiation in highly

fracture resistant foods. Happel (1988) noted that Cercocebus mangabeys use their

premolars to open hard pericarps. McGraw et al. (2011) conducted the first detailed

investigation into ingestive behaviors and observed sooty mangabeys using postcanine

crushing actions only when processing their two hardest foods, S. gabonensis seeds and

C. edulis nuts. C. atys consumed S. gabonensis seeds in the following manner:

…[F]ollowing manual harvesting from the leaf litter of the forest floor, the monkeys may scrape off any adherent material, and attempt to puncture the seed casing, all using the incisors. The casing is then placed behind the canines and one or more isometric bites are applied to shatter the object. This is followed by explusion of fragments and/or seeds from the oral cavity, a short bout of mastication, or placement in the cheek pouch for later processing (Daegling et al., 2011:2).

The expanded premolars of C. atys enable them to open the S. gabonensis seed without having a facial configuration capable of producing the high bite forces needed to cause catastrophic failure of this material (Daegling et al., 2011; McGraw and Daegling, 2012).

135

An examination of the microwear signature of C. atys posterior dentition also revealed pitting and complex wear patterns associated with the consumption of stress- limited foods (Daegling et al., 2011). These observations, along with the heavy wear on most other Cercocebus species premolars, indicate that these species use them as tools to crack open hard-food objects, a behavior not seen among Lophocebus mangabeys. It is important to note, however, that not all primate species with enlarged premolars are necessarily hard-object feeders and not all durophagous taxa feature premolar expansion (Daegling et al., 2011; McGraw and Daegling, 2012).

Clearly, Cercocebus, Mandrillus, and Lophocebus have adaptations for feeding on obdurate foods. However, the degree of reliance on these foods and how they are gathered and processed are proposed to differ between clades. This had led to an increased interest in studying the relationship among food properties, cranio-dental morphology, and food processing within Cercocebus species. Nevertheless, even basic dietary data and quantitative measures on the mechanical properties of foods are not yet available for many Cercocebus species.

Diet in Cercocebus and Mandrillus

Cercocebus-Mandrillus species are most commonly classified as frugivorous seed predators with adaptations for processing hard-object foods (Hoshino, 1985; Lahm,

1986; Caldecott et al., 1996; McGraw, 1996a; Rogers et al., 1996; Fleagle and McGraw,

1999, 2002; Shah, 2003). Seeds are a high-quality resource that provides a high concentration of fats and proteins (Peters, 1987). Cercocebus, mandrills, and drills also

136

feed on insects, mushrooms, and terrestrial herbaceous vegetation that occur in small,

dispersed clumps.

Diet profiles are not available for all the Cercocebus species (Table 3.1), but their diets are mostly composed of fruits and seeds. The exception to this trend is C. atys at

Taï (McGraw et al., 2011). Sooty mangabeys eat primarily seeds (55.4%) and invertebrates (13.01%). However, when seeds are counted separately from the fruit pulp, seeds account for as much as 42% of the diet in some C. galeritus populations and

34% of mandrill diets (Table 3.1).

Researchers have only recently begun to examine the physical properties of

Cercocebus foods (Wieczkowski, 2009; Cooke and McGraw, 2009; Daegling et al., 2010;

Pampush et al., 2011). These studies suggest that a significant amount of the

Cercocebus diet is hard foods inaccessible to other primate species. For example, the

Sacoglottis seeds eaten by both C. atys and C. torquatus have extremely high Shore hardness values (Cooke and McGraw, 2009; McGraw et al., 2011). Indeed, chimpanzees at Taï need to use tools to open the hard endocarp of the Sacoglottis seeds (Boesch and

Boesch, 1982; McGraw et al., 2011). Tana River mangabeys were observed eating some very hard seeds with hardness values exceeding the values of other known hard-object feeders such as L. albigena (Lambert et al., 2004) and pitheciins (Kinzey and Norconk,

1990; Wieczkowski, 2009).

The suite of cranio-dental features found among Cercocebus and Mandrillus has led mangabey researchers to speculate on the evolutionary significance of this obdurate feeding niche. Researchers disagree as to the importance of hard-object foods within

137

this clade: either they are considered facultative fallback foods, eaten when fruits are

not available (Wieczkowski and Ehardt, 2009) or Cercocebus are habitual hard-object

feeders (Cooke and McGraw, 2009; McGraw et al., 2011; McGraw and Daegling, 2012).

The key data needed to understand the role of obdurate feeding among Cercocebus

species are the physical properties of foods and the contribution of hard foods to the

overall diet compared to food availability.

3.3 Research Questions

I present information on the diet and physical properties of C. torquatus

foods in Sette Cama, Gabon. For this study, I address the following questions:

• What is the diet of C. torquatus in Sette Cama, and how does their diet compare

to C. torquatus at other sites and to other Cercocebus species?

• What are the Shore hardness values of C. torquatus foods, and how do these

values compare to other Cercocebus species?

• Does C. torquatus show a preference for certain food items in correspondence

with availability?

These data are then used to evaluate two competing explanations for the adaptive role of durophagy among Cercocebus taxa: 1) Hard-object foods serve as fallback items during periods of preferred food scarcity; or 2) Cercocebus mangabeys are adapted for the routine consumption of obdurate foods.

138

3.4 Predictions

1. The diet of C. torquatus will be comprised mostly of fruit and seeds as seen in

other Cercocebus species. However, C. torquatus will eat foods of equal or higher hardness values than those foods eaten by other Cercocebus species.

The diet of C. torquatus should be similar to other mangabeys and include fruits, seeds, and hard-object foods. C. torquatus foods should be at least as hard as those eaten by C. atys and C. galeritus. C. torquatus has the thickest dental enamel of all

Cercocebus species studied, and they exhibit extreme posterior and anterior dental wear. Therefore, C. torquatus may also be able to eat harder foods than other

Cercocebus species.

2. If obdurate feeding is a fallback strategy for C. torquatus, these foods should be eaten only when preferred foods (fruits and other soft foods) are scarce. According to fallback feeding theory as outlined by Lambert (2007) and Marshall and Wrangham

(2007), the cranio-dental characteristics of Cercocebus mangabeys are adaptations to obdurate feeding during times of food scarcity.

Current interpretations of fallback feeding suggest that hard-objects foods are most often consumed when preferred foods are limited (Lambert, 2007; Marshall and

Wrangham, 2007). For frugivorous primates, fruits classify as preferred foods.

Therefore, the thick dental enamel and molarized premolars of C. torquatus evolved to process obdurate foods only eaten primarily during periods of low fruit availability.

139

3. If obdurate feeding is habitual for C. torquatus, these foods should be consumed every month, and the percentage of contribution of hard foods to the diet should not be significantly negatively correlated with consumption of soft foods.

Contrary to the hypothesis that Cercocebus eats hard-object foods only during critical periods, others suggest that obdurate foods are the main component of this genus’ diet (Cooke and McGraw, 2009; McGraw et al., 2011). If this is true, C. torquatus should eat obdurate foods year-round, and they should continue to eat hard foods even when other foods (such as fruits) are available.

3.5 Methods

Study site and Subjects

Data were collected on a group of red-capped mangabeys (N=70) in the Sentier

Nature forest of Sette Cama, Gabon. The Sentier Nature Forest is a protected area that borders south Loango National Park and is contained within the Gamba Park Complex.

Annual rainfall is 2093 mm (Lee et al., 2006). The annual temperature is 24˚-28˚ C, and there are two dry seasons from June to September and January to February. The forest covers approximately 254 ha and is bordered on the west by the Atlantic Ocean, on the east by the Ndougou Lagoon, and on the north and south by tourist camps. Sentier

Nature features a mosaic of habitat types including mangrove, terra firme, and coastal palm forests.

140

Behavioral Data Collection

Data collection occurred in two phases: the habituation period and the post-

habituation period. Dietary data was collected during both periods, but the results are

presented and analyzed separately.

Phase 1 (February 2008 – February 2009): Habituation

The goal of the habituation period was to get the C. torquatus group used to researcher presence in order to collect systematic data. My field assistants and I entered the forest daily for five days (not necessarily consecutive) each week beginning at 7:00 AM. Each day we would walk the trails slowly listening for mangabey vocalizations or visual identification of the group. Once the group was located, we followed them until they ran into the inaccessible swamp zone each day. We then waited outside the swamp zone for the mangabeys to return to the other sections of the forest. Usually, they did not leave if they could detect our presence. Therefore, we changed our strategy and left the field and returned back in an hour or two, depending upon the time of day, to try and find the group again.

During daily encounters, any foods eaten by C. torquatus were noted. The foods that were recorded included species that were directly observed being ingested by C. torquatus and fresh food remains left on the ground after the group had moved. The species of food eaten was only recorded the first time it was observed each day regardless of how many times we saw mangabeys eating that food. Therefore, the dietary data from this research period do not accurately reflect the average daily intake of a particular food type. Rather, the goal of data collection in this period was to

141

estimate the overall breadth of the C. torquatus diet and monthly variations in food species eaten because focal follows were impossible. It is possible that some foods were erroneously attributed to the mangabey group. Cercopithecus cephus occasionally joined C. torquatus in polyspecific associations and may have been eating the food remains that dropped to the ground.

Phase 2 (May 2009 – September 2009): Systematic behavioral data collection

Systematic behavioral data were collected five days a week (not always consecutive) for a period of nineteen weeks from May – September 2009. Data collection occurred each morning from 7:00 am to 12:00 pm and each afternoon from

2:30 pm until dusk. The monkeys spent most mid-days resting in the inaccessible

swamp zone, and therefore, we were unable to obtain data during these hours.

Behaviors were studied using ten minute group scans every twenty minutes

(Altmann, 1974). The number of individuals recorded in each scan varied from 1 to 36,

and the average number of individuals sampled per scan was 9.85. Every effort was

made to sample all individuals of the group during each scan; however, each group scan

represents only a subset of the entire C. torquatus group/subgroup under study. Issues of habituation, visibility, and large group spread made whole group scans not feasible at this site.

During group scans, for each individual seen, the data collected were: sex, age class (adult, subadult, juvenile), maintenance activity (travel, feed, forage, rest, socio-

sexual, other), height above ground or in the trees (visually estimated in meters),

142

positional behavior (locomotion and posture), forest zone, support size, and habitat

type (see Chapter 2 for more detailed descriptions).

Feeding was defined as the processing (with hands, teeth, or lips) or mastication of food items. Cheek pouch feeding (placement of food into the cheek pouch or eating

foods from the cheek pouch) was also recorded, and these observations were combined

with feeding for the data analysis. When feeding from their cheek pouches, the food

was only noted if I had observed the items placed in the pouch and was certain what

food was being ingested. Foraging was the search for foods prior to ingestion. During

feeding and foraging scans, I recorded the food species, the part eaten (pulp, seeds,

leaves), and ripeness (when applicable). A food was recorded as unknown if it was not

certain what an individual was eating. This was particularly problematic during periods

of foraging and feeding on the forest floor because C. torquatus movements were very quick and often obscured from view. Foods were identified using local plant guides

(Raponda and Sillans, 1995; White and Abernethy, 1999) and in consultation with the

Sette Cama village chief.4

Food Properties

For this study, only the hardness values of foods were measured. Toughness is

much more difficult to quantify in a field setting (Lucas et al., 2003). There is no

4 It is important to note that these data do not represent the entire annual diet of C. torquatus in Sette Cama. Because of this, the amount of fruit in the diet may be underrepresented. Several important fruit species (Dialium, Manilkara) do not fruit until December – February (pers. obs.) and therefore, the contribution of fruit to the overall diet is likely higher than that observed during the May – September 2009 study period.

143

standardized methodology or tool for measuring food hardness in the field, and

researchers must rely on instruments that are portable, low-cost, and efficient (Lucas et

al., 2001; Lucas et al. 2003, Pampush et al., 2011). One of the more commonly used

instruments for determining hardness is a Darvell HKU mechanical tester (Lucas et al.,

2003; Lucas et al., 2009). However, this instrument is expensive ($10,000) and requires

a laptop or computer to calculate hardness values (Lucas et al., 2003), and at many field

sites (including Sette Cama) electricity is not reliably available.

For this study, I tested a new method for measuring hardness of food items using

a highly portable, light-weight, handheld durometer that requires no electricity. The

Asker handheld durometer (Hoto Instruments; Figure 3. 2) is designed to measure the

hardness of plastic and rubber. Durometers provide an estimate of Shore hardness and

come in different types depending upon the force it is able to generate. The C.

torquatus foods were measured using both a Type A and Type D Durometer. The Type A durometer is suitable for softer materials such as sponges and normal rubber, and the plunger size is larger and flatter (Figure 3.3). The Type D durometer is designed to measure harder materials, and the plunger size is smaller and pointed. The smaller Type

D plunger generates a greater pressure on initial contact than the Type A plunger (Strait,

1997; Figure 3.4).

Whenever C. torquatus was observed feeding, samples of these foods were collected from the field and placed in ziplock bags. The samples were measured within three hours of collection back at the field station. The durometer was first calibrated, and then the plunger was slowly placed on the food at a constant rate. The maximum

144

score for each measurement was recorded. The test was repeated five times and the

results averaged. Foods were first measured with the Type A durometer. If a food’s

measurements reached 50 or above on the Type A durometer, the food was then measured with the Type D durometer.

Measurements were taken on or near the parts of the foods that were processed or consumed. The exocarp is the outside protection of the fruit (or the skin); the mesocarp is the fleshy area underneath the exocarp, and the endocarp is the seed casing (Figure 3.5). The exocarp was measured when the pulp (or mesocarp) was eaten.

If a seed was encased by a hard outer shell (endocarp), then this part of the seed was measured, as well as the seed itself.

When collecting hardness values, plunger placement on the object being measured can affect the readings obtained (Pampush et al., 2011). For example,

Sacoglottis gabonensis seeds feature “pockets” of air where the material is less dense and may not offer a true reading of hardness (Figure 3.6). Therefore, I took precautions to measure foods in the same general area with each consecutive reading.

3.6 Data Analysis

Behavioral Data

A dietary profile for both study periods was calculated by dividing the number of each particular food species recorded by the total number of feeding/foraging observations. The dietary profiles include both individual food species and general food categories.

145

In order to address the assertion that certain foods act as a fallback resource for

C. torquatus, feeding preference was estimated. In this case, “…preferred food items are selected disproportionately often relative to their abundance within the population’s habitat” (Marshall and Wrangham, 2007:1221). In other words, preferred foods are selected in positive correlation with availability, or they are overselected

(Wieczkowski and Ehardt, 2009).

Preference is hard to determine because of the short duration of most feeding

studies (this study included) and the complexity of primate habitats (Marshall and

Wrangham, 2007). However, I used the estimate employed by the only other

Cercocebus study examining food preference (Wieczkowski and Ehardt, 2009), and the

method that fit with my available data. These data provide a preliminary approximation

of how C. torquatus is utilizing its food sources in relationship to availability.

Food availability from May – September 2009 was measured using the

phenological samples of ten fruiting trees (5 individuals/species). The mean DBH and

density were also calculated for each species using 13- 100m x 10m transects. These

measures were then used to estimate the food crop score of each species by multiplying

mean phenological score x mean DBH x density (Wieczkowski and Ehardt, 2009). Data

were tested for normality and considered normal if the skew or kurtosis were no greater

than two times the standard error.

Food crop scores from the May – September 2009 sample period were

compared to the relative contribution of each dietary category to test for correlations

using Pearson’s correlation coefficient with a significance value of p=0.05. Pearson’s

146 correlation coefficient tests the null hypothesis that there is no linear association between two variables (Madrigal, 1998). Foods were also divided into “hard,” “soft,” or

“cross-over” (see below) and tested for any associations between availability and monthly percent contribution to the diet. This tests if a particular food group serves as a fallback resource (as defined by Marshall and Wrangham, 2007) for C. torquatus.

Food Properties

Foods were classified as “softer-pliable,” “harder-stiffer,” or “cross-over” based on Shore hardness measurements (as defined by Pampush et al., 2011). Foods were divided according to the following criteria (Daegling, pers commun; Pampush et al.,2011).

Softer-pliable: Type A measurements of 0 – 70

Harder-stiffer: Type A measurements of 70+, Type D measurements of 30+

Cross-over: Type D measurements of 0 – 30

For comparison, some common human foods that fall into each category are

(Pampush et al., 2011):

Softer-pliable: Yam, broccoli, avocado meat, coconut meat

Harder-stiffer: coconut husk, black walnut

Cross-over: avocado pit

The Shore hardness values for each food sample were averaged by species and the standard deviation calculated. Kruskal-Wallis tests were performed to determine if the monthly average hardness values of foods were significantly different.

147

3.7 Results

Pre-habituation scans

C. torquatus feeding observations were collected on 110 days from February

2008- December 2008. Data collection was interrupted from November 2008 –

February 2009 (by a BBC film crew), and therefore, trips into the forest during these

months were limited.

C. torquatus were observed eating 26 different species of foods over the prehabituation period (and 10 unknown items) (Table 3.2). Figure 3.7 presents the number of feeding observations each month and the number of food species identified each month. The most feeding observations were obtained in June 2008 followed by March

2008. These were also the months with the most variety in food species eaten. The lowest number of feeding observations (6) occurred in both August and November

2008. These months also featured the least variation in food species observed.

The breakdown of foods by category is presented in Figure 3.8, and Figure 3.9 and Table 3.3 show the frequency of observations of each food species. Note that these data represent the number of times a particular food was observed at least once during daily observations. In other words, C. torquatus were observed eating Manilkara fruits during 19 out of the 110 observation days. This can only provide a rough estimate of the contribution of each food to overall C. torquatus diet.

148

Fruits were the most commonly observed food type (52.1%) followed by seeds

(29.2%) and crabs (11.7%) (Figure 3.8)5. Leaves, invertebrates, and bark made up the rest of the observations during habituation. Guibortia seeds were eaten during 15% of the total observation days, crabs were eaten during 11.7% of the total observation days, and Sacoglottis seeds were eaten in 8.3% of the days (Table 3.4). Guibortia seeds, crabs, and Sacoglottis seeds were also eaten in the most number of months compared to other foods (eight, seven, and six months, respectively). Crabs and Sacoglottis seeds are available for most of the year, however, the availability of Sacoglottis seeds diminishes from July – October when the Sacoglottis fruits are fruiting (pers. obs). It is not known if the consumption of crabs is opportunistic or if C. torquatus deliberately seek out crabs.

This is the first time C. torquatus were observed eating crabs at any study site. Again, the difficulty of identifying food items obtained from the forest floor must be stressed; it is likely C. torquatus were consuming insects, fungi, and other foods from the ground that were impossible to see from a distance. Therefore, these items are most likely underrepresented in the dietary data.

Systematic Feeding Data

From May – September 2009, 216 individual feeding and foraging records were recorded. The total number of feeding observations varied monthly (Figures 3.10 and

3.11) with the most individual records in August (87) followed by September (50). May

5 Although crabs are invertebrates, this food was separated from other invertebrates because of the importance of this food item during certain times of the year.

149

contained the fewest feeding records (10), and this was also the first month of

systematic data collection.

Twelve different foods species were eaten (not including unknowns; Table 3.5

and Figure 3.10). The top three species eaten were Guibortia seeds, Sacoglottis fruits, and Sacoglottis seeds. Guibortia seeds were eaten in four out of the five study months and comprised the majority of the diet (26.4%) during the study period (Table 3.6).

Guibortia trees fruit during the dry season (June – September). Once the fruits are ripe, the soft seeds (which are encased by a durable exocarp) are eaten by C. torquatus.

Sacoglottis fruits accounted for 25% of all feeding records, and these fruits are an important resource for several other species including elephants (Morgan, 2009).

The consumption of Sacoglottis fruits occurred in August and September, when the fruits became ripe (see Chapter 2). Dried Sacoglottis seeds (17.1%) were eaten in four

out of the five study months. Phenology data from this study suggests that S.

gabonensis seeds are available year-round, however, the number of seeds on the

ground decreases from July – September. This is probably due to the depletion of seeds

that were left over from the previous year’s fruit harvest. Several other foods, which

are also available for most of the year, were eaten. Hyphanae guineensis palm fruits

and insects were eaten in two of the five months. Various other seed and fruit species

comprised the remainder of the C. torquatus diet from May – September 2009.

The total number of food species observed by month varied (Table 3.6 and

Figure 3.11). The highest species variation was in August (8 species) and the least was in

May (2 species). This corresponds with the results from the phenology analysis (see

150

chapter 2). The months of the highest food species availability were between July and

September.

When combining foods into the different food types, seeds made up the majority

of the C. torquatus diet (45.8%) followed by fruits (38%) during the sample period

(Figure 3.12). Insects, leaves, crabs and other items comprised the remainder of the C. torquatus diet (3.8%). In at least 12% of the records, the food item was either an unknown species or the food item was not visible for identification. These data are

different from the dietary diet collected on C. torquatus in Campo, Cameroon (Mitani,

1989). In Campo, C. torquatus ate more fruits (60%) than seeds (20%). C. atys is the only other Cercocebus species that consumes more seeds than C. torquatus in Sette

Cama.

Table 3.7 shows the contribution of each food category by month. Seeds were the largest percentage of the diet in all months except for September. During

September, C. torquatus ate mostly S. gabonensis fruits and, in general, fruit availability was higher in September than in other months. Fruits were the next most common food category eaten from June - September. The lack of fruit in the diet during May might be related to the small number of feeding events observed during this month.

The diet was the most varied during June, one of the months with lower fruit availability.

Fewer species of foods were eaten by C. torquatus during the systematic data collection period (12) compared to the pre-habituation period (26). The pre-habituation period gives a more realistic approximation of overall dietary breadth among C.

151

torquatus but not frequency of consumption. However, during both study periods,

Guibortia seeds were the most commonly observed food which suggests that this is an important food item for C. torquatus in Sette Cama. Sacoglottis seeds were also some of the most frequently observed food items during both study periods. This suggests that seeds are a major resource year-round for C. torquatus.

The C. torquatus diet contained more seeds (45.8%) during the systematic study

period of 2009 than during the prehabituation period of 2008 (29.2%). Again, this may

be due to the shorter study period in 2009 and the timing mismatch with the fruiting of

some major C. torquatus fruits (such as Dialium, Manilkara, Phoenix).

Food preference

There is no significant correlation between food availability and contribution to

the diet for the study period of May – September 2009. Table 3.8 presents the food

crop scores for each dietary category. Food availability increased during each

consecutive month of the study period with August and September showing the highest

availabilities. The food crop scores were compared to the monthly percentages of each

dietary category (fruit, seeds, insects, other) eaten, and there were no significant

relationships between availability and food type eaten (Table 3.9). As food availability

increased, the consumption of fruits and insects increased whereas the consumption of

seeds and other foods (such as crabs, leaves, bark) decreased. Nevertheless, C.

torquatus does not exhibit a significant preference for any particular food group, at least

during the dry season months.

152

The ability of C. torquatus to eat both soft and obdurate foods may enable them to maintain a diverse diet year round. Unlike C. torquatus in Cameroon, where fruits comprised 60% of the diet (Mitani, 1989), C. torquatus in Sette Cama are eating a substantial amount of foods besides fruits. As seen during both study periods, hard- object foods such as S. gabonensis seeds and crabs are eaten during all seasons, including the high fruiting periods. This indicates that any one food category does not serve as a fallback for this population.

Food hardness

Out of the 25 food species eaten by C. torquatus during the entire 2008-2009 study period, five classified as “Harder-stiffer” foods (Tables 3.10 and 3.11). See

Appendix A for photos of the hard C. torquatus foods. Hard foods made up 22.9% of the diet during the prehabituation period and 22.2% of the diet during systematic study.

The hardest food was the Sacoglottis seed with a Shear D hardness of 29.39 ± 10.91.

The degree of error may relate to the heterogeneous structure of the Sacoglottis seed covering. Studies from Taï National Forest found that Sacoglottis seeds were also the hardest item in the sooty mangabey diet (Daegling et al., 2010; McGraw et al., 2011), and they scored Shore D Hardness values of 78.3 (Pampush et al., 2011). This is equivalent to cherry or prune pits (Williams et al., 2005). The hardness value for S. gabonensis seeds was higher in Taï than those obtained from Sette Cama, but several factors may have contributed to the variation including age and dryness of the seed at testing, placement of the plunger, and force at which the plunger was applied.

153

Regardless of the deviation in measurements, Sacoglottis seeds are an extremely hard- object eaten by at least two Cercocebus species.

Seven foods are “Cross-over” foods, meaning they scored from 1-30 on the Type

D durometer (see Appendix B for photos). Cross-over foods comprised 29.5% of the

2008 diet and 31.5% of the diet from May – September of 2009.

The remaining foods did not measure above 70 on the Type A durometer and were categorized as “Softer-pliable” foods. Soft foods made up 35.9% of the foods during the prehabituation period and 31.1% of the feeding observations during systematic study. 6 Overall, the diet of C. torquatus contained fewer hard foods (hard- stiff and cross-over foods) during the May – September 2009 study period (52.4%) compared to the prehabituation period (53.7%), although not by a large margin.

Table 3.12 presents the mean Type A and Type D hardness values for each month of the systematic study of 2009. The months of May and June had the highest hardness averages, and these were also the months with the lowest food availability during the study period according to phenological analysis (see Chapter 2). The mean

Type A and Type D food hardness values were not significantly different across the five study months (Kruskal-Wallis test, p=.406).

As food (or fruit) availability increased during the dry season, the mean hardness of the diet decreased (Table 3.12). Hard foods were still consumed in all months, albeit in smaller percentages (Table 3.13). Softer foods were not eaten during the months of

6 These estimates do not include leaves, bark, invertebrates, or unknown foods.

154

May – July, the period of lower fruit availability. Cross-over foods were eaten in all

months except May.

A comparison of the monthly consumption of different food property types and

food availability revealed a significant relationship between the consumption of soft

foods and food availability (Table 3.14). As soft food availability increased (fruits), the

consumption of soft foods increased as well (Pearson’s correlation=0.893, p=0.042).

There was not, however, a significant decline in hard and cross-over food consumption

associated with the increase in food abundance over the study period. This may suggest

a preference for soft foods (as defined by Marshall and Wrangham, 2007), but the

consumption of other food property categories did not significantly decline with each

month. Therefore, this does not indicate a “switch” in diet from fallback foods to softer

foods. Hard and cross-over foods formed a major component of the C. torquatus diet in

each month of both the systematic and prehabituation study periods.

3.8 Discussion

Although this study only represents part of an annual feeding cycle7; the results

indicate that C. torquatus in Sette Cama are reliant on fruits and seeds and show no dietary preferences during the dry season. The results from the prehabituation period

February 2008 – December 2008 reveal a different dietary composition than the results obtained from the period of systematic study during the dry season of May – September

7Only the systematic behavioral data collected from May – September 2009 will be used when comparing the diet of C. torquatus to other Cercocebus species. These data are comparable to feeding frequency estimates derived from the other studies whereas the prehabituation data only represent the number of days a food was eaten by C. torquatus.

155

2009. Fruit consumption was more prevalent during the longer study period (52% of

observations), most likely because this more closely represents the annual fruiting cycle

and changes in fruit availability. Seeds comprised around 30% and 46% of the diet,

during 2008 and 2009, respectively. Fruit abundance was highest towards the end of

the dry season months (July – September), but seed consumption continued during these months in both study periods. Other items such as crabs, leaves, and insects were eaten in smaller amounts during both time periods.

The only other detailed dietary study on C. torquatus comes from Campo,

Cameroon (Mitani, 1989). At this site, C. torquatus ate mostly fruits (60% of the diet) followed by seeds (20%). These groups maintained high levels of fruit consumption year-round. The diet of C. torquatus in Cameroon is more diverse, with 48 different food species compared to 36 among the Sette Cama population (Mitani, 1989).

Several factors may underlie the dietary variation between regional populations of C. torquatus. The most obvious reason is the limitation of this study—the data from

Sette Cama represent only a portion of the annual diet. Nevertheless, C. torquatus in

Sette Cama eat foods not eaten by the Campo groups despite their prevalence in both forests. For example, C. torquatus in Campo only eats the fruits of S. gabonensis and were not observed eating the seeds whereas both the fruit and seed are important foods for C. torquatus in Sette Cama.

The presence of sympatric species may also influence the feeding and foraging behaviors of C. torquatus populations. The diet of C. torquatus populations living with fellow clade members such as drills or mandrills may include fewer terrestrial food

156

items due to resource partitioning and competition. C. torquatus in Korup National

Park, Cameroon used a higher strata level when associated with drills (Astaras et al.,

2011). “The red capped mangabey’s day foraging was more arboreal than the drill’s and

is best described as semi-terrestrial” (Astaras et al., 2011:132). C. torquatus in Campo,

Cameroon were observed associating with mandrills and up to four other cercopithecid

species (Mitani, 1991). C. torquatus are the only ground dwelling primate in Sette

Cama, and they face feeding competition from only two other primate species (C. cephus and C. nictitans). The presumably lower interspecific feeding competition in

Sette Cama may allow C. torquatus to balance a diet of both fruit and seeds. The group size in Sette Cama is also significantly larger (around 70 individuals) than those observed in Campo (around 25 individuals). Therefore, while interspecific feeding competition may be low, intraspecific competition may force C. torquatus to diversify their diets.

Ranging patterns and habitat structure can also influence a primate’s diet.

Mitani (1989) related the seasonal shift in home range of his C. torquatus groups to the search for different fruits. This enabled the Campo populations to maintain a steady diet of fruit year-round. The Sentier Nature forest of Sette Cama is a much smaller and more isolated forest than that of the Campo C. torquatus population (refer back to chapter 2). Perhaps C. torquatus in Sette Cama consume more seeds than other populations because they do not have the flexibility of shifting ranging patterns over a larger area to locate fruits (see Chapter 4).

157

C. torquatus diet compared to other Cercocebus species

Categorically, the overall C. torquatus diet most closely resembles that of C.

galeritus (Homewood, 1976; Kinnaird, 1990), but C. torquatus are most similar, in terms

of obdurate food consumption, to C. atys, sooty mangabeys. C. torquatus in Sette Cama

ate fewer food species than other Cercocebus species. C. atys were observed eating at

least thirty different food species, but the diet was mainly composed of S. gabonensis

seeds, invertebrates, and Coula edulis nuts (McGraw et al., 2011). C. torquatus in Sette

Cama ate a similar variety of food items (26 identified species), but they consumed a

wider variety of food species more frequently than C. atys. C. agilis had a more expansive diet of 59 species in Mondika (Shah, 2003), and C. sanjei reportedly ate 99 different food species (Mwawende, 2009).

Seeds comprise a large percentage of several Cercocebus species’ diets (Table

3.1) which suggests that seeds are an important resource for this clade. S. gabonensis seeds make up over half the sooty mangabey diet (51.9%) and 17.1% of the C. torquatus diet at Sette Cama (McGraw et al., 2011). Interestingly, C. torquatus in Cameroon were not noted to consume the seeds of S. gabonensis despite its availability (Mitani, 1989).

Among C. torquatus in Sette Cama, S. gabonensis seeds were eaten during ten of the fifteen months of data collection. At Taï, C. atys ate S. gabonensis seeds during every month of the study period of twelve months, and S. gabonensis seeds made up

25-80% of the monthly C. atys diet (McGraw et al., 2011; McGraw and Daegling, 2012).

In general, as rainfall increased, the consumption of Sacoglottis seeds by C. atys increased, although the relationship was not significant (McGraw, pers. comm). In Sette

158

Cama, C. torquatus ate fewer Sacoglottis seeds during the dry season compared to the rainy seasons. However, the dry season tends to be a period of high food availability for

C. torquatus in Sette Cama, and the Sacoglottis trees come into fruiting at the end of the season. Another reason for the drop in consumption may be the reduced availability of

Sacoglottis seeds left on the ground from the previous season.

Seeds (in particular, dry, hard seeds) are considered a fallback food for the

Eastern Cercocebus species (Tana River and Sanje mangabeys) (Wahungu, 1998;

Wieczkowski and Ehardt, 2009). During periods of fruit scarcity, Tana River mangabeys

“…[I]ncreased their consumption of invertebrates and fed mostly at ground level. The crested mangabeys spent considerable time turning the leaf layer for insects, grubs, bird and reptile eggs and dry seeds within the forest” (Wahungu 1998: 170). Other clade members, such as drills, also reportedly increase their seed predation during the dry season, or the period of low fruit abundance in Korup, Cameroon (Astaras et al., 2011).

However, the status of seeds a fallback resource has not been evaluated for drills.

Dietary differences exist among the different Cercocebus taxa because of geography, seasonality, and competition from sympatric species. The amount of seeds and hard foods in Cercocebus diets varies, and the role of durophagy and seed eating within this clade may also vary among species.

Comparison of food properties among sites

The evidence from other sites and Cercocebus species confirms the suggestion that the ability to feed on obdurate foods is a trait found in all Cercocebus mangabeys.

The Shore hardness values of C. torquatus foods are similar to those obtained for foods

159

eaten by C. atys in Taï (Daegling et al., 2010). Anecdotal evidence also suggests that C. torquatus eat other hard-object foods, such as Coula nuts, where they are available

(such as Loango Park, pers. commun). C. torquatus in Campo, Cameroon were observed eating Anthonotha cladantha seeds (Mitani, 1989). These seeds, which make up 15.38% of their annual diet, are protected by a husk-like pod and presumably rank high on the hardness scale (and toughness, as well). Anthonotha seeds are eaten by other species such as colobines, which feature adaptations for hard-object feeding (Daegling and

McGraw, 2001; White and Abernethy, 1999).

Other Cercocebus species (galeritus, sanjei) have been reported to eat seeds

(such as Parinari spp.) that rank in hardness with some of the hardest foods eaten by any primate (Kinzey and Norconk, 1990; Peters, 1993; Wieczkowski, 2009). Shah (2003) also remarked on the tendency of C. agilis in Mondika, CAR to consume harder seeds compared to the sympatric L. albigena.

Food Preferences among Cercocebus species

In order to elucidate the function of seed-eating and obdurate foods in the mangabey diet, consumption must be compared to overall food availability. As suggested by Marshall and Wrangham (2007), the percentage of seeds and obdurate foods in the diet were compared to food availability to determine if they were preferred or non-preferred food items. Studies of two of the East African Cercocebus species

(galeritus and sanjei) report that seeds are a non-preferred food item, and therefore, qualify as fallback foods (Wieczkowski and Ehardt, 2009). Tana River and Sanje mangabeys eat seeds during every month of the annual cycle, but Tana mangabeys

160

displayed a significant drop in seed consumption associated with increased fruit

availability (Wieczkowski and Ehardt, 2009). Similarly, it is suggested that the Sanje

mangabey uses seeds and nuts as a fallback food item when preferred foods are less

abundant.

Unlike the Tana River and sanje mangabeys, C. torquatus in Sette Cama did not

show a significant change in the consumption of different food categories (fruits, seeds,

etc.) associated with an increase in food availability, and therefore, did not show

evidence of preference in food choice. The consumption of obdurate foods decreased

and soft food consumption increased as fruit availability increased. Nevertheless, hard

foods remained a large component of overall C. torquatus diet, and the drop in hard

food consumption was not statistically significant. The reason for the lack of preference

in food items may be attributed to the overall dietary breadth of C. torquatus. C.

torquatus exploited unusual food sources such as crabs, and they were often observed

foraging on the beach (pers. obs.). Unlike other C. torquatus populations, C. torquatus

in Sette Cama also took advantage of the S. gabonensis seeds found on the forest floor for most of the year.

The importance of “hard” and “cross-over” foods in the diet of C. torquatus in

Sette Cama may change once data become available for the full annual cycle. Fruit consumption will increase with the inclusion of soft fruits available in seasons not observed in the systematic study such as Phoenix reclinata, Dialium spp, and Manilkara fouilloyara (from the months of November to February). Nevertheless, I predict that harder foods will remain in the diet of C. torquatus even during these periods of

161

increased fruiting. They will opportunistically eat crabs and continue to consume

Hyphanae guineensis palm fruits and S. gabonensis seeds. The ability to eat these hard foods is part of their adaptation for living in a large group in their relatively small home range.

Conclusions on fallback feeding for this clade

At least two species of West African Cercocebus (torquatus and atys) routinely eat hard seeds and other obdurate foods (McGraw et al., 2011; McGraw and Daegling,

2012). Hard-object foods are often considered fallback foods, or “last resort,” low preference food items that drive adaptive changes in morphology (Lambert et al., 2004).

As evidenced from both the prehabituation and systematic data periods, C. torquatus

frequently eats hard-object foods such as S. gabonensis seeds, H. guineensis palm fruits, and crabs that are readily available for most of the year (personal obs). The consumption of these foods also did not significantly vary with food availability. These data suggest that durophagy and seed eating is not fallback strategy for C. torquatus in

Sette Cama.

The definitions supplied for fallback feeding among primates by both Marshall and Wrangham (2007) and Lambert (2007) are insufficient to explain the evolution of the suite of cranial and skeletal characteristics in all Cercocebus species. According to the current conceptions of fallback feeding, “[R]elatively high-quality foods drive harvesting adaptations while relatively low-quality foods drive processing adaptations and …low quality foods are disproportionately important in determining anatomical

162 traits while high quality foods are more implicated in behavioral adaptations” (Marshall et al., 2009:605).

The morphologies of the Cercocebus and the Mandrillus genera display adaptations for both harvesting and processing durophagous foods. As noted in Chapter

1, this group of primates displays forelimb morphologies associated with harvesting obdurate foods from the leaf litter on the forest floor (Fleagle and McGraw, 1999,

2002). These foods are then processed using the enlarged premolars that distinguish

Cercocebus and Mandrillus from Lophocebus. Furthermore, the hard-object foods eaten by these taxa include seeds, nuts, and crabs which cannot necessarily be classified as low-quality food items. It is also hypothesized that the unusual grouping patterns of this clade are facilitated by feeding on slowly accumulating terrestrial obdurate foods.

Therefore, durophagy within the Cercocebus-Mandrillus clade does not fit with current interpretations of fallback feeding (McGraw and Daegling, 2012). This does not, however, negate the possibility that these definitions of fallback feeding apply to other primate groups, such as Lophocebus, gorillas, or orangutans.

This study of C. torquatus, although not necessarily representative of an entire annual cycle, indicates that they are more similar dietarily to the C. atys population at

Taï than other Cercocebus taxa. Unlike the other Cercocebus species studied thus far, both C. atys and C. torquatus in Sette Cama habitually consume a large amount of hard seeds and other obdurate foods. These similarities also lend support to the proposed mangabey biogeographical radiation, with C. torquatus and C. atys being closely related

(McGraw and Fleagle, 2006).

163

3.9 Future Directions and Conclusions

The study of food properties have only just begun to be applied to primate

studies. Researchers are still experimenting with different field and laboratory

techniques to estimate material properties both efficiently and accurately (Lucas et al.,

2003; Lucas et al., 2012). This study presents a novel method of estimating Shore

hardness values using a handheld durometer in the field. These values can be compared

to similar studies in other sites. Nevertheless, a vital component missing from this

research is an estimate of food toughness. Toughness may also be a major factor

influencing food choice and dental adaptations among primates (Lucas et al., 2012).

Future research into the material properties of C. torquatus foods in Sette Cama will most likely reveal that this species is reliant on both hard and tough foods. Most mangabey species eat terrestrial herbaceous vegetation such as shoots and stems, a food which presumably contains abrasive materials such as phytoliths (Mitani, 1989;

Shah, 2003; Wiezcowski and Ehardt, 2009; DeVreese, 2010). Shoots and stems should also measure as tough, or displacement-limited.

Another interesting area for research is the nutritive properties of so-called

fallback foods. These foods are usually considered low quality and less nutritious than

primate food sources. However, sooty mangabeys, C. atys, subsist primarily on “fallback

foods,” S. gabonensis seeds, which suggests that these foods are more nutritious than

assumed. Indeed, a study on the nutritive properties of several common seed and nut species throughout Africa reveals that these foods are a highly nutritious (Peters, 1987).

164

Further studies on C. torquatus should also focus on how they access and

process hard-object foods.

The lack of such detailed contextual data is significant given that the molarized premolars of Cercocebus, mandrills and drills are presumed to reflect the key aspect of their feeding ecology (habitual hard-object processing) and are part of a craniomandibular complex marking the clade’s origin in the fossil record (McGraw et al., 2011:141).

McGraw and colleagues (2011, 2012) were the first to combine food hardness measurements with detailed observations on the processing and mastication of foods.

The knowledge of how cranio-dental morphology relates to food properties will aid in the reconstruction of diets of extinct species, such as Procercocebus antiquus, and strengthen hypothesized form-function relationships between diet and morphology.

Preliminary observations on food processing indicate that C. torquatus uses

diverse extractive techniques for obdurate feeding, similarly to sooty mangabeys (Cooke

et al., 2009). C. torquatus eats fruits that have relatively hard mesocarps, such as the

Hyphanae guineensis palm fruits, that they access with their incisors (Figure 3.14).

These fruits are inaccessible to the sympatric Cercopithecus cephus. C. torquatus also eat Guibortia tessmannii and Sindora klaineana by piercing the durable outer covering with their incisors to expose the soft seed inside. The S. gabonensis seeds that C. torquatus consumes are contained within hard pericarps that require postcanine crushing, as observed among sooty mangabeys (McGraw et al., 2011; McGraw and

Daegling, 2012). Both the anterior and the posterior dentition of a C. torquatus specimen collected from Sette Cama exhibit extreme signs of wear (Figure 3.15). This suggests that both sections of the dental arcade figure prominently in obdurate feeding.

165

Finally, the study of durophagy among Cercocebus species is informative, not only for understanding the evolution of this particular clade, but Cercocebus mangabeys can also serve as a modern analog for hominins (Daegling et al., 2011; McGraw and

Daegling, 2012). More specifically, many of the earliest hominin species are presumed obdurate feeders. A comparison of craniodental morphology and enamel microwear of

C. atys and Australopithecus africanus recently discredited the hypothesis that A.

africanus were habitual obdurate feeders (Daegling et al., 2011). Further analysis of diets among Cercocebus taxa may help interpret the diet of other hominin species and the role of obdurate feeding among our ancestors.

166

Figure 3.1: Stress-strain curve indicating elastic modulus and yield point. Elastic modulus measures stiffness of a material and the yield point is the point of permanent deformation. Stress is equal to force applied and strain is equal to displacement due to stress. Figure is based on Williams et. al, 2005:332. Reproduced by Tom Cooke.

167

Species Fruit Fruit + Seeds Structural1 Flower Invert Other Site2 Seeds Leaves

C. agilis -- 75 -- 16 -- 5 4 Mondika, CAR C. agilis -- 67.6 -- 20.8 -- 6.2 4.5 Bai Hokou, CAR

C. atys 17.1 -- 55.4 <1 1 13.01 3.4 Taï, Côte d’Ivoire C. -- 76 -- 12 5 2 5 Tana galeritus River, Kenya

C. 34 -- 42 7 5 11 -- Tana galeritus River, Kenya C. 44 -- 32 ------Tana galeritus River, Kenya C. sanjei -- 47 -- 15 9 29 -- Udzungwa , Tanzania C. 60 -- 20 ------Campo, torquatus Cameroon M. leuco 58 -- -- 16 -- 26 -- Bioko, -phaeus Equatorial Guinea M. sphinx 84 ------8 -- Campo, Cameroon M. sphinx 47 -- 34 -- 7 5 -- Lope, Gabon

Table 3.1: The diets of known species of Cercocebus and Mandrillus. These numbers are as they were reported in each study and do not include values for unknown items.

1This category includes bark, twigs, pith, and sap

2Sources in order by species: Shah, 2003; Devreese, 2010; McGraw et al., 2011; Homewood, 1976; Kinnaird, 1990; Mwawende, 2009; Mitani, 1991; Swedell, 2011; Hoshino, 1985; Tutin et al., 1997.

168

Figure 3.2: The Type A and Type D Asker Durometers. (Photo courtesy of J. Pampush and D. Daegling).

Figures 3.3 and 3.4: The plunger of the Type A Durometer and the Type D Durometer. Note that these are not to scale. (Photos courtesy of J. Pampush and D. Daegling).

169

Figures 3.5 and 3.6: A Sacoglottis gabonensis endocarp and its cross-section. Note the variety of textures and air pockets. (Photos courtesy of J. Pampush and D. Daegling).

170

SPECIES NAME FAMILY PART EATEN TYPE

Alchornea cordifolia EUPHORBIACEAE PULP L Cardisoma armatum GECARCINIDAE MEAT INV Chrysobalanus icaco CHRYSOBALANACEAE PULP/SEED S Cola caricifolia STERCULIACEAE SEED S Cyperus spp CYPERACEAE LEAF THV Dialium spp CAESALPINIOIDEAE PULP/SEED T Diosperos dendo EBENACEAE PULP T Ficus elasticoides MORACEAE PULP/SEED T Hyphanae guineensis PALMACEAE PULP T Guibourtia tessmannii CAESALPINIOIDEAE SEED T Larvae spp N/A MEAT INV Landolphia latifolia APOCYNACEAE SEED T Lecanodiscus cupionoides SAPINDACEAE PULP T Macrolobium spp CAESALPINIOIDEAE PULP T Manilkara fouilloyara SAPOTACEAE PULP T Mareyopsis longifolia EUPHORBIACEAE PULP T Pachylobus spp UNKNOWN PULP S Phoenix reclinata PALMACEAE PULP S Pycnanthus angolensis MYRISTICACEAE SEED T Sacoglottis gabonensis HUMIRIACEAE PULP/SEED T Scytopetalum klaineaum SCYTOPETALACEAE PULP T Sindora klaineana LEGUMINOSAE SEED T Tabernanthe iboga APOCYNACEAE PULP S Vitex doniana VERBENACEAE PULP T Warneckea yangambensis MELASTOMACEAE PULP L

Table 3.2: All foods identified during the study period from 2008 – 2009 and consumed by C. torquatus. The type refers to vegetation type where INV= invertebrate, L= liana, S=shrub, T= tree, and THV= terrestrial herbaceous vegetation.

171

Monthly Summary 2008 60 50 40

30 FEEDING OBSERVATIONS 20 FOOD SPECIES 10 0

Figure 3.7: The total monthly number of food species and feeding observations for the prehabituation study period.

% Feeding observations 2008 (N=240)

UNKNOWN THV SEED LEAVES INSECTS FRUIT CRAB BARK

0 10 20 30 40 50 60

Figure 3.8: Percentage of foods by category observed from February – December 2008.

172

Food Frequency of Percent of observations observations Guibortia tessmannii 36 15.0 Cardisoma armatum (Crab) 28 11.7 Sacoglottis gabonensis (Seed) 20 8.3 Manilkara fouilloyara 19 7.9 Lecanodiscus cupionoides 16 6.7 Cola carcifolia (Ripe) 13 5.4 Scytopetulum klaineaum 12 5.0 Sacoglottis gabonensis (Ripe Fruit) 11 4.6 Unknown 11 4.6 Ficus elasticoides 10 4.2 Vitex doniana 9 3.8 Pycnanthus angolensis 8 3.3 Leaves (Species Unknown) 7 2.9 Landolphia latifolia 6 2.5 Dialium spp 4 1.7 Larave (Species Unknown) 4 1.7 Warneckea yangambensis 4 1.7 Cola carcifolia (Unripe) 3 1.3 Pachylobus spp 3 1.3 Alcornea cordifolia 2 0.8 Chrysobalanus icaco 2 0.8 Hyphanae guineensis 2 0.8 Sacoglottis gabonensis (Unripe Fruit) 2 0.8 Sindora klaineana 2 0.8 Bark (Species Unknown) 1 0.4 Cyperus spp 1 0.4 Diosperos dendo 1 0.4 Guibortia tessmannii (Unripe) 1 0.4 Tabernanthe iboga 1 0.4 Mareyopsis longifolia 1 0.4 Total 240 100 Table 3.3: The food species eaten by C. torquatus during the February – December 2008 habituation period and their frequencies of observation.

173

Figure 3.9: Graphical representation of the foods eaten and their frequencies during the Februrary – December 2008 habituation period.

174

SPECIES FEB MAR APR MAY JUN JUL AUG SEPT OC NO DEC Alcornea cordifolia 0 0 0 0 1 1 0 0 0 0 0 Bark 0 0 0 0 0 0 0 0 0 0 1 Chrysobalanus icaco 0 2 0 0 0 0 0 0 0 0 0 Cola carcifolia (Ripe) 0 6 0 1 2 1 0 0 0 1 2 Cola carcifolia (Unripe) 0 1 0 1 0 0 0 0 0 0 1 Crab 2 9 1 4 5 2 0 5 0 0 0 Cyperus sp 0 0 1 0 0 0 0 0 0 0 0 Dialium sp 0 0 0 0 0 0 0 0 0 0 4 Diosperos dendo 0 1 0 0 0 0 0 0 0 0 0 Ficus elasticoides 1 2 1 1 3 2 0 0 0 0 0 Guibortia tessmannii 1 0 1 0 14 2 0 8 5 3 2 (Ripe) Guibortia tessmannii 0 0 1 0 0 0 0 0 0 0 0 (Unripe) Hyphanae guineensis 0 0 0 0 2 0 0 0 0 0 0 Tabernathe iboga 0 0 0 0 1 0 0 0 0 0 0 Landolphia latifolia 0 4 0 0 0 0 0 0 1 1 0 Larvae Species 1 1 0 0 0 0 0 1 0 0 1 Leaves 0 0 2 2 1 0 0 1 1 0 0 Lecanodiscus 0 0 0 4 0 4 2 5 0 0 1 cupionoides Manilkara fouilloyara 7 11 0 0 1 0 0 0 0 0 0 Mareyopsis longifolia 0 0 0 0 0 0 0 1 0 0 0 Pachylobus sp 0 1 2 0 0 0 0 0 0 0 0 Pycnanthus angolensis 0 0 0 0 1 2 0 5 0 0 0 Sacoglottis gabonensis 0 0 0 0 0 0 4 7 0 0 0 (Ripe Fruit) S. gabonensis (Unripe 0 1 1 0 0 0 0 0 0 0 0 Fruit) S. gabonensis (Seed) 0 3 2 4 7 3 0 0 0 0 1 Scytopetalum 0 0 0 7 4 1 0 0 0 0 0 klaineaum Sindora klaineana 0 0 0 0 0 0 0 1 1 0 0 Unknown Species 0 3 1 0 5 0 0 0 0 1 0 Vitex doniana 0 2 0 0 6 1 0 0 0 0 0 Warneckea 0 3 0 1 0 0 0 0 0 0 0 yangambensis

Table 3.4: The number of each observations of each food species by month for the prehabituation period (February – December 2008). The species highlighted in grey were eaten in the most number of months.

175

Food % Observations Total Observations Alchornea cordifolia 4.2 9 Crab 0.5 1 Cola caricifolia 0.5 1 Guibourtia tessmannii 26.4 57 Hyphanae guineensis 4.6 10 Insects 2.3 5 Lecanodiscus cupionoides 1.4 3 Sacoglottis gabonensis (Ripe 25.0 54 Fruit) Sacoglottis gabonensis 17.1 37 (Seed) Sindora klaineana 2.3 5 Vitex doniana 2.8 6 Young leaves 0.5 1 Other 0.5 1 Unknown Species 12.0 26 Total 100.0 216

Table 3.5: Total number of records of each food species and the contribution to overall diet from May – September 2009.

176

Feeding Data: May - September 2009

Unknown Other Young leaves Vitex doniana Sindora klaineana Sacoglottis gabonensis (seed) Sacoglottis gabonensis Lecanodiscus cupionoides % Observations Insects Hyphanae guineensis Guibourtia tessmannii Cola caricifolia Cardisoma armatum Alchornea cordifolia

0 5 10 15 20 25 30

Figure 3.10: Graphical representation of the frequency of observation of each food species from May – September 2009.

177

Food May June July August September Alchornea cordifolia 0 0 0 0 9 Cardisoma armatum(Crab) 0 1 0 0 0 Cola caricifolia 0 0 0 0 1 Guibourtia tessmannii 0 7 21 19 10 Hyphanae guineensis 0 9 1 0 0 Insects 0 1 0 4 0 Lecanodiscus cupionoides 0 0 0 3 0 Sacoglottis gabonensis 0 0 0 32 22 Sacoglottis gabonensis(Seed) 8 8 3 18 0 Sindora klaineana 0 0 0 1 4 Vitex doniana 0 0 5 1 0 Young leaves 0 0 1 0 0 Other 0 1 0 0 0 Unknown 2 9 2 9 4 Total 10 36 33 87 50

Table 3.6: Monthly summary of the number of records of each food species eaten from May – September 2009.

Summary of Feeding Records 2009 100 90 80 70 60 # Feeding or Foraging 50 Observations 40 # Food Species 30 20 10 0 MAY JUNE JULY AUGUST SEPT

Figure 3.11: Total number of feeding or foraging records by month and the number of different food species recorded from May – September 2009.

178

Diet Composition May - Sept 2009 (N=216)

Fruit

Seeds

Insects

Leaves

Crab

Other

Unknown

0 10 20 30 40 50

Figure 3.12: Diet composition from May – September 2009 by food type.

Month Fruits Seeds Insects Leaves Crab Other Unknown May 0 80 0 0 0 0 20 June 25 41.7 2.8 0 2.8 2.8 25 July 18.2 72.7 0 3 0 0 6.1 August 41.4 43.7 4.6 0 0 0 10.3 September 64 28 0 0 0 0 8

Table 3.7: Contribution of each food type by month from May – September 2009.

179

Month Food Crop Score May 2.0075 June 2.2391 July 3.3974 August 5.0573 September 5.0235

Table 3.8: Food crop scores for May – September 2009.

Category Correlation p-value Result Fruit 0.775 0.124 not significant Seeds -0.567 0.319 not significant Insects 0.221 0.721 not significant Other -0.249 0.686 not significant

Table 3.9: Pearson’s correlation coefficients for food category compared to food crop score from May – September 2009. None of the relationships were significant which indicates no preference for these foods based on availability.

180

Food Name Part Ripe/ Part Eaten N Avg SE Type Measured Unripe Alchornea cordifolia Exocarp Unripe Seed 10 14.27 0.79 Soft Alchornea cordifolia Seed Unripe Seed 10 22.43 1.62 Soft Chrysobalanus icacao Mesocarp Ripe Mesocarp 10 1.402 0.79 Soft Chrysobalanus icacao Seed Ripe Seed 2 1 1 Soft Chrysobalanus icacao Exocarp Unripe Seed 3 71.03 0.89 Hard Cola caricifolia Exocarp Ripe Seed juice 10 58.32 5.27 Soft Cola caricifolia Exocarp Unripe Seed juice 6 62.16 6.14 Soft Dialium Exocarp Ripe Mesocarp 8 22.2 2.32 Soft pachyphyllum Guibortia tessmannii Exocarp Ripe Seed 15 44.7 10.26 Soft Guibortia tessmannii Exocarp Unripe Seed 3 34.53 8.64 Soft Guibortia tessmannii Seed Unripe Seed 5 37.04 4.8 Soft Guibortia tessmannii Seed Ripe Seed 6 41.01 10.12 Soft Hyphaene guineensis Mesocarp Unripe Mesocarp 3 89.8 3.8 Hard Hyphaene guineensis Mesocarp Ripe Mesocarp 13 68.67 2.65 Hard Hyphaene guineensis Mesocarp Old Mesocarp 3 71.9 4.25 Hard Landolphia latifolia Exocarp Ripe Seed juice 5 50.16 5.76 Soft Lecanodiscus Mesocarp Unripe Mesocarp 8 33.07 11.33 Soft cupanoides Manilkara fouilloyara Mesocarp Unripe Mesocarp 12 5.26 0.42 Soft Pachylobus species Mesocarp Ripe Mesocarp 9 67.22 5.69 Hard Continued

Table 3.10: The average Shore hardness values and standard error for foods which registered on the Type A Durometer. Foods in blue are “Harder-stiffer,” foods in grey are “Cross-over,” and white foods are “Softer-pliable.” 1Pycnacanthus angolensis fruits were categorized as “Cross-over” because the majority of the samples measured below 30 on the Type D Durometer.

181

Table 3.10: Continued

Food Name Part Ripe/ Part N Avg SE Type Measured Unripe Eaten Phoenix reclinata Mesocarp Ripe Mesocarp 10 36.36 2.16 Soft Pycnacanthus Seed Ripe Seed 3 75.5 4.25 Cross angolensis1 Sacoglottis gabonensis Mesocarp Unripe Mesocarp 5 11.6 8.19 Soft Sacoglottis gabonensis Mesocarp Ripe Mesocarp 6 1.01 0.44 Soft Sindora klaineana Exocarp Unripe Seed 5 63.24 6.61 Soft Sindora klaineana Exocarp Ripe Seed 4 46.55 10.9 Soft Sindora klaineana Seed Ripe Seed 2 17.95 16.6 Soft Tabernanthe iboga Mesocarp Ripe Mesocarp 6 57.8 8.43 Soft Vitex doniana Mesocarp Ripe Mesocarp 7 3.96 0.85 Soft Vitex doniana Mesocarp Unripe N/A 2 30.3 6.92 Soft Warneckea Mesocarp Unripe Mesocarp 1 38.8 N/A Soft yangambensis W. yangambensis Mesocarp Ripe Mesocarp 3 22 5.54 Soft Unknown orange fruit Mesocarp Ripe Mesocarp 2 6.1 1.55 Soft Unknown yellow liana Mesocarp Ripe Mesocarp 4 27.45 8.36 Soft

182

Food Name Part Ripe/ Part N Avg SE Type Measured Unripe Eaten

Cardisoma armatum Shell N/A Meat 6 61.9 10.87 Hard Chrysobalanus icacao Endocarp Ripe Seed 3 29.33 6.61 Hard Chrysobalanus icacao Exocarp Unripe Seed 8 7.23 1.4 CR Chrysobalanus icacao Endocarp Unripe Seed 5 28.9 3.6 Hard Guibortia tessmannii Exocarp Ripe Seed 6 5.85 1.3 CR Hyphaene guineensis1 Mesocarp Unripe Pulp 2 1.02 0.11 Hard Hyphaene guineensis Mesocarp Ripe Pulp 9 5.19 2.7 Hard Hyphaene guineensis Mesocarp Old Pulp 4 7.69 6.51 Hard Landolphia latifolia Exocarp Ripe Seed 2 2.54 2.09 CR juice Pycnacanthus Exocarp Ripe Seed 7 11.5 1.62 CR angolensis Sacoglottis Endocarp Ripe Seed 17 29.39 10.91 Hard gabonensis Sacoglottis Endocarp Unripe n/a 8 29.21 5.32 Hard gabonensis Sindora klaineana Exocarp Unripe Seed 3 12.43 0.05 CR Sindora klaineana Exocarp Ripe Seed 3 9.64 1.94 CR Vitex doniana Seed Ripe Pulp 6 15.12 5.02 CR

Table 3.11: The average Shore hardness values and standard error for foods which registered on the Type D Durometer. Those in blue are categorized as “Harder-stiffer” foods and those in grey are categorized as “Cross-over or CR” foods. 1H. guineensis fruits could be categorized as “Hard” with the Type A Durometer or “Cross-over” on the Type D Durometer. I included them with the “Hard” foods for this analysis because a higher number of samples placed them in the “Hard” category compared to “Cross- over.”

183

Number of foods by property category 16 14 12 10 8 6 4 2 0 Hard Soft Cross-over

Figure 3.13: The number of C. torquatus foods classified as hard, soft, or cross-over identified during the study period.

A Hardness D Hardness May 89.2 29.39 June 67.52 25.58 July 51.63 13.47 August 36.41 14.96 September 32.97 7.74

Table 3.12: The monthly mean Shear hardness values from the Type A and Type D durometers. There is no significant difference among the means for either durometer type (Kruskal Wallis test, p=.406).

184

Month Hard Soft Cross-over Other Unknown May 80 0 0 0 20 June 50 0 19.4 5.6 25 July 12.1 0 78.8 3 6.1 August 20.7 40.2 24.1 4.6 10.3 September 0 64 28 0 8

Table 3.13: Monthly summary of the percent contribution of each food category to the C. torquatus diet.

Category Correlation p-value Result Hard -0.840 0.075 Not significant Soft 0.893 0.042 Significant Cross-over 0.238 0.699 Not significant

Table 3.14: Pearson’s correlation coefficient comparing consumption of each food property type category with food availability. The consumption of soft foods significantly increased with the availability of foods.

185

Figure 3.14: C. torquatus incising a hard palm fruit. Photo still from the BBC film “Living with Monkeys”.

186

Figure 3.15: Maxillary dentition of a deceased C. torquatus from Sette Cama, Gabon. Note the wear on the incisors and premolars.

187

Chapter 4: Ranging and Subgrouping Behaviors

4.1 Introduction

Research suggests that the ability to feed on terrestrial obdurate foods is the key

adaptation of the Cercocebus-Mandrillus clade (Fleagle and McGraw, 1999, 2002; Jolly,

2007). This clade shares morphological characteristics of the postcrania and dentition

that allow them to exploit hard-food resources that accumulate on the forest floor and remain available for most of the year. Despite the proposed importance of these foods to Cercocebus and Mandrillus, it remains to be seen how the spatio-temporal distribution of obdurate foods relates to the ranging and subgrouping behaviors of

Cercocebus and Mandrillus. Therefore, the goal of this chapter is to describe the ranging

behaviors of C. torquatus in Sette Cama and then compare these data with the seasonal distribution of food sources. I also include some preliminary observations on subgrouping in this population. In this chapter, I address the following questions:

• What is the home range of C. torquatus? Does ranging vary by season or food

availability? Does the availability of certain food groups (such as fruits,

Sacoglottis gabonensis seeds) influence ranging behaviors?

• How does the ranging behavior of C. torquatus in Sentier Nature compare to C.

torquatus in Cameroon and other members of its genus

188

• Does the C. torquatus population of Sentier Nature subgroup? Is

subgrouping influenced by the spatio-temporal distribution of foods?

4.2 Background

Home Range

A population’s home range is broadly defined as the total area used by the group

for everyday activities such as feeding, mating, and sleeping (Clutton-Brock and Harvey,

1977; Kaplin, 2001). Multiple factors influence home range size including group biomass

(Milton and May, 1976), predation pressures (Altmann, 1974; Cowlishaw, 1997),

territoriality (Mitani and Rodman, 1979; Kaplin, 2001; Buzzard, 2006) and resource monitoring (Buzzard, 2006; Janmaat et al., 2006). Nevertheless, diet is often considered the primary factor influencing home range (Clutton-Brock and Harvey, 1977). The distribution and availability of resources potentially impact the ranging behaviors of species as they strive to maximize nutritional intake and minimize energetic output while locating and collecting foods (Charnov, 1976).

The majority of primate species live in tropical environments. Despite the seeming abundance of fruits and plants in a tropical forest, food availability fluctuates throughout the year. This variation in resources is due to the different patterns of leafing, flowering, and fruiting among plants both within and between species (Oates,

1987). Therefore, phenological variation (or the spatio-temporal distribution of foods)

will influence how primates utilize their habitats (van Schaik et al., 1993). Most

189

primates have developed mechanisms to cope with these seasonal and spatial food

fluctuations (van Schaik et al., 1993; Chapman et al., 1995). “In ecological time, there

are only two clear options [for primates]: change their range use to find more fruit

elsewhere… or switch to alternative foods” (van Schaik and Pfannes, 2005:40). Both

overall fruit abundance and the availability of specific foods potentially impact primate

movements.

In general, species that feed on patchy foods should occupy larger areas than

species that feed on uniformly distributed resources (Terborgh, 1983). Among primates,

it is assumed that frugivores occupy larger home ranges than folivores (Milton and May,

1976; Oates, 1987). Fruits tend to be seasonal and occur in discrete patches compared

to leaves. Folivores, on the other hand, tend to occupy smaller home ranges and travel lower daily distances (Clutton Brock and Harvey, 1977; Fashing et al., 2007).

During periods of fruit scarcity, primates often increase home range size and

daily path length to maintain a consistent diet (Struhsaker, 1978; Boinski, 1987; Olupot

et al., 1997). Other species decrease daily path lengths and supplement their diet with

other foods such as foliage or invertebrates during low fruiting periods (e.g. brown

capuchins in French Guiana: Zhang, 1994). Primates may also occupy different areas of

their home ranges at different times of the year according to food seasonality. For

example, black-faced spider monkeys (Ateles chamek) are predominantly frugivorous

190 monkeys that shift their range in association with the availability of fleshy fruits

(Wallace, 2006).

Nevertheless, some primate species show no relationship among resource availability or fruit abundance and home range (Gautier-Hion, 1988; Kaplin, 2001;

Buzzard, 2006). Because of their reliance on insects and a consistent foraging pattern, several tamarin monkeys show no marked change in feeding and foraging behaviors by season (Garber, 1993). Among blue monkeys (Cercopithecus mitis), ranging behavior was not related to overall fruit abundance but instead to the availability of specific fruit species (Kaplin, 2001). Guenons at Taï also show no relationship among fruit abundance and daily path lengths, home range, or habitat use (Buzzard, 2006).

Those primates that do not actively shift their ranging or habitat use according to food availability may rely upon other foods during periods of fruit scarcity. One option includes switching to more readily available foods such as bark and seeds (e.g.,

Lophocebus albigena, Lambert et al., 2004) or increase the intake of other food types.

Both Tana River mangabeys (C. galeritus) and yellow baboons ate more insects during periods of fruit scarcity, and C. galeritus increased the time devoted to foraging in the leaf litter for insects, grubs, and dry seeds (Wahungu, 1998). Nevertheless, dietary switching or supplementing often requires physiological or anatomical adaptations for the alternative food source.

191

Home ranges of Cercocebus species

Home range sizes vary among Cercocebus species (Table 4.1). In general, though, larger group sizes occupy larger home ranges. For example, sooty mangabeys at Taï (group size=+100) range over at least 800 hectares (McGraw et al., 2011), and the large group of agile mangabeys (N=230) at Bai Hoku occupies 1000 hectares (DeVreese,

2010). The smaller mangabey groups range between 20 and 300 hectares. Several factors influence home range size and how these species utilize their home ranges including competition from sympatric primates, predation pressure, and resource availability.

For example, C. atys in Taï maintain a fairly consistent diet of seeds and invertebrates year round (McGraw et al., 2011). They also occupy a large home range

(700-800 ha) and their groups number up to 100 individuals. The relationship between ranging and food availability is not known among C. atys; however, evidence suggests that they monitor resources within their home range (Janmaat et al., 2006). The sooty mangabeys repeatedly visited certain Anthonota trees in search of fallen fruits despite any visual cues indicating their presence. The large home ranges and range use of sooty mangabeys may be a consequence of multiple factors including group size, resource monitoring, and predation pressure.

Responses to seasonal resources in Cercocebus species responses

As discussed in previous chapters, Cercocebus species are characterized by their dental and skeletal adaptations for hard-object feeding (Fleagle and McGraw, 1999,

192

2002). This suggests that resource switching or supplementing with alternative foods may serve as a coping mechanism during periods of fruit shortages, rather than a dramatic shift in ranging behaviors. Indeed, some researchers suggest that fallback feeding is the mangabey’s main method of adapting to spatio-temporal variation of foods (Lambert et al., 2004; Wieczkowski and Ehardt, 2009). Nevertheless, the available data for Cercocebus species show a wide range of responses to fluctuating resources that includes strategies such as range shifting (Mitani, 1989), supplementing with less preferred foods (Wieczkowski and Ehardt, 2009), and possibly routine resource monitoring (Janmaat et al., 2006). Many Cercocebus species rely upon more than one strategy to ensure adequate nutrition during fruit scarce periods.

Several mangabey species show shifts in ranging associated with low fruiting periods. For example, when food availability decreased, C. galeritus increased its dietary diversity, total distance moved, and total area searched for food (Homewood,

1978). Mwawende (2009) observed that C. sanjei ranged farther and moved faster during the dry season. C. agilis devoted less time to travel during periods of fruit scarcity but ranged farther due to an increased reliance on terrestrial food items (Shah,

2003).

The available evidence suggests that C. torquatus do not alter their diets significantly with each season, but rather alter their ranging patterns (Mitani, 1989). C. torquatus in Cameroon displayed seasonal shifts in their home range associated with the availability of four high quality fruiting species including Sacoglottis gabonensis and

193

Anthonotha cladantha (Mitani, 1989, 1991). Given these data, C. torquatus movements

in Sette Cama should also vary according to seasonal availability of fruits.

Subgrouping

Another mechanism used by primates to adapt to fluctuating food availability is

to divide into subgroups during foraging. This phenomenon is broadly categorized as a

fission-fusion social dynamic (Aureli et al., 2008). In a fission-fusion system, subgroup

membership is fluid and ranges from being stable and cohesive to flexible and changing.

Spider monkeys and chimpanzees are most commonly associated with this type of

grouping pattern (Symington 1988; White and Wrangham, 1988; Chapman 1990;

Chapman et al., 1995; Asensio et al., 2008), but it has also been observed among

muriquis (Strier et al., 1993; Strier et al., 2002), hamadryas baboons (Kummer, 1971),

and bonobos (Stumpf, 2007). It is now thought that a flexible grouping strategy may characterize many primate species (Aureli et al., 2008).

The frequency and composition of subgroups are known to vary according to ecological factors such as food patch size, density, and distribution (Symington, 1988;

White and Wrangham, 1988; Chapman, 1990; Chapman et al., 2005; Aureli et al., 2008) and social factors such as reproductive state among females (Chapman, 1990; Dias and

Strier, 2003) and overall group size (Lehmann and Boesch, 2004). It has also been suggested that subgrouping represents a tradeoff between the need for a large group for predator protection and the resulting competition for resources (van Schaik and van

Hooff, 1983; Janson and Goldsmith, 1995; Boesch and Boesch-Achermann, 2000). In

194

general, the more unevenly distributed a resource, the more likely a group with flexible

grouping strategies is likely to break into subgroups.

Subgrouping in Cercocebus and Mandrillus species

Although it has not been well documented, several species of Cercocebus,

including agilis, atys, galeritus, sanjei, torquatus and mandrills have been reported to break into subgroups (Homewood, 1978; Jones and Sabater Pi, 1968; Mitani, 1989;

Quris, 1975; Range, 2004; Shah, 2003; Mwawende, 2009). The composition of subgroups and the frequency of subgroupings are unknown. Furthermore, the forces driving these subgrouping behaviors are not well understood but may be related to food availability. C. atys tends to subgroup only during the dry season when foods are less abundant (Range, 2004; Shah, 2003). Sanje mangabeys often split into subgroups during foraging and reconvene after feeding (Mwawende, 2009). There does not appear to be a relationship, though, between subgrouping and overall group size. C. torquatus in Campo, Cameroon live in groups of approximately 25 individuals, yet Mitani

(1989) reported subgrouping among this population. C. agilis in Baï Hoku, Central

African Republic, live in a very large group (up to 200 members), and they also were observed subgrouping (Devreese, 2010). It is expected that species should split into subgroups when feeding on patchily distributed or clumped, contestable resources to reduce intragroup feeding competition.

Mandrills and C. galeritus have been observed to form large groupings, or supergroups (Abernethy et al., 2002; Homewood, 1978). Mandrills reportedly convene

195 as massive groupings, or hordes, that contain over 800 members in Lopé National Park,

Gabon (Abernethy et al., 2002). The formation of supergroups in C. galeritus and mandrills has been related to periods of food abundance and evenly distributed resources (Abernethy et al., 2002; Homewood, 1978). It is expected that feeding on slowly accruing, evenly distributed hard-object foods may facilitate supergrouping among Cercocebus and Mandrillus because of a reduction in intergroup feeding competition (Jolly, 2007). Devreese (2010) suggests that it is more efficient for C. agilis in Baï Hoku, Central African Republic to maintain a large group size when feeding on slowly accumulating resources. Feeding as a large group prevents individuals from returning to depleted patches before food sources are again available.

Because C. torquatus in Sette Cama have such a large group size for their habitat size (see below), subgrouping probably plays a major role in the maintenance of this population. Subgrouping is perhaps a mechanism to reduce feeding competition among group members when feeding on resources that are not abundant enough to feed the entire group at once (Janson, 1988).

4.3 Research Questions

The previous chapter established that C. torquatus in Sette Cama did not use seeds or obdurate foods as a fallback resource when fruit was less abundant. This chapter examines the role of ranging behavior as a means of adapting to the spatio-

196

temporal variability in fruits and other key food items. In particular, I address the

following questions:

• What is the range use of C. torquatus in the Sentier Nature forest? Does ranging

vary by season or food availability? Does the availability of certain food groups

(such as fruits, Sacoglottis gabonensis seeds) influence ranging behaviors?

• How does the ranging behavior of C. torquatus in Sentier Nature compare to C.

torquatus in Cameroon and other members of its genus?

• Does the Sentier Nature C. torquatus population subgroup? How frequently

does subgrouping occur? Is subgrouping influenced by the temporal distribution

of foods?

4.4 Predictions

1. C. torquatus will shift its range based according to the availability of fruits.

Based on observations of C. torquatus in Cameroon (Mitani, 1989), C.

torquatus in Sette Cama should alter their ranging patterns to match the timing of fruit

trees in the Sentier Nature forest. Data collected during the pre-habituation phase of

the study suggests that the Manilkara fouillarya fruits located in the costal palm habitat

are an important food source during the short dry season. Therefore, during the

months of January to March when these trees are fruiting, C. torquatus should be found

more frequently along the coastal palm forest than other habitat types. C. torquatus

197

should be found more often in the terra firme and mangrove habitats during the rest of

the year because most other foods, such as Guibortia tessmannii and Sacoglottis

gabonensis, are located within these habitat types. This should be reflected by a strong

positive correlation between ranging and phenology patterns.

2. The monthly ranges of C. torquatus will always include the S. gabonensis trees

because these seeds represent a stable food source year round.

As suggested in the previous chapter, C. torquatus relies heavily on seeds and

hard-objects as a food source in both the wet and dry seasons. In particular, both the S.

gabonensis seeds and fruits are important food sources for this group. Therefore, it is expected that their ranging will include these trees in both the wet and dry seasons, and

they will show a positive correlation between movements and the locations of these

trees.

3. Based on overall group size, C. torquatus should range over a similar area to C. atys. However, because C. torquatus occupies a forest fragment, C. torquatus will use its habitat more intensively to compensate for the lack of overall space.

In general, as primate group size increases, so too does home range size and daily path length (Olupot et al., 1994; Chapter 2). The C. atys group at Taï has over 100 individuals and they range over an area of at least 800 hectares (McGraw et al., 2011).

The C. torquatus group in Sette Cama numbers greater than 70 individuals, but the forest is cut off by two tourist camps. Therefore, I expect C. torquatus to intensively utilize its habitat because it cannot range over a large area. For this study, intensive 198

habitat use is defined as the repeated use of the same forest areas and the use of

multiple forest strata by the group at one time. This will be reflected in a high density of

sightings in certain resource rich areas of the forest such as around the Sacoglottis trees

and along the Ndougou Lagoon and a high vertical group spread.

4. C. torquatus will break into subgroups when fruits are less abundant.

Therefore, subgrouping should be more common during the wet season when fruit

availability is reduced.

Subgrouping, in this study, is defined as a separation among the whole

population of greater than 500 meters. A key driving force behind subgrouping among

primates is food abundance and distribution (Aureli et al., 2008). When a food is evenly

distributed and plentiful, there is more of a chance that all members of a group can gain

adequate nutrition when foraging together. However, as resources become patchy in

space or less abundant, there is more competition for access to these resources. C.

torquatus should spread out during foraging and form subgroups more frequently

during periods of less food abundance.

4.5 Methods

Data were collected on a group of red-capped mangabeys (N=~70) located in the

Sentier Nature forest of Sette Cama, Gabon. The average annual temperature ranges

from 240-280 C and the average rainfall is around 2100 mm (Lee et al., 2006). The forest contains three microhabitat types: terra firme forest, coastal palm forest, and

199

mangrove forest (Figure 4.1). These habitat types are not evenly distributed and 20.11

ha of the mangrove habitat was inaccessible to researchers. Unfortunately, this area

was frequented by the mangabey group during the study.

GPS data were collected to estimate the home range of C. torquatus and to map

and analyze the areas of the Sentier Nature forest used by the group. The GPS points

(using the Universal Transverse Mercator [UTM] projection, Zone 32 South, WGS84

datum coordinate system) were collected with a Garmin eTrex handheld GPS. The

positional error of GPS points was usually 5 meters or less.

Ranging data were obtained during both phases of the study period: the

prehabituation stage (February 2008 – April 2009, excluding December 2008 and

January –March 2009) and the systematic behavioral data collection stage (May –

September 2009). Because the group was not habituated during the early phase of the study, their ranging area may not be adequately represented. Sampling was also limited by the inaccessibility of certain areas of the home range and logistical issues (as discussed in chapter 2). However, these ranging data can be used to provide a general idea of where C. torquatus were located within the study forest.

Data were collected five days a week (not necessarily consecutive) from 7:00 am until noon and then again in the afternoon from 2:30 pm until dusk (see chapter 2 for more details). Each day in the field, GPS points were taken every 10 minutes from initial group contact until the group was no longer in sight. Most ranging studies take the location from the center of the group, but the habituation levels of this C. torquatus

200

group prohibited the use of this method in all instances. Points were taken after the

group had moved on or from the periphery of the group. The GPS points were then

transcribed into a notebook and transferred to Microsoft Excel for analysis in ArcGIS 10.

With each C. torquatus encounter, I also noted if the whole group was present or

if it was a subgroup. The group was considered to be divided when members were at

least 500 meters apart. This is a larger distance than would be expected for normal

group spread.8 In most cases, the subgroups contained at least one dominant male who

gave a loud call to the other subgroup’s dominant male. This further verified the

presence of subgroups.

4.5 Data Analysis

All home ranges and ranging estimates were calculated using geostatistical and

geospatial analysis techniques in ArcGIS 10. The most common methods for

determining home range size include the grid cell analysis (Hayne 1949), the minimum

convex polygon method (Ostro et al., 1999), and the kernel method (Worton 1989). For

this study, the combined C. torquatus ranging areas were calculated using the grid cell and minimum convex polygon (MCP) methods. The monthly and seasonal home ranges were calculated only using grid cell analysis. Grid cell analysis calculates the number of quadrants entered by the group. The grid cell method tends to be the most

8 The typical group spread of sooty mangabeys during terrestrial feeding is around 100 meters (McGraw, 1996a; McGraw et al., 2011).

201

conservative method and is dependent upon the grid size selected. Nevertheless, this

method is the most commonly used technique in other mangabey studies, and

therefore, it is used for this analysis.

I selected a grid size of one hectare (100 x 100m) in consistency with other

mangabey studies (Shah 2003; Devreese 2010). This also corresponds with estimates of

group spread among Cercocebus species (Shah 2003; McGraw et al., 2011). I calculated the total number of different quadrants entered per month, the total number of quadrants by season, and summarized the overall habitat usage density as a percentage of total GPS points per grid cell.

For the MCP method, an estimate of range size “…is constructed by connecting the outer locations to form a convex polygon, and the area of this polygon is then calculated” (Grueter et al., 2009:81). The MCP adjusts for outlying points but often results in an overestimation of range use because it can include areas never entered by the animals (Worton, 1995; Ostro et al., 1999; Kaplin, 2001). This method is most appropriate when the number of data points is low and for calculating monthly and seasonal home ranges (Grueter et al., 2009; Seaman et al., 1999). The cumulative MCP data are presented.

The ranging data were also analyzed in comparison to the phenology data from

January – September 2009. I divided the data into wet (September – December, March

– May) or dry seasons (January – February, June – August) based on the overall climate trends in Gabon. These data were then mapped with the trees that were in fruit (or had

202

a phenology score of 1 or 2) during those months. Because phenology data were only

taken during 2009, these results are used with ranging data taken from both 2008 and

2009. Table 4.2 lists the months combined for each map and the season type. October

2008 and September 2009 were not included in the analysis because they only

represent one month of that particular season.

Even though the data are lacking for several months in 2008 and 2009, some

broad conclusions can be made about C. torquatus ranging in relationship to the spatio-

temporal availability of food. I provide qualitative interpretations of movements

compared to food availability, and then the data were tested for any statistical

relationships in ArcGIS 10. First, the data were plotted as a scatterplot matrix to see if

there was a linear relationship among the points. Next, the GPS points of C. torquatus

movements were tested for spatial auto-correlation using the Global Moran’s I statistic.

This determines if C. torquatus movements were clustered, dispersed, or random.

Finally, given a non-random distribution of C. torquatus movements, the relationships

among fruiting trees and movements were tested for significance using the

Geographically Weighted regression analysis in ArcGIS 10. When testing for specific relationships between certain tree species (such as Sacoglottis gabonensis) the data

field was narrowed to only include the GPS points that were within 5 meters of the

chosen target.

203

The subgrouping data were not statistically analyzed because it was too difficult

to obtain accurate numbers of the frequency and composition of subgroups. Therefore,

I present some qualitative observations to develop hypotheses for future testing.

4.7 Results

Ranging Behavior

I collected 635 GPS points on C. torquatus movements from March 2008 –

September 2009 (excluding the months of August, November, and December 2009 and

January – March 2009). A total of 396 GPS points were taken during May – September

2009 (the period of systematic behavioral observations). GPS points were collected

over a total of 84 days between 2008 and 2009 (Table 4.3). Figure 4.2 illustrates the

total number of GPS points collected each month. The most GPS points were collected

in August 2009 (102) and the least points in July 2008 (11). Sampling efforts were

uneven among study months.

The area of the entire Sentier Nature forest is 254 ha, and C. torquatus most likely ranges throughout the entire forest. However, during the study, C. torquatus

sightings and follows were limited to the central area of the forest. The two different

methods for estimating range size yield different results. The cumulative grid cell range

size was 99 hectares (Figure 4.3). Using the minimum convex polygon method, the

cumulative range was estimated at 143.73 ha (Figure 4.4). These estimates fit with the

observation that grid cell analysis yields a more conservative estimate of range size.

204

The monthly values for the grid cell method are presented in Table 4.3. Figures

4.5-4.6 show quadrant use per month as estimated by the grid cell method. C.

torquatus used between 8 and 38 1-hectare quadrants during the study period. The

average number of quadrants entered was 22.2 (Table 4.3). The highest number of

quadrants were used in June 2009 (38) followed by October 2008 (28). The fewest

quadrants were used in July 2008 and April 2009 (8).

There doesn’t appear to be a relationship between season and the number of

quadrants used. Both the highest and lowest number of quadrants used occurred

during both the wet and dry seasons. An analysis of the mean quadrant use by season

using two-way ANOVA reveals no significant correlation (F=38.793, p<0.001). The average number of hectares used was highest in the dry season of 2009 (33 1-ha quadrants) and lowest in the dry season of 2008 (15.5 1-ha quadrants). This may also be influenced by the overall number of data points collected in 2009 compared to 2008.

Unfortunately, both the grid cell and MCP methods both represent underestimates of the total area used by C. torquatus during this study period. The area of C. torquatus sightings most likely represents the most intensively used portion of their home range. The mangabeys were outside the trail system several times during the study. Indeed, the staff of the two eco-lodges bordering the Sentier Nature forest reported seeing the mangabeys on days when we could not locate them. Furthermore, the group went to the inaccessible swamp zone on a daily basis. Shah (2003) encountered similar issues when studying agile mangabeys in Central African Republic.

205

She writes, “These home ranges are undoubtedly underestimates… mangabey groups

were still entering new areas at the end of the study…” (Shah 2003:95). Therefore, the

overall home range of C. torquatus is best estimated as the area of the Sentier Nature

forest or 254 hectares.

Even though the overall home range is an underestimate, we can examine how

C. torquatus used the Sentier Nature forest. C. torquatus movements were spatially correlated and clumped in distribution (Moran’s index: 0.596, p=<0.001). This statistic is not surprising for several reasons. First, the method of GPS point data collection lent itself to including many points in a similar location. Second, many of the points were collected during feeding or foraging periods. Nevertheless, if C. torquatus was moving to particular trees at particular times of the day, the points would also be expected to be clustered in space.

Figure 4.7 illustrates the intensity of range use by C. torquatus. The more times

the group was located in a quadrant, the darker the color on the map. C. torquatus was

most frequently observed in the area bordering the swamp zone by the lagoon. This

area of the forest features many lianas and fruit trees (pers. obs.) and was the location

of the majority of the important fruiting trees (Figure 4.8; Chapter 2). C. torquatus was

observed least frequently along the coastal palm forest which is more open and

contains fewer fruiting trees.

The top two food species for C. torquatus were Guibortia tessmannii and

Sacoglottis gabonensis (Chapter 3). A map showing the density of observations and

206

locations of S. gabonensis and G. tessmannii trees reveals that GPS points were the most concentrated in this region (Figure 4.9). Again, the Moran’s I global index revealed the

data points were significantly clumped throughout the Sentier Nature forest.

Ranging and food availability

The location of C. torquatus movements were significantly related to the location

of the phenology trees (F=0.414, p=0.05). The phenology trees were chosen because of

proximity to the trail system, and they were often visited by the C. torquatus group (see

also Chapter 2). The relationship between movements and the location of phenology

trees may have been related to the overall clumped distribution of the sightings (see

above), so the results were further analyzed by season. A comparison of the seasonal

ranging behavior of C. torquatus with food estimates derived from phenology transects

during 2009 reveals that seasonal movements were significantly related to the location

of fruiting trees each month of 2009 (wet season: F=0.664, p=0.05; dry season: F=0.019,

p=0.05). However, in each of these comparisons, the degree of significance in the

relationship between movements and fruiting trees is not very high.

Figures 4.10-4.13 illustrate the ranging and phenology GPS points by season. A

qualitative comparison of ranging patterns suggests that the movements of C. torquatus

most closely matched fruiting patterns during the dry seasons of 2008 and 2009. During

the dry season, the most species and individual trees were in fruit, and the majority of

these trees are located in the terra firme and mangrove habitats. Therefore, C.

207

torquatus ranged in this area to exploit the fruits that were in season such as Guibortia tessmannii, Sacoglottis gabonensis, Pycnacanthus angolensis, etc.

In the wet seasons of 2008 and 2009, C. torquatus were observed to follow fruiting patterns, but they also ranged in areas away from the fruiting trees in the coastal palm forest. The wet season is also a period of relatively low fruit abundance compared to the dry season. Therefore, the observations in the coastal forest may be related to the consumption of several foods that are available almost year-round (pers.

obs.) in this part of the habitat but that were not included in the phenology analysis9.

These foods include Chrysobalanus icacao seeds and Hyphenae guineensis palm fruits.

During June 2009, the most commonly eaten food was the H. guineensis palm fruits

which are only located in the coastal forest habitat (Chapter 3). This coastal habitat is

also where crab-eating was most often observed. In the months before the dry season

of 2009, the group appeared to expand its range to include the C. icacao shrubs located near the field station. The brigade officers would often report that they saw the group by the beach while my assistant and I were out in the terra firme and mangrove forest searching for the group (and not finding them).

Because of the suggested importance of Sacoglottis gabonensis seeds as a stable resource year-round for C. torquatus, I also analyzed ranging patterns in relationship to

S. gabonensis trees. C. torquatus included the S. gabonensis trees in their overall

9 Some of these foods, such as H. guineensis and C. icacao, were not known to be important parts of the C. torquatus diet when the phenology species were chosen for monitoring.

208

movements more often than predicted by chance (R2=0.81, Moran’s Index=0.27, p=<0.001). This supports the hypothesis that C. torquatus visit S. gabonensis trees in all seasons regardless of its fruiting status and suggests that C. torquatus were in the proximity of S. gabonensis trees in 81% of the observations.

I also compared ranging with the location of the most important C. torquatus fruiting tree (Chapter 3), Guibortia tessmannii, to see if their movements were significantly related to these trees. The relationship between movements and G. tessmannii trees is not as strong as the previous relationship (R2=0.43, Moran’s Index=

0.45, p=<0.001), but it is significant. This suggests that C. torquatus were in proximity of

G. tessmannii trees in 43% of the observations. The percentages for S. gabonensis and

G. tessmannii trees overlap because these trees are found near each other in several parts of the C. torquatus home range.

Subgrouping

C. torquatus in the Sentier Nature forest were observed in subgroups every month of the systematic study period (Table 4.4). Indeed, it was more common to

observe a subgroup rather than the whole group together during most months. The

number of days each month where subgrouping was observed ranges from a high of 9

days (June) and a low of 4 days (May) (Table 4.4).

There does not appear to be a trend in subgrouping behaviors in relationship to

fruit availability or season; however, the highest number of days of subgrouping

209

occurred in June when less trees were in fruit compared to the majority of the rest of

the study period (Figure 4.14). Because the systematic study only covered five months,

it does not provide a good impression of the influence of food availability on subgrouping. Overall, though, these data suggest that subgrouping is a very common phenomenon among C. torquatus in Sette Cama.

4.8 Discussion

Even though these data only represent part of an annual cycle, some broad

conclusions can be made about the ranging behavior of C. torquatus in Sette Cama.

Furthermore, these data create avenues for future investigations on the influence of

particular foods on ranging behaviors. The total area used by C. torquatus during the 12 months of the 2008-2009 study period differs by the methodology used to calculate range size. The red-capped mangabeys were observed using between 99 (GCA) and 143

(MCP) hectares of the Sentier Nature forest. These numbers underestimate the probable total home range of this group (200-300 ha); however, they do provide an idea of how the monkeys were using their habitat during the study period.

Ranging compared to other Cercocebus species

The home range size of C. torquatus in Sette Cama was less than that of other

Cercocebus species (Table 4.1). A comparison of C. torquatus and C. agilis shows that the number of 1-hectare quadrants used by C. torquatus was much lower than the C. agilis group at Mondika. C. agilis ranged over 23 to 66 1-hectare quadrants (Shah,

2003). In comparing the use of space among C. torquatus and other Cercocebus species,

210

C. torquatus most closely resembles C. galeritus. C. galeritus occupies a home range of up to 47 hectares (Wieczkowski, 2005). This group of C. galeritus increased their home range size from 17 to 47 ha over a 30 year period (Homewood, 1978; Wieczkowski,

2005). However, the estimated overall home range size of C. torquatus in Sette Cama is the area of the Sentier Nature forest, or 254 hectares. This is similar to that of the C. torquatus population in Campo, Cameroon (Mitani, 1989) despite the much larger size of the Sette Cama population.

The similarity in home range size between the Campo population of C. torquatus and the Sette Cama population is surprising. The Sette Cama population includes at least 70 individuals whereas the Campo population features around 25 individuals.

However, the Sette Cama population is limited in their home range size by the size of the Sentier Nature Forest. They are essentially living in a fragmented forest that is bordered on both ends by human settlements (see Chapter 2 for more details on the field site). The Sette Cama group has no option but to live in this restricted area, yet these mangabeys live in a larger group size than other mangabeys in similar sized home ranges. The intensive use of their habitat (as exhibited by the clumped distribution of ranging and high degree of vertical group spread) perhaps allowed this C. torquatus population to increase.

The C. torquatus population in Campo is also composed of more than one group.

Mitani (1989) reports, “At most, five C. torquatus troops were counted in the 276-ha census area per day. However, only [two] troops regularly used the area” (311).

211

Around 30% of the home ranges of these two groups were overlapping. This suggests

that the home range of the main study group in Campo is able to support a higher

number of red-capped mangabeys than were found in the group. A current census of

this population may reveal an increase in group numbers over the past twenty years.

Range size versus group size

C. atys in Taï most closely resembles C. torquatus in Sette Cama in group size.

Despite having similarly large groups, C. torquatus occupies a much smaller area than C.

atys. Therefore, the question is how does the C. torquatus population in Sette Cama

survive in such a small habitat area? There are several plausible explanations. First, C.

torquatus occupies multiple forest strata during feeding and foraging, or has a wide vertical group spread. Second, the high density of identifications in certain forest areas may suggest that C. torquatus intensively forages its habitat.

As shown in chapter 2, C. torquatus use multiple levels of the forest at one time.

The group members used different forest strata during activities and frequently were

seen from the ground to 30 meters in the canopy. Similarly, Shah describes C. agilis as

“…typically [seen] anywhere from the ground to 30 meters in the canopy. One could

think of a foraging group of agile mangabeys occupying a sphere of space…” (2003:100).

This foraging technique of spreading out, both vertically and horizontally, may serve to reduce intragroup feeding competition. For example, a red-capped mangabey might feed on S. gabonensis seeds on the ground while another individual eats Guibortia fruits from the canopy.

212

The data presented here also suggest that the C. torquatus population at Sette

Cama manages to maintain its large group size in a small area by intensively using its

resources and ranging in areas with high fruit availability. Shah (2003) noted a similar

phenomenon among agile mangabeys in Mondika. “…[A]gile mangabeys seemed to

exploit each small area in their home range much more thoroughly by foraging around

the same local area extensively, … [returning to] areas they had just visited (especially

when foraging on the ground)” (Shah 2003:100). C. torquatus moved throughout its home range but always returned to the area by the mangrove forest (pers. obs.), which contained many fruits and seeds.

As mentioned above, C. torquatus occupies multiple levels of the forest. C. torquatus in Sette Cama feed from terrestrial food sources in over 50% of their feeding time. The addition of Sacoglottis gabonensis seeds is a major difference in the diets between C. torquatus in Sette Cama and Campo, Cameroon (Mitani, 1989)10. S.

gabonensis seeds are a resource that persists year-round and are available underneath the Sacoglottis trees. The ranging data suggest that C. torquatus repeatedly returns to the area of the forest with a high concentration of Sacoglottis trees. A reliance on intensively foraging on terrestrial obdurate foods may mitigate the intragroup feeding competition that limits group size in other sites.

10 Mitani (1989) did not observe the Campo population eating S. gabonensis seeds but that does not preclude the possibility that it is a food source for this population.

213

The harvest-efficiency hypothesis has been proposed as an explanation for the large group size of C. agilis in Bai Hokou (Altmann, 1974; DeVreese, 2010).

According to this hypothesis, foraging efficiency may be higher in large groups when individuals can better regulate their return time to patches previously depleted by themselves or other group members. Continuous terrestrial foraging on dispersed, slowly regenerating food items may be indicative in this respect (Devreese, 2010:6).

According to this argument, it is more efficient for large groups that forage on slowly accumulating resources to feed together. This reduces the energy required to monitor the food patches. However, DeVreese (2010) does not provide data on the subgrouping behaviors of C. agilis in Bai Hokou. This may be another mechanism for adapting to slowly accumulating resources in a large group (see below for discussion).

Ecological adaptability has important implications for the conservation and reintroduction of red-capped mangabey groups. Since mangabeys seem capable of intensively exploiting their home ranges, the overall area of the home range may not be as important as the quality of the foods available in that area. Because they are able to exploit such a wide variety of foods, and occupy multiple forest strata, mangabeys can survive in areas with a few key food species such as S. gabonensis. The C. torquatus mangabeys appear to be efficient at exploiting their available resources and show ecological flexibility. Despite their isolation to a 300 hectare patch of forest, the Sentier

Nature C. torquatus population is thriving.

Ranging and the spatio-temporal availability of foods

Unlike the C. torquatus population in Campo, Cameroon, C. torquatus in Sette

214

Cama do not appear to dramatically shift their ranging behavior by season. There was a correlation between movements and all the fruiting trees by season among C. torquatus in Sette Cama, but it was only slightly significant. Mitani (1989) observed C. torquatus using different quadrants by season within their overall home range. The Campo population used different “seasonal ranging areas” every three months. C. torquatus in

Sette Cama may range more frequently in parts of the forest with fruiting trees during the dry season; however, they appear to include all areas of the forest in their movements during the wet season and to some extent, during the dry season.

Mitani (1989) also observed a significant correlation between ranging patterns and several fruiting trees among the Campo, Cameroon C. torquatus population.

The members of this mangabey species which depended considerably on the fluctuating food resources produced by the canopy trees, possibly varied their “seasonal ranging area” size and/or the location of their core area according to the spatial distribution of the main food fruits, thus realizing a stable fruit acquisition (Mitani 1989: 319).

Similarly, the ranging behavior of the Sette Cama C. torquatus group appears to be influenced by the location of their top two fruiting trees, S. gabonensis and G. tessmannii. The reasons for the relationship could be the presence of S. gabonensis seeds below the fruit trees. This is a stable food source almost year-round, and the seeds were included in the C. torquatus diet in nearly every month of study (Chapter 3).

The significant inclusion of G. tessmannii trees in the C. torquatus ranging patterns may suggest that they are monitoring the status of an important food source.

215

Future studies in Sette Cama will probably reveal more distinct seasonal ranging

trends. For example, during the period of Guibortia fruiting (June-August), the C.

torquatus group in Sette Cama used areas outside their normal range. We observed the

group in a patch of forest by the research station which contained many Guibortia trees

on several occasions.11 However, the group always returned to the main forest.

It is also important to note that C. torquatus relies upon several other foods that

are available almost consistently year-round including Chrysobalanus icacao seeds and

H. guineensis palm fruits. These foods likely influence the movements of C. torquatus in

periods of lower food abundance. The fruiting patterns and specific location of these

trees and shrubs should be included in future phenology and ranging studies among this

population.

Subgrouping

The grouping behaviors of C. torquatus in Sette Cama are perplexing. They were

often observed to divide into at least two subgroups. It was assumed that they were in

subgroups when we heard the groups contact calling each other from at least 500

meters apart. The subgroups would travel and forage separately, but they appeared to

reconvene at the mangrove habitat (Chapter 2) during mid-day and at the end of the

day. Occasionally we observed the whole group together, but the number of times the

whole group was in association was probably underestimated because of the wide

11 When the group was observed outside of the forest, it was never during systematic behavioral sampling. Usually we spent the day searching for the group and did not locate them in the forest and returned to camp to hear (or see) that they had been in a different part of their range.

216 degree of group vertical and horizontal spread. Shah (2003) had difficulty identifying subgrouping among agile mangabeys because they can forage up to 100 meters apart and in multiple trees. The red-capped mangabeys in Sette Cama were also often very spread out during foraging and travel, but when the whole group was together, there were noticeable differences in the amount of mangabeys occupying a particular space.

The high frequency of subgrouping among C. torquatus in Sette Cama suggests that this is an important mechanism in maintaining a large group size in a small habitat.

As mentioned earlier, the C. torquatus population studied by Mitani (1989) contained several groups with overlapping home ranges. Mitani (1989) also reports that his main study population formed subgroups during foraging. Perhaps the Sette Cama group is actually two (or more) separate groups that convene to form a supergroup, as seen among other species such as C. galeritus and mandrills (Homewood, 1978; Abernethy et al., 2002). Further study on the frequency and composition of subgroups among the

Sette Cama population can shed light on the exact nature of their flexible grouping strategy.

4.9 Future directions

Cercocebus is a genus characterized by flexibility and versatility. The ability to feed and travel in multiple forest strata is reflected in their morphology, range size, and group composition. Future studies in Sette Cama should include more trees in the phenology analysis to compare to ranging patterns. This will help determine if ranging at this site is more strongly correlated with season.

217

Another adaptation to seasonality of food resources and range size includes the

shifting of group size and composition. Most Cercocebus species have been observed

subgrouping, and C. torquatus frequently divided into at least two subgroups in Sette

Cama. This is probably another mechanism to adapt to living in large group sizes and

feeding on foods that are highly concentrated in space. Dividing into subgroups helps

minimize feeding competition within large groups. Future studies should focus on discerning how and when C. torquatus subgroup. Studies on the degree of within group feeding competition can also shed light on the mechanisms driving subgrouping among

C. torquatus. The relationship between food availability, season, and subgrouping remains to be discovered among the Cercocebus-Mandrillus clade, but it is likely a key adaptation for this group.

218

Species Group Home Site Source Size Range (hectares) C. agilis 21-22 303 Mondika, Shah, 2003 CAR C. agilis 230 1000 Bai Hokou, Devreese, CAR 2010 C. atys 100+ 700-800 Taï, Côte McGraw et al., d’Ivoire 2011 C. galeritus 36 17 Tana River, Homewood, Kenya 1976; Kinnaird, 1990 C. galeritus 17 19 Tana River, Kinnaird, 1990 Kenya C. galeritus 50 47 Tana River, Wieczkowski, Kenya 2005 C. sanjei 62 300 Udzungwa, Mwawende, Tanzania 2009 C. 70+ 200-300 Sette Cama, Cooke and torquatus Gabon McGraw, 2007 C. 25 250 Campo, Mitani, 1989, torquatus Cameroon 1991

Table 4.1: Summary of known ranging and grouping data for Cercocebus species.

219

Figure 4.1: The distribution of habitat types within the Sentier Nature forest, Sette Cama, Gabon. The area in red is the inaccessible swamp zone frequented by the red- capped mangabeys.

220

Number of GPS Points By Month 120 100 80 60 40 # GPS Points 20 0

Figure 4.2: Total number of GPS points collected for C. torquatus by month and year.

Group Months and Year Season 1 March, April, May 2008 Wet 2 April 2009, May 2009 Wet 3 June, July 2008 Dry 4 June, July, August, September Dry 2009

Table 4.2: Summary of the months represented in the phenology and ranging maps by season.

221

Figure 4.3: The cumulative range use of C. torquatus in 2008 and 2009 calculated with the grid cell method. Each square represents 1 hectare (100 x 100 meters).

222

Figure 4.4: The cumulative range use of C. torquatus in 2008 and 2009 calculated by the minimum convex polygon method.

223

# Month Year Quadrants # Days March 2008 25 12 April 2008 15 4 May 2008 16 9 June 2008 23 8 July 2008 8 4 October 2008 28 6 April 2009 8 4 May 2009 30 4 June 2009 38 10 July 2009 26 6 August 2009 35 11 September 2009 14 6

Average 22.17 Total 84

Table 4.3: The total number of 1-hectare quadrants used in each month of the study and the total number of days of data collection each month.

224

Figure 4.5: Grid cell maps for the 2008 study period. Each cell represents 1-ha (100x100m). The number of days of data collection differed in each month: March (12), April (4), May (9), June (8), July (4), and October (6) (after Shah, 2003).

225

Figure 4.5: Continued

226

Figure 4.6: Grid cell maps for the 2009 study period. Each cell represents 1 hectare (100x100m). The number of days of data collection differed in each month: April (4), May (4), June (10), July (6), August (11), and September (6) (after Shah, 2003).

227

Figure 4.7: The density of observations by quadrant during 2008-2009. Each square represents 1 hectare (100 x 100 meters). The higher the intensity of the red color, the more GPS points taken in that area.

228

Figure 4.8: The location of phenology trees compared to habitat use in 2008-2009. Each square represents 1 hectare.

229

Figure 4.9: The location of Guibortia and Sacoglottis phenology trees compared to habitat use during 2008-2009. Each square represents 1 hectare.

230

Figures 4.10-4.11: The movements of C. torquatus compared to fruiting trees during the wet (March-April-May) and dry (June-July) seasons of data collected during 2008.

231

Figures 4.12-4.13: The movements of C. torquatus compared to fruiting trees during the wet (April-May) and dry (June-July-August) seasons of data collected during 2009. 232

Whole Group Subgroup Total Days of Observation May-09 3 4 5 Jun-09 3 9 10 Jul-09 1 6 6 Aug-09 5 8 11 Sep-09 2 5 5

Table 4.4: The total number of days that C. torquatus were observed as the whole group and as subgroups compared to total days of observation for May to September 2009.

Grouping patterns compared to number of trees in fruit May - September 2009 50 45 40 35 30 # Trees 25

Days Subgroup 20 Whole Group 15 10 5 0 May-09 Jun-09 Jul-09 Aug-09 Sep-09

Figure 4.14: The total number of days C. torquatus were observed as a whole group and as subgroups compared to the number of fruit trees available each month for May to September 2009.

233

Chapter Five: Locomotion

5.1 Introduction

Studies of positional behavior are critical for understanding how a primate is

suited to its particular environment and also for reconstructing the movement and

ecology of extinct primate species (McGraw, 1996a; Prost, 1965). The members of the

genus Cercocebus, a group of medium-bodied, semi-terrestrial African monkeys, are

adapted for both arboreal and terrestrial movements (Fleagle, 1999). This study examines the locomotor behavior of C. torquatus with the goal of understanding the

overall patterns of locomotion in different contexts and how this species compares with

other members of its genus and its former clade members, Lophocebus. I also attend to

larger issues within the study of primate locomotion by addressing the following

questions: 1) Do sex and age affect locomotion and support use, and 2) Does

locomotion vary across two distinct habitat types (terra firme forest and coastal palm

forest)? These data are used to create a locomotor profile for C. torquatus that

addresses both ecological and ontogenetic variation. Finally, these findings are

combined with studies on the phylogeny of the Cercocebus genus to help illuminate the

adaptive radiation of this primate group.

234

5.2 Background

Compared to most other mammalian groups, primates display diverse locomotor

adaptations. Primate locomotion is highly variable and each locomotor type represents

a different solution to problems presented by the environment. A primate’s locomotion

influences most other aspects of its life including how and where it feeds, ranging

patterns, and escape from predators (McGraw, 1996a). For example, Callitrichids, a

group of small New World monkeys, retain claws that allow them to cling and leap to

large tree trunks where they feed on gum and insects (Fleagle, 1999; Garber and Kinzey,

1992). The elongated forelimbs and mobile shoulder joints of hominoids enable them

to exploit an arboreal environment using suspensory locomotion and brachiation

(Fleagle, 1999; Hunt, 1992).

Functional morphology and positional behavior are two fields concerned with

primate locomotion, posture, and morphology. These fields combine both behavioral and anatomical observations and offer insights into the movements and lifeways of extinct primate species. When strong connections between musculoskeletal form and behavioral function in extant species are identified, scientists can discern a fossil

primate’s locomotion and adaptations.

Primate functional morphology examines the relationship between

musculoskeletal form and its corresponding locomotor function (Bock and von Wahlert,

1965; Fleagle, 1979). Because a primate’s musculoskeletal system is adapted to routine

and critical forces that act upon it, researchers can predict how primates should move

235

based on their skeletal characteristics (Hunt et al., 1996). Most primate functional

morphology studies are conducted in laboratories and focus on biomechanics or skeletal measurements. These studies concentrate on applying mechanical laws to movements and determining the full range of locomotor capabilities of both non-human and human

primates (e.g. Demes, 2007; Demes et al., 1999; Richmond and Jungers, 1995).

Studies of movement also explain how extant primate species adapt and live in

their distinct environments. The form-function relationship can only be truly

understood by combining studies of morphology with behavioral observations in the

wild (Bock and von Wahlert, 1965; Prost, 1965; Ripley, 1967). Positional behavior refers

to a primate’s movements in a natural setting and allows researchers to observe how

and when primates employ particular movements (McGraw, 1996a; Prost, 1965).

Positional behavior is divided into two categories: locomotion and posture (Prost,

1965). Broadly speaking, locomotion is the displacement of body mass from one place

to another (Ripley, 1967). Primates use different types of movements such as walking, running, or leaping, which vary depending on activity, environment, and skeletal morphology.

Postural behavior, on the other hand, involves little or no displacement of the body (Rose, 1974). During postural activities, movement is primarily restricted to the limbs and the trunk remains stationary (Prost, 1965). Although it is thought that postures have less effect on skeletal morphology than locomotion, posture is an important component of a primate’s life (Fleagle, 1999). In most cases, primates spend

236 a greater amount of time in postural behaviors than locomotion, and primates use a wider variety of postural behaviors than locomotor behaviors (Rose, 1974; McGraw,

1998b). Some examples of postures are sitting, suspending, or standing, and postural behaviors are employed during feeding, foraging, resting, or social behaviors (Bicca-

Marques and Calegaro-Marques, 1993; McGraw, 1998b).

Fleagle (1976) conducted one of the first studies to combine functional morphological data with positional behavior data. He related skeletal differences in limb proportions and articular surfaces in two species of Malaysian leaf monkeys,

Presbytis obscura and Presbytis melalophos, to their locomotor behaviors. Fleagle found that the more saltatory species, P. melalophos, had longer hindlimbs and more extensive articular surfaces on the femoral head than P. obscura, a primarily quadrupedal species. The lengthened hindlimbs of P. melalophos increased the distance of accelerating force required during leaping and the structure of the femoral head allowed for more femoral excursion. Because these skeletal traits are very strongly correlated with locomotor behaviors, these characteristics can be used to predict locomotion in fossil primate species.

Trends in Positional Behavior Studies

Early positional behavior studies searched for predictable relationships between positional behavior and variables such as body size, maintenance activity, and support use. Fleagle and Mittermeier (1980) suggested that as body size varies, animals perceive different environments within the same arboreal habitat.

237

The smaller animal would ‘see’ a relatively larger number of discontinuities that could only be crossed by leaping. A larger animal, by virtue of its longer dimensions, would see a relatively greater number that could be crossed by bridging or climbing. Thus, one would expect leaping to decrease with an increase of body size and climbing to increase with size (Fleagle and Mittermeier, 1980:309).

They also hypothesized that larger animals would be restricted to larger substrates because of the need to support greater body weights and maintain center of gravity above a branch.

As predicted, Fleagle and Mittermeier (1980) observed that as body size in seven

Surinam monkey species increased, the frequency of climbing increased and leaping decreased. In general, climbing was more common during foraging and primates used larger supports during travel than during foraging. During travel, the monkeys chose regular pathways on stable supports whereas feeding or foraging required movement to the smaller terminal branches where foods are located. Larger monkeys used larger arboreal supports whereas smaller monkeys used smaller supports. However, Fleagle and Mittermeier found few associations between locomotion and canopy layer or forest type.

The relationships outlined by Fleagle and Mittermeier (1980) served as hypotheses for further positional behavior research in other primate species (Doran,

1993; Garber, 1991; Gebo and Chapman, 1995a; Hunt, 1992; McGraw, 1996a). These studies revealed that the relationship between body size and locomotion is complex and body size is not always a useful predictor of positional behaviors and support use (Gebo and Chapman, 1995a; McGraw, 1996a, 1998a, 1998b). Research on other New World 238

species, such as Saimiri boliviensis and Ateles geoffryi, upheld Fleagle and Mittermeier’s

predictions for locomotion and body size but not support use (Fontaine, 1990). The

smaller Saimiri leaped more often than Ateles and Ateles used more suspensory

locomotion; however, both species used similar sized supports. Youlatos (1999, 2002)

compared support use among seven sympatric species in Ecuador and found no

correlation between body size and substrate size. Further studies in Ecuador also

revealed no consistent relationship between body size and locomotion (Cant et al.,

2003).

In Kibale Forest and Taï National Park, the body sizes of Old World monkey

species did not correspond with changes in locomotor frequencies in the direction observed in the Fleagle and Mittermeier (1980) study. For example, among Kibale primates, the larger species leaped more often than smaller species and smaller species climbed more often than larger species (Gebo and Chapman, 1995a). There was no consistent relationship between support size and body size in Kibale, and leaping was most often observed in the upper to mid-canopy.

In his study on cercopithecids in the Taï Forest, Ivory Coast, McGraw (1996,

1998a, 1998b) also found that body size did not consistently predict locomotor frequencies, larger monkeys did not always use larger supports than smaller species, and leaping is not only common in the understory layer. For example, the species with larger body sizes, the colobines, leaped more often than smaller bodied guenon species.

McGraw (1996, 1998a, 1998b) reasoned that leaping among colobines may be the best

239

way of negotiating the main canopy due to their lack of suspensory specializations.

These studies highlight the complexity of the relationship among body size, habitat use,

and positional behavior. Positional behavior appears to be related to an interaction of

multiple factors including diet, foraging strategy, and morphology (Garber, 2011).

Issues in Positional Behavior Studies: Intraspecific variation

Positional behaviors are constrained by anatomy, but other factors exist that may influence movements such as life history stage, predator avoidance, resource distribution, and habitat type (Dagasto, 1995; Doran, 1992; Gebo and Chapman, 1995a).

Each of these variables influences how a primate interacts with its environment in order

to find food and to survive, and these factors potentially change throughout a primate’s

life (Rose, 1979). For example, researchers suggest that morphological adaptations are

influenced by rarely occurring but critical events such as fleeing from a predator (Gebo

et al, 1994; Prost, 1965). Gebo and colleagues (1994) argue that leaping is more

developed in red colobus monkeys than other colobines because it is their primary

mode of escape from predators.

This question of intraspecific variation in positional behavior is important not

only for reconstructing extinct species’ behaviors but also for more precisely

understanding the relationship between anatomical form and the behavioral and

ecological function of that form. Gebo and Chapman note, “If the variation exhibited by

a single species in different contexts is large, then caution must be used in interpreting

interspecific differences on studies which are based on a single context” (1995a:493).

240

Therefore, it is vital to study the positional behavior of a species in a variety of different

contexts (both ecologically and ontogenetically) to determine whether or not positional

behavior is conservative. The sections below highlight some studies of intraspecific

variation in positional behavior.

Intraspecific variation: Habitat

Primates are faced with ecological challenges that may vary with habitat type.

Indeed, “The physical structure of an animal’s habitat presents obstacles to effective

movement and food acquisition…” (Cant, 1992:274). Therefore, primate locomotor

behavior is presumably influenced not only by morphology but also by the different

challenges presented by diverse habitats (such as differences in available substrates,

liana and tree densities, amount of canopy cover). For example, a heavily logged forest

may have longer distances between trees than an undisturbed forest. An animal that

normally leaps from tree to tree may be forced to climb down one tree and walk to the

next tree on the ground. This can impact locomotor behaviors by increasing the

frequency of quadrupedalism compared to leaping.

Some factors that must be dealt with during arboreal locomotion include: straightening the path of movement within trees, dealing with large vertical supports, crossing gaps, and increasing speed along the path of movement (Cant, 1992:276;

McGraw, 1996a). In the case of C. torquatus, members of this genus display

morphological adaptations for climbing on vertical supports such as tree trunks (Fleagle

and McGraw, 1999; Fleagle and McGraw, 2002). Cercocebus and Mandrillus have a

241

scapula with a tall suprascapular fossa and deep inferior angle (Figure 5.1). The

expanded inferior angle “…creates a large flange for the origin of the M. teres major [a retractor of the humerus], at the same time lengthening this muscle’s moment arm about the shoulder” (Fleagle and Meldrum, 1988:232). These features are important for species that climb. Other morphological characteristics found in Cercocebus and

Mandrillus associated with climbing include a broad basal ilium, a patellar groove with a more prominent medial lip (similar to that of climbing chimpanzees), and a rounded tibial shaft (Fleagle and McGraw, 1999, 2002; Ward et al., 1995). These morphological adaptations for climbing suggest that Cercocebus can survive in more open habitats with fewer horizontal arboreal supports. These features would allow mangabeys to travel on the ground between trees and then use vertical climbing to access foods.

Studies on a variety of primate taxa provide conflicting results as to the impact of habitat on locomotor behaviors. On the one hand, researchers have identified differences in locomotor frequencies associated with structural differences due to habitat type (Dagasto, 1992; Gebo and Chapman, 1995b; Remis, 1998; Walker, 1993).

For example, Gebo and Chapman (1995b) found that red colobus populations in Uganda differed in locomotor frequencies in primary, secondary, and pine forest types with a decrease in climbing in secondary and pine forest and an increase in the use of quadrupedalism.

Other studies found no locomotor differences within species over varying habitats (Cant, 1986; Doran and Hunt, 1994; Garber and Pruetz, 1995; McGraw, 1996a;

242

Schubert and McGraw, 2010; Schubert, 2011). Chimpanzees inhabit a wide range of

habitats across Africa from open woodland forest to closed forests, but there were no

significant differences in overall locomotor behavior or use of substrates among the

same subspecies of chimpanzees at different sites (Doran and Hunt, 1994). McGraw

(1996) observed similar locomotor behaviors and support use among the cercopithecid

monkeys using structurally distinct portions of the Taï Forest. Each species maintained

locomotor equivalence by selecting similar supports in both environments despite

differences in support abundance. However, McGraw (1996a) brought up an interesting

caveat to his and other habitat based studies. Perhaps the habitat differences are not

significant enough to influence locomotion. A more informative measure of the

flexibility of positional behavior may be an examination of primate locomotion in highly

disturbed or open forested areas. Schubert (2011) did find a difference in Lowe’s

monkey (Cercopithecus campbelli lowei) locomotion and support use when comparing populations in a significantly disturbed versus non-disturbed forest in Ghana; however, the locomotion of the ursine colobus (Colobus vellerosus) remained consistent regardless of forest type.

The contradictory results of these studies highlight the need for more research into the flexibility of locomotor behaviors among primates. It is important to understand if primates are conservative in their movements regardless of distinct habitat differences. If primates maintain locomotor equivalence in varying habitats, it

243 strengthens and validates reconstructions of extinct primate locomotion based on their modern counterparts.

Intraspecific variation: Sex and ontogeny

One would predict that high levels of sexual dimorphism or changes in body weight throughout the life cycle will impact positional behavior and substrate use. As body weight increases, a decreasing number of substrate sizes are negotiable. In particular, body weight may impact substrate use and positional behaviors in arboreal or semi-arboreal primates. “…[T]he animal’s perspective of the continuity of a given canopy—the relative number and diversity of travel paths available—varies between species, depending on their morphological and behavioral attributes” (Cannon and

Leighton, 1994:506).

In an arboreal environment, there are 3 main types of substrates available: the vertical trunk (which is the most stable), branches (stretch outwards from the trunk and taper towards the end), and twigs (the most slender, terminal part of a branch) (Fleagle,

1976; McGraw, 1996a). Preferred fruits and leaves are usually located on the smallest, terminal ends of the branches. This end of the branch is thinner, weaker, and more subject to deformation (Grand, 1972, 1984; Cant, 1992). Therefore, it cannot support animals over a certain size and these animals are forced to negotiate these substrates in other ways than smaller animals. The need for different solutions to obtain foods and travel through the complex arboreal environment should be reflected in positional behavior studies in sexually dimorphic species.

244

Contrary to predictions, the positional behavior studies that have compared sexes discovered few, if any, differences in positional behavior. (Doran, 1993; Gebo,

1992; Gebo and Chapman, 1995a; Remis, 1998). Doran (1993) found differences in arboreal locomotion between male and female chimpanzees but no variation in overall locomotion. Females used more quadrupedal locomotion in arboreal contexts whereas males increased in climbing. In mountain gorillas, despite adult males having two times the body weight of adult females, both sexes had comparable patterns of locomotion

(Remis, 1998). Orangutans (Cant, 1987), New World monkeys (Alouatta palliata and

Cebus capucinus; Gebo, 1992), and several species of Old World monkeys (Gebo and

Chapman, 1995a) also exhibit few differences in locomotor behaviors between the sexes. These trends suggest that locomotion between male and female adults within a species are conservative (Garber, 2011).

The ontogenetic effect on locomotion is a burgeoning area of inquiry in positional behavior studies based on the assumption that each age class presents distinct challenges for primates. As individuals age, they experience changes in body mass and length, motor skill, strength, and physiology. “…[Young animals]… have changing musculoskeletal systems, which, combined with an immaturity of motor control mechanisms, limit their ability to perform the controlled, deliberate locomotor behaviors of mature adults” (Workman and Covert, 2005:376). These factors impact a growing individual’s ability to negotiate its environment (Fleagle, 1999; Garber, 2011;

Wells and Turnquist, 2001). For example, younger primates have a smaller body size

245

and a shorter body length than their adult counterparts. Therefore, younger individuals encounter more discountinuous supports in the arboreal environment (Workman and

Covert, 2005). Younger individuals would have to leap to cross these distances, as opposed to bridging or quadrupedalism (Cant, 1992; Fleagle and Mittermeier, 1980).

The life stages before adulthood are also a crucial period of learning and discovery for a primate. A wider positional behavior repertoire might be expected among growing individuals because of the tendency of younger primates to play and explore their environment while learning how to forage and interact with peers

(Workman and Covert, 2005).

The results of investigations into the influence of age on positional behaviors are equivocal. Several studies did not find any major differences in locomotor behaviors among differently aged primates (Bezanson, 2006; Lawler, 2006). Two New World monkey species, Cebus capucinus and Alouatta palliata begin “adult-like” locomotion

early in life, but they displayed differences in actions such as bridging and leaping

among age classes (Bezanson, 2006). Lawler (2006) found no differences in positional

behaviors and substrate use in adult and juvenile sifakas due to the almost adult sized

hands and feet of juveniles.

Other studies suggest significant differences among age classes in positional

behaviors in several New World and Old World species. Infants use a more diverse

range of locomotor types than adults and younger individuals climb more or use more

arboreal supports than adults (e.g. Mountain gorillas: Doran, 1997; Howler monkeys:

246

Prates and Bicca-Marques, 2008; Macaques: Wells and Turnquist, 2001). In their study of several Asian colobines, Workman and Covert (2005) observed a larger number of positional behaviors among young animals than adult animals. Eakins and McGraw

(2010) observed similar trends in captive silvered langurs (Trachypithecus cristatus). The

younger langurs used a wider range of postures and were observed leaping and climbing

more often than adults. More research is necessary on a greater number of species in

order to elucidate the flexibility of positional behavior during ontogeny.

Morphological correlates of positional behavior and substrate use

Because one of the primary aims of positional behavior studies is to aid in the

reconstruction of extinct primate locomotion, it is important to recognize traits

associated with different types of locomotion and substrate use. Skeletal indices, such

as the intermembral index (humerus length + radius length/femur length + tibia length x

100) and brachial index (radius length/humerus length), are means to estimate a

species’ primary locomotor mode (Fleagle, 1976; 1999). Typically, leapers tend to have

longer hindlimbs for propulsion (low IMI), suspensory species have longer forelimbs

(higher IMI), and quadrupedal species have similarly proportioned forelimbs and

hindlimbs (intermediate IMI). For example, gibbons and siamangs are highly suspensory

species with intermembral indices ranging from 129-147 (Fleagle, 1999). The IMI for C.

torquatus is 83 whereas L. albigena (a more arboreal species) has an IMI of 78. This

suggests that Lophocebus has slightly longer hindlimbs than forelimbs as an adaptation

247

for leaping. A very high brachial index is associated with species that practice

brachiation or vertical clinging and leaping (Fleagle, 1976).

Primates using different forest levels also encounter distinct challenges, and therefore, the skeletal morphologies of arboreal and terrestrial primates display distinct characteristics associated with their preferred substrates and means of negotiating those substrates (Fleagle, 1976; Rodman, 1979). Arboreal travel requires contending with gaps in the forest canopy and maintaining balance and stability on branches of various sizes (Cant, 1992; Grand, 1984). Arboreal quadrupeds tend to have shorter forelimbs and hindlimbs than terrestrial quadrupeds. Arboreal quadrupeds use flexed limbs to lower the center of gravity and, therefore, usually have a long ulnar olecranon process (Fleagle, 1999) and highly mobile joints (Fleagle, 1976; Morbeck, 1977). The abducted limb postures of arboreal quadrupeds are also reflected in the high angle of the femoral neck and asymmetrical femoral condyles. Some arboreal primates have specializations for leaping such as elongated hindlimbs and a long ischium, both of which increase propulsive force and increase leaping distance (Fleagle, 1999). This helps cross gaps within the tree canopy. The tarsier, which uses vertical clinging and leaping, is known for its long hindlimbs compared to forelimbs.

Terrestrial travel provides a more uniform substrate and pathway but primates are also exposed to a different set of predators and food availability (McGraw and

Bshary, 2002). Terrestrial primates tend to have restricted joint mobility, adducted and extended limbs, and a larger body size than arboreal primates (Rodman, 1979).

248

Compared to arboreal quadrupeds, terrestrial species also have shorter digits adapted

for weight bearing and a posteriorly extended olecranon process (Fleagle, 1999).

The morphological distinctions between semi-terrestrial and arboreal primates are less clearcut. Semi-terrestriality is a unique adaptation found in the cercopithecids

(Nakatsukasa, 1994). Nevertheless, the category of “semi-terrestrial” is not well defined, and there is no threshold for distinguishing between a primarily terrestrial primate and a semi-terrestrial primate. For example, Japanese macaques have been described as semi-terrestrial based on substrate use (68.3% arboreal and 31.7% terrestrial for males and 39.8% arboreal and 60.3% terrestrial for females; Chatani,

2003) whereas Cercocebus atys is also considered semi-terrestrial and it spends 67.24% of its locomotor time on the ground (McGraw, 1998a).

Morphological studies also reveal the difficulties in defining the skeletal differences between arboreal and semi-terrestrial. Among guenons, semi-terrestrial and arboreal species share skeletal similarities related to arboreality regardless of environment or geography (Gebo and Sargis, 1994). Terrestrial guenons, however, are morphologically divergent from both the arboreal and semi-terrestrial guenons. The

terrestrial species have longer limbs and reduced joint surfaces. Nakatsukasa (1994)

had difficulty identifying characteristics that distinguished terrestrial from arboreal

guenons. Nevertheless, Nakatsukasa (1994) identified several differences in the

skeletons of Cercocebus (semi-terrestrial) and Lophocebus (arboreal) mangabeys

associated with positional behavior and habitat use. These studies show that within

249

different groups of species, it may be more difficult to define specific features related to

an arboreal versus terrestrial habitat. Furthermore, when a species (such as a semi-

terrestrial guenon) habitually uses more than one type of substrate, the skeletal

distinctions based on habitat use may be ambiguous.

Cercocebus

The phylogeny of mangabeys, a group of long limbed, medium-sized African

monkeys, has undergone many revisions over the last decade (Cronin and Sarich, 1976;

Hewett-Emmett and Cook, 1978; Groves, 1978; Groves, 2000; Fleagle and McGraw,

1999; Fleagle and McGraw, 2002). Researchers now agree that mangabeys should be

divided into two genera12: the arboreal Lophocebus and the semi-terrestrial Cercocebus

(Groves, 2000; Fleagle and McGraw, 1999). Furthermore, Cercocebus mangabeys are

more closely related to the Mandrillus genus than they are to the Lophocebus species.

The Cercocebus genus includes six species that range from West to East Africa: atys,

torquatus, agilis, chrysogaster, galeritus, and sanje.

Researchers have tried to elucidate the evolutionary history and radiation of the

Cercocebus-Mandrillus clade by comparing the distribution of morphological characteristics with the biogeographical distribution of each clade member (McGraw and Fleagle, 2006; Gilbert, 2007). McGraw and Fleagle (2006) identified a morphocline

12 A recently described monkey species, kipunji, was originally put in the genus Lophocebus based on its substrate preference and several skeletal features (Jones et al., 2005) but was later placed into its own genus, Rungwecebus (Davenport et al., 2006). Subsequent molecular investigations suggest that R. kipunji is a hybridization of Papio and Lophocebus (Burrell et al., 2009).

250

in several facial characteristics among mangabeys and mandrills. They found that out of

all Cercocebus mangabeys, C. torquatus, most closely resembled Mandrillus in the degree of paranasal ridging and shallow suborbital fossae on the crania (Figures 5.2 and

5.3). These data, along with the proposed dispersal route from central to eastern and western Africa of this clade (Grubb 1978, 1982) led to the hypothesis that C. torquatus is the sister taxon to mandrills and drills (McGraw and Fleagle, 2006).

A re-evaluation of Papionin fossil evidence suggests that C. torquatus retains the most morphological similarities with the earliest representative of the Cercocebus taxa,

Procercocebus antiquus (Gilbert, 2007). Procercocebus from Taung, South Africa dates to 1.5 – 2 million years ago. Gilbert argues that, “Rather than radiating east and west from the low latitudes of central Africa, a scenario must be considered where the genus arose in either western or southern Africa and dispersed north, south, and east from these regions occupied by P. antiquus and C. torquatus” (2007:85). Therefore, researchers disagree as to the status of C. torquatus within the Cercocebus-Mandrillus

clade. Either C. torquatus is the most derived of the Cercocebus species or it is the

ancestral Cercocebus species.

In order to understand how the Cercocebus-Mandrillus evolved and the polarity

of their morphological characters, it is critical to have an idea of how the living animals

move and utilize their environments. Knowledge of the behaviors of extant species

helps researchers more accurately reconstruct the lifeways of extinct species, as well as

elucidating any behavioral or morphological trends or changes among groups of

251

primates. Understanding the behavior of C. torquatus can shed light on the transition

from semi-terrestrial to terrestrial locomotion and the overall radiation of this group of

primates.

Studies also have to highlight the range of variation in positional behaviors

among the members of an entire genus, particularly when concerned with

reconstructing the phylogenetic history of a group. Researchers must understand not

only how morphology relates to behavior but also the adaptive significance of these

behaviors and how these behaviors evolved (Cant, 1992). In the case of the Cercocebus-

Mandrillus clade, it is argued that their semi-terrestrial positional behavior is part of an adaptive complex of characteristics that allows these species to exploit a hard-object

food niche unavailable to other sympatric primates (Fleagle and McGraw, 1999; Fleagle

and McGraw, 2002). Therefore, this study on the positional behavior of C. torquatus

offers insight into the behavioral manifestation of traits associated with this adaptive

complex.

Cercocebus positional behavior

Cercocebus is one of the least studied primate genera. The positional behaviors

of Cercocebus species have not been well documented. Cercocebus is defined as a semi- terrestrial genus (Fleagle, 1999), and C. atys from Taï National Park, Côte d’Ivoire, is the only species for which detailed positional behavior data were collected (McGraw 1996a,

1998a, 1998b). C. atys are semi-terrestrial quadrupeds that forage and feed near or on the forest floor (McGraw, 1996a, 1996b, 1998a, 1998b, 2007). C. atys climb during

252 feeding and foraging but do not frequently leap, despite being capable of crossing large gaps in the forest canopy. Sitting and standing are the predominant postures in C. atys.

There have been no quantitative, systematic studies on the positional behavior of C. torquatus. Jones and Sabater Pi (1968) noted that C. torquatus spends time on the ground and on mangrove roots. They also remarked that adult C. torquatus prefer larger branches than younger individuals, and C. torquatus climbed vines and large objects using head-first, hand-over-hand ascension (Jones and Sabater Pi, 1968). C. torquatus uses a digitigrade hand position during quadrupedal locomotion (Rose, 1973).

Trends in Cercocebus-Mandrillus morphology and predictions

Positional behavior and morphology influence how a primate subsists and survives. The positional repertoires of any species “…both limit and make possible other aspects of primate life” (Ripley, 1967:150). The locomotor and postural capabilities of a primate help determine its niche and influences how that animal utilizes its environment. This is particularly applicable to Cercocebus and Mandrillus species.

In their attempt to further identify morphological traits that unite the

Cercocebus and Mandrillus genera, Fleagle and McGraw discovered skeletal similarities in each species (1999, 2002). Fleagle and McGraw hypothesized that the morphological similarities in the forelimbs of Cercocebus and Mandrillus are functionally related to a peculiar feeding strategy characterized by “aggressive manual foraging… and the processing of hard-object foods” (Fleagle and McGraw, 2002:267). The complex of osteological features found in Cercocebus and Mandrillus is proposed as an adaptation

253

that allows them to glean hard nuts and seeds from the forest floor. Specifically, the

humerus features musculoskeletal markers associated with habitual

pronation/supination and flexion/extension movements. These characteristics include

an expanded deltoid tuberosity, broad brachialis flange, and proximally extended and laterally widened supinator crests. The forelimb also has pronounced crest development that indicates prominent wrist or digit flexor musculature that would allow extensive manual and forelimb dexterity (Fleagle and McGraw, 1999; Fleagle and

McGraw, 2002). Although these are not positional behaviors, they relate to an overall

foraging strategy dependent upon a flexible and intensive use of the environment.

Anecdotal evidence has shown that during foraging, mandrills obtain terrestrial

food sources by aggressively pawing through the leaf litter and ripping apart logs for

arthropods and mushrooms (Hoshino, 1985). At least 60% of the C. atys diet is comprised of seeds and invertebrates gleaned from the forest floor (McGraw et al.,

2011). A preliminary study on the forelimb movements of cercopithecids in the Taï

Forest, Côte d’Ivoire reveals that C. atys uses raking and pronation/supination actions during over half of foraging observations (Kane, pers. comm). Shah (2003) also reports that C. agilis rummages through elephant dung to find undigested seeds.

Nevertheless, the locomotor and postural behaviors associated with foraging for food items have not yet been explicitly studied or quantified for this clade. Given the assumption that morphological form accurately predicts biological function, C. torquatus

254

should engage in extensive forelimb, wrist, and digit movement while foraging for

terrestrial food items as seen in the other Cercocebus-Mandrillus species.

One of the original goals of this project was to examine these movements but

limited time and visibility made this unachievable. However, it is still useful to compare

the amount of time feeding and foraging on the ground among Cercocebus species and the different feeding postures.

Morphological differences in Cercocebus and Lophocebus

Despite the difficulties of defining morphological differences between semi- terrestrial and arboreal guenons, Nakatsukasa was able to identify major distinctions in

Cercocebus and Lophocebus skeletal anatomies (1994a, 1994b, 1996). C. torquatus displays differences in limb morphology compared to Lophocebus albigena that are related to cursorial locomotion (1994b). In contrast to L. albigena, C. torquatus

“…displays in the humerus a large greater tuberosity, an acute intertuberosity angle, a weak medial torsion of the humeral head, a retroflected medial epicondyle, a proximally prominent greater trochanter, and a mediolaterally narrow distal epiphysis of the femur…” (1994b:133). These features give C. torquatus a longer lever arm with restricted anterior-posterior joint mobility compared to L. albigena. These more limited limb movements are associated with species that are primarily terrestrial quadrupeds and focus more on speed than flexibility and use adducted limb postures (Fleagle, 1999).

Furthermore, the retroflected medial epicondyle on the humerus aids in the use of the

255

wrist and hand flexors during pronation, a common forelimb position among terrestrial

quadrupeds (Fleagle, 1999).

At the time of Nakatsukasa’s study (1994), data on the positional behavior for

each genus were not available. A comparison of the positional behaviors of Cercocebus

and Lophocebus can help elucidate if the morphological differences among these genera

are translated behaviorally and also aid in defining semi-terrestrial locomotion.

5.3 Research Questions

I present information on the locomotor behavior of C. torquatus and examine if differences in age, sex, and habitat influence the use and frequency of different locomotor modes in this species. Given the lack of behavioral data on C. torquatus and the array of factors influencing locomotor behavior, the following questions were investigated:

1. What is the locomotor behavior of C. torquatus and is it conservative in different

habitat types? How does the locomotor behavior of C. torquatus correspond

with predictions based on morphology?

2. What is the range of variation in locomotor behaviors within the Cercocebus

genus?

3. Is there a difference in the amount of terrestriality among Cercocebus species? If

so, what factors account for these differences? Do the frequencies of substrate

use correspond with differences in locomotor behaviors? (for example, more

leaping in the more arboreal species)

256

4. Using Cercocebus and Lophocebus as a comparison, how different is semi-

terrestrial locomotion from arboreal locomotion?

5.4 Predictions

1. C. torquatus will use quadrupedal locomotion most frequently during all maintenance activities involving locomotion, but climbing will be more frequent than leaping during arboreal activities. C. torquatus will spend most of their time on the ground, and C. torquatus will use larger supports during arboreal travel than during arboreal feeding or foraging.

C. torquatus are classified as semi-terrestrial primates, and their anatomy displays many adaptations for quadrupedal locomotion (Nakatsukasa 1994, 1994b,

1996). Therefore, the overall C. torquatus locomotor profile should predominantly involve quadrupedal walking or running during travel, feeding and foraging. In general, cercopithecines have been found to be active during foraging and frequently travel while collecting and processing food items (McGraw, 1996a). I predict that among C. torquatus, quadrupedal walking will be the most frequently observed positional behavior and that many feeding or foraging events will occur during travel along the forest floor.

Additionally, C. torquatus should climb more frequently than leap during arboreal travel because of morphological features that suggest adaptations to climbing.

These skeletal traits include a short and deep scapula with pronounced extensor muscle

257

attachments, a broad based ilium, prominent medial margins of the patellar groove, and

a rounded tibial shaft (Fleagle and McGraw, 1999, 2002).

Climbing should also occur more frequently than leaping during periods of

foraging or feeding, “Because of the often patchy distribution of food within the canopy

(distributed on thin, unstable supports), acquisition of food requires a versatile

behavioral repertoire. For this reason, climbing assumes a more important role in

feeding than during travel” (McGraw, 1996a:263).

Monkeys tend to use larger supports more during travel because they are less

restricted in where they can move (McGraw, 1996a). Again, most food sources are

located on the smaller, more unstable terminal ends of branches. Even the sooty

mangabey, which spends the majority of its locomotor time on the ground, uses smaller

supports during feeding because it frequently climbs understory saplings to search for

food (McGraw 1998a). Therefore, C. torquatus should use smaller supports when

feeding or foraging compared to traveling. I expect that C. torquatus will move on large vertical supports by climbing or descending rather than leaping from one tree trunk to another during all locomotor activities.

2. There will be differences in locomotor behaviors between male and female adult C. torquatus, particularly in an arboreal context. Locomotion will also vary across age categories with juveniles showing a wider range of locomotor types on a variety of substrates (forelimb suspension, climbing on small substrates) than both subadults and adults.

258

There should be differences in locomotion between the sexes and the age

classes because of overall size differences. The two sexes have a large degree of

dimorphism (males=9.45 kg and females=5.5 kg; Smith and Jungers, 1997) and, presumably, maneuver through the arboreal environment differently. Other strongly sexually dimorphic species, such as chimpanzees, display differences in arboreal locomotion with females using more quadrupedal locomotion and males relying more

upon climbing (Doran, 1993). Among C. torquatus, heavier males are less likely to be supported by the smaller terminal branches, and therefore, should move between trees by vertically ascending and descending the large tree trunk. On the other hand, females should more frequently leap between trees on the terminal branches because of their smaller size.

I do not expect a difference in overall locomotion between subadults and adults,

but subadults may differ in arboreal locomotion from adult males based on size differences. Some ontogeny of positional behavior studies suggest that once a primate reaches a certain age, locomotor diversity declines (Bezanson, 2006; Eakins and

McGraw, 2010). Juveniles, though, should vary in their frequencies of locomotor types and substrate use compared to older individuals. As described above, primates that are smaller encounter and perceive more discontinuities in the forest canopy (Cant, 1992).

Therefore, juveniles should leap more frequently in above-ground contexts than adults

and subadults due to their smaller size and shorter body length. These features will also

259 contribute to a wider variety of locomotor types seen among juveniles such as arm suspension or climbing on lianas or twigs.

3. Locomotion will differ by forest stratum and tree zone but quadrupedalism will be the most common form of locomotion in all contexts. Climbing or descending will be higher at lower forest levels (0-10 meters) and the tree zone associated with the understory (Zone 5). Leaping will be more prevalent at greater forest heights (20+ m) and at the outer edge of tree zones (Zones 2 and 3) because of the greater distances between substrates.

Gebo and Chapman (1995a) and McGraw (1996) observed locomotor trends by forest level and height. Each level of the forest and zone of a tree presents different available substrates of varying size and stability for a primate to negotiate. I predict that

C. torquatus will leap more frequently in the upper canopy heights and at the outer tree branches (Zone 3). At these heights and position in the tree, supports are thinner, less stable, and more discontinuous (McGraw, 1996a). Therefore, leaping or climbing is required to negotiate these areas. Movement on the ground and inner tree branches

(Zone 2) will be quadrupedal because these supports are continuous and stable.

Locomotion in the forest undergrowth (Zone 5) will be primarily quadrupedal but C. torquatus may also climb among the small lianas and branches that characterize this zone.

4. Juveniles will be able to use smaller supports more frequently than other age categories and will be found more frequently in all forest strata.

260

The canopy architecture should also influence the preferred strata or forest

levels used by primates of different sizes.

As noted by McGraw:

If substrate size limits quadrupedal locomotion, then large-bodied quadrupeds are more likely to be found in the main canopy where large supports are generally more abundant. Smaller monkeys, because of the ratio of support to body size, are able to utilize a greater number of support types and can, consequently, more easily exploit more forest layers and will thus tend to be more widely distributed throughout all forest strata (1998a:497).

Juveniles should be able to negotiate smaller supports more frequently than the

other age categories because of their lower body mass. The smaller size of juveniles

may also preclude them from using large, vertical substrates, such as tree trunks with a

large DBH, because of difficulties in grasping the substrate with smaller hands (Cant,

1992).

5. C. torquatus will climb and descend more frequently in the coastal palm

habitat than the terra firme habitat.

Because C. torquatus are presumably primarily quadrupedal animals, I predict that

C. torquatus will most frequently use quadrupedal locomotion in both of the habitat types: terra firme and coastal palm beach forest. However, I expect C. torquatus to use climbing and descending more often in the coastal habitat because of a larger distance between trees and more strictly vertical supports (palm trees with few branches) in this habitat. I expect leaping to be more common in the terra firme habitat type because of the higher availability of fruit trees and more continuous canopy.

261

5.5 Methods

Study site and Subjects

Data were collected on a group of red-capped mangabeys (N=70) in the Sentier

Nature forest of Sette Cama, Gabon from May 2009 to September 2009. This forest, located between 2˚29’30” to 2˚30’58.7”S and 9˚43’24.3”E to 9˚44’56.2”E, is a protected area located in the Gamba Park Complex in southwestern Gabon. Annual rainfall is

2093 mm (Lee et al, 2006). The annual temperature is 24˚-28˚ C, and there are two dry seasons from June to September and January to February. This study site is a part of the

Brigade of Fisheries and Wildlife and is overseen by WWF-Gabon. The forest covers 254 ha and is bordered by the Atlantic Ocean on the west side and the Ndougou Lagoon on the east side.

Two habitat types were distinguished for this portion of the study—coastal palm forest (known hereafter as the beach forest) and terra firme forest. The beach forest is characterized by Hyphenae guineensis palm trees, scrub bushes, and an open canopy

(Figure 5.4). The terra firme forest features more tree species, extensive undergrowth and lianas, and a canopy that is almost completely closed (Figures 5.5 and 5.6). C. torquatus preferred the terra firme forest (Figure 5.7). This preference, and the lack of seasonal data, led to a higher number of scans in the terra firme forest than the beach forest. For a more detailed description of the different habitat types and their distributions, refer to chapter 2.

262

Behavioral Data Collection

Data were collected five days a week for a period of nineteen weeks from May –

September 2009. The days of the week in which data were collected often varied due to

weather conditions and the presence of elephants and buffalo in the forest. My field

assistants and I went into the forest two times a day: in the morning from 7:00 am to

11:30 am and in the afternoon from 2:00 pm until dusk. The monkeys spent mid-day

resting in the inaccessible swamp zone (see chapter 2), and therefore, we were unable

to obtain data during these hours.

Behavior was recorded using ten minute group scans every twenty minutes

(Altmann, 1974). Group scans are the most appropriate method of data collection when

interested in comparing behaviors across different age and sex classes. An average of

9.85 individuals was observed in each scan. Every effort was made to sample all

individuals of the group during each scan. Nevertheless, unequal habituation levels

made it possible that some individuals were more likely to avoid the observer, and

therefore, certain individuals were not sampled as regularly as others. Each group scan

represents only a subset of the entire C. torquatus group/subgroup under study. Issues of habituation level, visibility, and large group spread made whole group scans not

feasible at this site. Researchers studying this and other Cercocebus species report similar problems (Mitani, 1989; Shah, 2003). The groups did not flee or alarm upon contact with observers, but they were very aware of observer presence and would often look at us or stop activities and move to another area upon our arrival.

263

The variables noted during each scan are derived from Shah (2003) and McGraw

(1996) in order to facilitate comparisons with C. agilis (agile mangabeys) and C. atys

(sooty mangabeys). The variables not related to positional behavior are defined in detail in chapter 2. During group scans, for each individual seen, the data collected were: sex, age class (adult, subadult, juvenile), maintenance activity (travel, feed, forage, rest, socio-sexual, other), height (visually estimated in meters), positional behavior (locomotion and posture), forest zone, support size, and habitat type. The sex of subadults and juveniles were not noted because of visibility issues. It is also possible that subadult males were erroneously classified as adult females based on size similarities.

There also is a large difference in the number of scans by each maintenance activity. Travel was observed far more often than instances of feeding or foraging, and therefore, represents a bias in data collection toward more visible activities. These data definitely underestimate the amount of time C. torquatus devotes to feeding and foraging.

The categories of locomotion recorded include: quadrupedal walk (QW), quadrupedal run (QR), leap (LP), climb (CL), descend head first (DH) and descend bottom first (DB). All definitions are based on Fleagle (1977) and McGraw (1996a).

Quadrupedal walk was pronograde movement using all four limbs to support the body weight (Figure 5.8). Quadrupedal run was similar to quadrupedal walk but at a faster pace (Figure 5.9). Leap was movement from one substrate to another using the

264

hindlimbs for propulsion and landing using both the forelimbs and hindlimbs (Figure

5.10). Climbing was a vertical ascent on substrates oriented 45-90˚ using the forelimbs

to pull up the body while the hindlimbs propel the body upwards (Hunt et al., 1996;

Figure 5.11). Descend was vertical downward movement on a substrate with either the head or bottom section of the body leading the descent (Figures 5.12 and 5.13). The category descend was added to this study to supply more detailed information on locomotion (Cant et al., 2001).

Postural behaviors are the positions taken during stationary periods or during feeding and foraging and will be analyzed in the next chapter. Postures include: quadrupedal stand (QS), bipedal stand (BS), sitting (SI), lying (LY), suspend (SP), droop

(DP), and supported stand (SS) (definitions based on McGraw, 1996a). Quadrupedal stand was pronograde posture with support from all limbs. Bipedal stand included pronograde posture with support from only the hindlimbs. Sitting was an orthograde posture with the body weight supported by the ischial callosities or the lower body.

Lying included any posture where the trunk or limbs support body weight on a substrate. Suspend involved below substrate postures with the body weight supported by any combination of forelimbs and hindlimbs. Droop is similar to lie except the limbs hang below the trunk. Supported stand involves the hindlimbs supporting most of the body weight with one or both of the forelimbs above the head.

The mangabey’s location within the tree was recorded to determine which positional behaviors are used in different areas of the tree (McGraw, 1996a). This

265 provides an estimate of position within or around a tree. Trees were broken down into

6 zones (Figure 5.14). The ground was delineated as zone 0. Zone 1 included the tree trunk and any branches immediately adjacent to the tree trunk. Zone 2 was the area between Zone 1 and the terminal branches of Zone 3. Zone 4 is the uppermost layer of the tree or the top of the canopy. Zone 5 includes areas outside of the tree or directly adjacent to the tree such as lianas, tree falls, or small trees and shrubs.

During each positional behavior, the support size was noted. Definitions of support size are taken from Fleagle (1976) and McGraw (1996a). Large supports, or boughs, are branches that are larger than 10 cm and cannot be grasped by the hands or feet (Figure 5.15). Vertical tree trunks and fallen tree trunks were also classified as boughs. Medium sized supports, or branches, can be grasped by the hands or feet

(Figure 5.16). These include lianas and tree limbs. The smallest sized supports are twigs, and they are found at the terminal end of branches and are less than 3 cm in diameter (Figure 5.17). Very small lianas were also included in this category. When none of these substrates were used (in other words, the mangabey was on the ground and not a fallen tree or log), I noted the support as “ground”.

All supports were classified based on size regardless of the location. For example, a liana that was less than 3 cm in diameter was described as a twig. If a mangabey leaped from the smallest terminal branches of one tree to another, these were also classified as twigs (even if they grasped multiple twigs).

266

Vegetation Sampling

This study investigates if there are any differences in locomotion between the distinct habitat types of the Sentier Nature forest. Therefore, in order to determine the densities and distributions of tree and liana species and gain a broad characterization of each habitat type, 12- 100 m x 10 m vegetation transects were placed along the 3 main trails (see Chapter 2 for more details). Each transect was spaced 200 m apart. A total of

1.2 ha were surveyed by the vegetation sampling. The DBH and height (estimated visually in meters) were taken for all trees and lianas within each transect strip. Tree and liana species were identified using field guides and local informants (Raponda and

Sillans, 1995; White and Abernethy, 1999). Species were only included if the DBH was greater than 10 cm. Each stem of multi-stemmed trees was measured and the average taken. If a tree had buttressing at breast height, the measurement was taken immediately above the buttress. Any dead trees or lianas were not included in the survey.

5.6 Data Analysis

The problem of data dependence is frequently discussed in positional behavior studies (Dagasto, 1994; McGraw, 1998a, 1998b). Independence of data points is not an issue for this study. I used group scans and every attempt was made not to scan the same individual twice during group scans. McGraw (1996a) suggests that a minimum of

15 minutes between re-sampling an individual is sufficient to maintain independence in positional behavior studies.

267

Data were imported from Excel into SPSS and analyzed for descriptive statistics.

Significance tests (p 0.05) were performed on raw data. This leads to a 5% chance of

Type I errors (or erroneously≤ rejecting the null hypothesis).

Data were organized into R x C contingency tables and Fisher Exact test was used

to determine independence among categories and variables. The Fisher Exact test

calculates whether the probability of getting an outcome equal to or more extreme than

the one observed is due to chance (McKillup, 2005). Therefore, if the test is significant,

the null hypothesis that the numbers are due to chance alone can be rejected. The

Fisher Exact test is suitable for small sample sizes, and there are no value restrictions for each cell (Lawal, 2003; McKillup, 2005).

5.7 Results

Habitat profiles

The Sentier Nature forest contains three habitat types (as defined in Chapter

2)—mangrove forest, terra firme forest, and coastal palm forest. However, the distribution and number of tree species in both the mangrove and terra firme forests are similar and, as shown in the locomotor results section, there are no significant

differences in locomotion between the two forest types. Therefore, two gross habitat

types were distinguished for this locomotor behavior study—beach forest and terra

firme forest (which includes the smaller mangrove forest). The terra firme forest covers

148 hectares compared to only 100 hectares of beach forest (Figure 5.7). The average

number of trees in each transect are presented for the forest types (Table 5.1).

268

Structurally, more arboreal or above ground substrates (such as lianas and treefalls) are available in the terra firme forest type (pers. obs). The average DBH is highest in the terra firme forest and both the beach and terra firme forests are significantly different in

average DBH (Kruskal Wallis test; p=<0.001). According to Cannon and Leighton

(1994:507), “The size of trees… is also a strong indicator of the stature and maturity of a

piece of forest. This data is readily available and can demonstrate selection for a

particular forest type.” In general, trees with a larger DBH are older and have more and

larger substrates available.

Based on the phenology study trees, the average tree height is highest in the

terra firme forest (26.73 m) (Table 5.2). The density of substrates (measured as the

number of trees and lianas per 100 meters) is also highest in the terra firme forest.

These trees have multiple substrates (branches and twigs) and are more closely spaced

than the open beach habitat. The canopy is also more closed than the other habitat

type (pers. obs).

The beach forest is the most distinct habitat type because of its uniformity and

lack of lianas. The average tree height for the beach habitat (24 m) is not much

different than the terra firme habitat average tree height (Table 5.2). However, the

trees along the coast are structurally different. Most of the trees are large and single

trunked with only a few palm fronds that begin at a height of approximately 20 meters.

These fronds often do not provide adequate support, and therefore, arboreal travel is

mostly restricted to climbing or descending the tree trunk or leaping from the interior of

269

the palm frond canopy to other vertical trunks. There is undergrowth, but this consists

mostly of Chrysobalanus icacao and Iboga tabernathe bushes that reach about a meter

in height and cannot support a mangabey’s weight.

Locomotor Behaviors

For each locomotor category, the overall results are presented as frequencies, or

percent of total scans engaged in each locomotor behavior. Within each category

(activity, height, forest zone, support type, and habitat), the results are divided into sex

and age class. If significant locomotor differences were found between sex and age

classes with the Fisher Exact test, the results are presented for each category. If no significant differences were found between sex and age classes, they are lumped for the remainder of the analyses. For each category, the percentage of time engaged in each locomotor behavior within that category is presented. The categories of descend head- first and descend rear-first are similar movements so they were combined into the category “descend” to aid in statistical analysis. The category “other” includes rarely observed movements including arm swinging and bipedal walking.

Locomotor behaviors for all age and sex categories combined

Table 5.2 shows the overall frequencies of locomotion for all age and sex classes combined. As predicted, quadrupedalism was the most frequent type of locomotion

(81.8%). The frequency of quadrupedal run in C. torquatus (15.9%) was higher than frequencies observed in C. atys (McGraw, 1996a; McGraw, 1998a). At Taï, C. atys were only observed running in 5.7% of scans. It is possible that the occurrence of

270

quadrupedal run may be artificially high in Sette Cama because of the level of habituation of the C. torquatus group members. When startled, or if we got too close to

the group, the usual reaction of C. torquatus was to flee (both on the ground and into

the trees).

It was predicted that climbing would be the most important locomotor mode

after quadrupedalism, but C. torquatus used leaping (6.7%) more often than climbing

(5.7%) and descending (5.4%). The other types of locomotion such as arm suspension or

bipedalism were seen very rarely (0.5% of scanned individuals). The combined

frequencies of these locomotor types account for around 19% of overall locomotion.

Locomotor behaviors by age and sex category

The total number of individuals scanned of each age and sex category is presented in Table 5.3. Juveniles and subadults were the most frequently scanned type of individual. It is possible individuals were erroneously classed as subadults (for example an adult female may be confused for a subadult male based on size alone).

Furthermore, subadults and juveniles make up a larger percentage of the group than

adult individuals. This may account for the discrepancy in observations. Adult males

and adult females were scanned the least often.

The frequencies of locomotor behaviors for each sex and age category are

presented in Table 5.4. The Fisher Exact test reveals significant differences in locomotor

behaviors among all age categories, but there are no differences in locomotor behaviors

between male and female adults. These results indicate that despite being sexually

271 dimorphic, male and female adults are moving in generally similar ways. Adults also may be more limited in movements compared to other ages. For example, adults use quadrupedalism more frequently than both subadults and juveniles. Adults also climb and leap less than juveniles and subadults.

Quadrupedal walking was the most common type of locomotion in all categories followed by quadrupedal running. Even at younger ages, individuals are dependent upon quadrupedalism as their primary mode of locomotion. Juvenile locomotor frequencies are the most divergent from other age and sex categories. Juveniles used leaping (9.1%), climbing (10.3%), descending (7.3%), and other forms of locomotion

(0.9%) more often than any other age category of C. torquatus (Table 5.4). This supports the prediction that juveniles have to leap more due to discontinuities in the forest canopy related to their shorter body lengths. They also are more apt to explore their environments using locomotor behaviors other than quadrupedalism. Juveniles were often seen climbing and descending lianas (pers. obs).

The use of leaping, climbing, and descending declined in C. torquatus with age.

The frequencies of non-quadrupedal locomotion were highest among juveniles followed by subadults and the lowest among adults. There were no significant differences in adult positional behaviors. However, some qualitative trends in positional behaviors were apparent. Adult males used leaping more often than adult females. Adult females were never observed leaping during the observation period. Many females in the

Sentier Nature group were pregnant or carrying infants which may have limited their

272

movements (pers. obs). On one occasion, multiple group members leaped from one

tree to another whereas a female with an infant “chose” to descend down the tree

trunk rather than leap. Adult males were only seen leaping in 3.8% of the scans. The

high frequency of leaping (19.6%) in unknown individuals is an observational artifact. In

general, leaping does not appear to be an important positional behavior among adult

Cercocebus species. C. atys from Taï were only observed leaping around 1% of the time

(McGraw, 1996a), and leaping was infrequent among adult C. torquatus (3.8%).

Climbing was observed most often in juveniles (10.3%) followed by subadults

(4.7%). The larger instances of climbing in juveniles may be attributed to their use of thin, vertical lianas that are abundant in the terra firme habitat. Subadults and adults used smaller substrates less often than juveniles (see below). When the categories of climb and descend are combined, the frequencies are similar for adult females (6.7%) and adult males (6.4%).

In general, C. torquatus are more arboreal than C. atys at Taï. Yet, C. atys were observed climbing twice as often as C. torquatus adults (McGraw, 1996a)13. The

habituation level of the C. torquatus group probably impacted not only forest strata use

and the frequency of quadrupedal running, but also how the group members were

observed. More probably, the most obvious individuals, who were already in the trees,

were chosen at the start of a scan sample and this created a bias in observations toward

13 McGraw (1996a) combined both ascending and descending movements into the single category of “climb.” When comparing this C. torquatus population to C. atys, I combined “descend” and “climb” to approximate McGraw’s definition of this positional behavior.

273

arboreal group members. Additionally, it was predicted that climbing might be

important for foraging and feeding in the Cercocebus genus (Fleagle and McGraw, 1999,

2002). I only observed feeding/foraging in .4% of the scans. This definitely led to an

underestimation of the importance of climbing during C. torquatus foraging or feeding.

Locomotor behaviors of all categories by maintenance activity

Table 5.5 presents the frequency of locomotor categories by maintenance

activity. C. torquatus was only observed feeding or foraging four times during locomotion. I also did not designate movements from one feeding site to another during foraging or movement within a fruiting tree as “feed” but instead as “travel”.

This definitely lends to a gross underestimate of the amount of time spent feeding and searching for food among C. torquatus in Sentier Nature that can be related to visibility issues and lack of full habituation.

Furthermore, it is probable that many movements categorized as “travel” were in fact feeding or foraging. Cercocebus tends to eat while in motion (McGraw, 1996a).

McGraw often observed C. atys picking up foods from the ground or eating foods stored

in their cheek pouches while traveling. Indeed, around 60% of the C. atys diet is found

on the forest floor (McGraw et al., 2011).

C. torquatus used quadrupedal walking most frequently during traveling,

feeding, and foraging. Among C. atys at Taï, quadrupedal walking was also the most

common locomotor behavior during both traveling and foraging (McGraw, 1996a,

1998a). Climbing made up 1/3 of overall C. torquatus scans. Climbing and descending

274

were observed in 11.1% of the traveling scans. Both of these estimates are higher than

those observed in C. atys. The observations of quadrupedal running in C. torquatus during social behavior can be attributed to juveniles that often chased each other (and gave loud screeches).

Since the activity scans were so biased towards travel, no significance values were computed for this category, and it was not broken down by age and sex category.

Unfortunately, these data cannot reveal any real locomotor trends based on activity.

Locomotor behaviors of all categories combined by height

Table 5.6 shows the average frequency of scans that individuals were observed at different forest heights as calculated in chapter 2. C. torquatus was most often observed in locomotion on the ground (39.4% of scans) followed by the understory (1-5 meters; 30.08%). C. torquatus was found in the trees (6-30 meters) for 30.48% of scans.

C. torquatus was never observed at the highest canopy level (31+ meters). The mean tree height in Sentier Nature is 25.5 meters (Table 5.1).

Data on strata use by C. atys at Taï (McGraw, 1996a, 1998a) indicates they preferred the lower heights (ground, understory, and shrub layer). This study suggests that C. torquatus is more arboreal than C. atys. The lack of full habituation of the group may have impacted the height use of C. torquatus. When startled, C. torquatus tend to flee, both on the ground and in the trees. However, in general, C. torquatus were more frugivorous than C. atys (McGraw et al., 2011). This feeding preference suggests that C. torquatus should exploit the arboreal habitat more often than C. atys.

275

Table 5.7 presents C. torquatus locomotor behaviors by height class. For these analyses, the quadrupedal walk and quadrupedal run categories were combined into a single category of quadrupedalism due to the limitations of the Fisher Exact test.

Quadrupedalism was the most common type of movement at all height categories.

Even at the greatest heights used by C. torquatus (21-30 meters), quadrupedalism remained the dominant form of locomotion. Leaping, climbing, and descending were most often observed at the 6-10 meter level compared to the other heights. This may be an effect of the lianas and small trees found at this height. C. torquatus also often traveled through brambles and tree roots which provided discontinuous supports that require other types of locomotion besides quadrupedalism (Figure 5.19). McGraw noted the tendency for C. atys to forage terrestrially for food and then climb up a few meters to sit in the small saplings of the understory (1996a).

There are some differences in the locomotor behaviors used at different heights among the age classes (Table 5.8). Adult locomotion was significantly different from that of juveniles on the ground, understory, and lowest canopy level. This was most likely due to the higher frequency of quadrupedalism in adults compared to juveniles.

Adult and subadult locomotion were not significantly different within the height categories. Subadults and juveniles differed in their locomotor behaviors on the ground and in the understory. Subadults were more quadrupedal than younger individuals.

276

Locomotor behaviors of adults by height

Adults were observed most frequently (54.5%) on the ground (Table 5.9). There

was a significant difference in locomotor behaviors used by height among adult C.

torquatus (Table 5.9, p=0.002). Quadrupedalism was the most dominant form of locomotion at all height levels, but it was used most frequently on the ground.

Locomotion is expected to be more varied in arboreal contexts. There were significant

differences in locomotor behaviors on the ground compared to the other height classes

(Table 5.9). This can be attributed to the use of other types of locomotion (climbing,

descending, etc.) in the trees.

Locomotion was much more varied from 6 -10 m (higher frequencies of leaping,

climbing, and descending) than any other height class despite the lack of a significant

difference of locomotor behaviors between most heights. Fruits (such as Cola carcifolia,

Landolphia sp) were often found on small trees or lianas of this height. If C. torquatus was foraging (rather than my presumption that they were traveling) at these heights, it may account for the locomotor diversity. There also was a significant difference in locomotion on the ground and in the understory compared to all other heights

(p=0.005). Adults are perhaps more limited by the lack of suitable substrates on the lowest forest levels, and therefore, they primarily move quadrupedally at these heights and stick to the forest floor.

277

Locomotor behaviors of juveniles by height

The locomotor behaviors at each height class for juveniles are shown in Table

5.10. Juveniles were most often observed from 1-5 meters (37.6%) followed by on the ground (34.5%). The frequency of observations at each height for juveniles was similar to that obtained for the other age groups; however, juveniles were seen at 6 – 10 meters more often than subadults and adults. It was possible that because of their small size, juveniles can move on lianas and small trees more easily than other age groups. Leaping, climbing, and descending were also observed most often within the heights of 6-10 meters compared to the other age categories. These types of locomotion aid movement on discontinuous supports.

Locomotion did not differ significantly between height classes (Table 5.10).

Quadrupedalism was most common at all heights except within 6-10 meters. The frequency of leaping at the 11-20 meter height class was higher for juveniles than adults. The smaller body length of juveniles may account for their higher frequency of leaping than adults higher up in the forest canopy. Leaping is the only way juveniles can cross these relatively larger gaps.

Locomotor behaviors of subadults by height

Locomotion at each height is presented in table 5.11. As in the other age groups, quadrupedal locomotion was the dominant form of locomotion at every height.

Subadults were most often seen (80% of scans) within the lowest height classes (0-5 meters). Subadults were more similar to adults in their use of different heights than

278

they were to juveniles. Subadults also used leaping and climbing less often than

juveniles. C. torquatus subadult locomotion did not differ significantly among height

categories despite the predominance of quadrupedalism within every height category.

Locomotor behaviors of all categories by tree zone

C. torquatus was most frequently observed on the ground (Zone 0) followed by the areas peripheral to trees (Zone 5) such as lianas and fallen tree trunks (Table 5.12;

Figure 5.14). The next most commonly used tree zone were the terminal branches

(Zone 3). C. torquatus were never observed in the emergent layer of the canopy (Zone

4). However, lack of visibility in Sette Cama cannot be ruled out as a factor for underestimation of the use of this zone. C. atys at Taï was also never observed at the uppermost layer of the tree canopy (McGraw, 1996a).

Quadrupedal walking was the most common type of locomotion in all zones except Zone 1, consisting of tree trunks (Table 5.13). C. torquatus were climbing and descending on vertical tree trunks often during travel and foraging. For example, C. torquatus would vertically climb the trunks of H. guineensis trees to access the palm fruits (per. obs). These behaviors were expected because C. torquatus has scapular, pelvic and lower limb anatomies similar to other climbing species (Fleagle and McGraw,

1999, 2002; also see Prediction 1). These features suggested that rather than leaping from tree to tree (as seen in classically arboreal primates), C. torquatus would ascend and descend tree trunks and walk terrestrially to the next substrate.

279

In Zone 5, the forest understory (or in many cases the roots of trees in swampy

areas), C. torquatus used quadrupedalism most frequently, but they also used all other types of movements. This can be associated with the architecture of this zone. Indeed

McGraw (1996a:260) notes:

The forest understory is dominated by discontinuous, vertical supports which generally preclude high frequencies of quadrupedalism. Primates moving through this forest layer are most often required either to leap from one vertical support to another or to climb between supports. Leaping was most common in the middle canopy (Zones 2 and 3) but a higher

frequency of leaping was observed in the outer middle canopy (Zone 3) than the inner

middle canopy (Zone 2). Substrates in Zone 3 are less stable and more discontinuous

(McGraw, 1996a). I would classify C. torquatus as “hesitant leapers.” When jumping from tree to tree, most C. torquatus appeared to drop rather than leap. C. torquatus

tend to be clumsy when leaping, and they clamber for the terminal branches on the end

of the landing tree.

Locomotor behaviors of adults by tree zone

Adults were most frequently observed on the ground (Zone 0, 54.5%) followed

by the area of undergrowth and lianas (Zone 5, 23.5%) (Table 5.14). Locomotion is

significantly different in all forest zones except between zones 0 and 2, zones 2 and 3,

and zones 2 and 5 (Table 5.14). Quadrupedalism was the most common type of

locomotion in all zones but climbing was highest in zone 1 (tree trunk), as expected.

Adult C. torquatus also used leaping and descending at this level most frequently.

280

Locomotor behaviors of juveniles by tree zone

Juveniles were most frequently observed in Zone 5, or the undergrowth that features lianas and small branches (Table 5.15). It was predicted that juveniles would use the outer canopy where smaller supports are found more frequently than other age groups. The smaller body size of juveniles would allow them to use the terminal branches. Nevertheless, juveniles and adults were observed in the outer canopy zone in similar proportions. Juveniles also used quadrupedalism less frequently than the other age groups. Juveniles were rarely seen climbing large vertical supports as suggested by the average DBH of these forests.

Locomotion is dependent on forest zone in all of the cross-comparisons except in

Zones 2 and 5 (Table 5.15). The similarity in locomotion between Zones 2 and 5 may be due to the similar frequencies of quadrupedalism and climbing by juveniles at these levels. There also were a higher number of juveniles observed in Zone 5 with each scan compared to Zone 2 (differences due to sampling error).

Locomotor behaviors of subadults by tree zone

The tree zones (1, 2, 3) were combined for the overall analysis due to the limitations of the Fisher exact test (Table 5.16). Subadults were observed in the tree zones during 18% of scans. However, the majority of subadult locomotion occurred on the ground (47.6%) or in the forest understory (34.4%). Juveniles spent more time in the trees than both adults and subadults. Table 5.16 presents the results of the Fisher exact test for locomotion and forest zone for subadults. Locomotion is significantly

281 different in all zones except 1 and 2. In these zones, subadults were never observed using quadrupedal locomotion. The differences among other zones are related to the higher frequencies of quadrupedalism on the ground compared to other forest zones.

Locomotor behaviors of all categories by support type

Table 5.17 shows the frequencies of C. torquatus locomotion on each support type. They were most often on the ground (45.5%) followed by medium sized supports

(41.5%). C. torquatus used branches more frequently than twigs. Most medium to large sized primates cannot use twigs during locomotion because twigs are thin and unstable and unlikely to be able to support an individual for more than a few moments. Large supports such as fallen trees or vertical tree trunks were used the least (2.7% of scans).

The scan samples in this study were biased toward the terra firme forest. Therefore, the frequency of large support use may have been underestimated among this population of C. torquatus as most of the supports in the coastal forest are large tree trunks (see chapter 2).

Quadrupedalism was the most common type of locomotion on all support types except for boughs (Table 5.18). For this analysis, I combined fallen trees, large supports, and vertical trunks into the category of “bough.” However, if tree trunks

(including vertical and diagonal trunks) are separated from other large supports, C. torquatus locomotion on trunks was primarily by descend (68.2%; Table 5.19). The category of descend was lumped together to include both head-first and rear-first descend.

282

Leaping was most commonly observed from the terminal branches of the trees

(23% of scans; Table 5.18). C. torquatus would often walk to the terminal branches of the tree for take-off and then touchdown on the destination tree’s terminal branches

(pers. obs). The individual usually grabbed multiple branches to add stability to the take-off and landing. In general, though, C. torquatus were clumsy leapers, and they made a lot of noise crashing from one tree to the next.

Locomotor behaviors in adults by support type

Quadrupedal walking was the most common type of locomotion on all support types among adults (Table 5.20). All of the major locomotor types were used on branches. This suggests that medium-sized substrates allow for more varied locomotion than any other substrate. As expected, C. torquatus used climb and descend on boughs

(which for this analysis included tree trunks) at the greatest frequencies. However, boughs were the least used support type. Support use is not independent of locomotion among adults (Table 5.20).

Locomotor behaviors in juveniles by support type

Quadrupedal locomotion was the most common movement on all support types except on boughs (Table 5.21). Juveniles used descending locomotion more often on boughs than any other substrate. Therefore, contrary to predictions based on DBH and overall body size and proportions, juveniles were able to negotiate larger supports. This suggests that descending on large supports begins early in life and continues as a major form of locomotion throughout the lifespan. Juveniles were also observed climbing to

283 the top of Hyphanae guineensis trees to acquire palm fruits but these movements were not seen during the sampling period (pers. obs).

As predicted, juveniles used smaller supports more frequently (18.8%) than adults (5.1%) and subadults (7.6%). The smaller body size of juveniles allowed them to use lianas and sections of the forest undergrowth that couldn’t support larger individuals. Juveniles were also the least terrestrial of all age categories which may be related to the higher availability of smaller substrates for their use in travel. All of the

Fisher exact comparisons were significant for support size and locomotion (Table 5.21).

Locomotor behaviors in subadults by support type

The overall differences among support types in subadults were not calculated because of the limitations of the Fisher Exact test. The support type comparisons are presented in Table 5.22. Subadult support use is more similar to that of adults than of juveniles; subadults have more body mass than juveniles and, therefore, are more limited in their substrate choices. Locomotion is significantly different on all support types except when comparing twigs and branches (Table 5.20). Locomotor types are more limited on boughs and the ground.

Locomotor behaviors by habitat

The percentage of scans in each habitat type are presented in Table 5.23. During data collection, I distinguished 3 habitat types: mangrove, terra firme, and beach.

There are no significant differences in locomotion in each forest type (p=.450) nor when the mangrove and terra firme habitats are combined and compared to the beach

284

habitat (p=.345). Therefore, it is justified to combine the mangrove and terra firme

habitats into a single habitat type. Each table, however, presents a breakdown of

locomotion in each of the three forest categories for comparison.

The majority of scans (92%) were in the combined terra firme and mangrove

habitat. C. torquatus was observed the least in the beach forest (8% of scans). This is not unexpected because the beach forest is mostly palm trees and scrub bushes.

However, the time spent in this habitat type by C. torquatus may be underestimated. It was difficult to track the mangabeys during elephant season (March – September).

Elephants prefer coastal forests during these warmer months (Morgan and Lee, 2007), and they are difficult to spot in the dense scrub that characterizes parts of the coastal forest. The lack of trails and visibility made it dangerous to perform all day follows on the mangabeys during these months. Therefore, on multiple occasions, we had to leave the mangabey group when we discovered signs of an elephant nearby.

Also, C. torquatus differs in its use of the beach habitat seasonally, and this study only represents a subset of the annual ranging and feeding cycle. For example, C. torquatus was frequently observed along the beach feeding on Manilkara fruits during the habituation period in January and February 2009. Nevertheless, these results can be used as an estimate of locomotor differences between habitat types.

Quadrupedalism was the most common type of locomotion in all habitat types

(Table 5.24). Overall locomotion in each habitat type fits the predictions with the exception of the frequency of leaping. C. torquatus of all ages used leaping, climbing,

285

and descending more frequently in the beach habitat than in the other habitat types.

The overall frequencies of climbing (8%) and descending (14.8%) were highest in the

beach habitat. The high frequency of leaping (17%) in the beach habitat is surprising

given the structure of the beach habitat. The beach habitat features fewer trees that

are spaced farther apart than the other forest type. I expected that C. torquatus would use terrestrial quadrupedalism and use climbing and descending to get up and down the palm trees.

Locomotion in juveniles by habitat type

Table 5.25 shows a summary of the locomotor observations for juveniles in each habitat type. Quadrupedalism is the most common type of locomotion in all habitats, as seen in the other age classes. As predicted for overall habitat use, there is no significant difference in locomotion in the mangrove and terra firme forests, but the beach forest differs from the other forest types. Juveniles are the only age class that had significant differences in locomotion by habitat type. The frequencies of leaping, climbing, and descending are highest in the beach habitat. Because of their smaller body sizes, juveniles have to climb and descend trees rather than leaping because the distance may be too far for juveniles to cross. Trees in the beach habitat are fewer and farther apart.

Locomotion in subadults by habitat type

Subadult locomotion follows the same patterns as both adults and juveniles

(Table 5.26). Quadrupedalism is the most common type of locomotion in all habitats.

Subadults were observed the least in the beach habitat but used leaping, climbing, and

286

descending most often in the beach habitat. There are no significant differences in

locomotion by habitat type (Fisher exact value=15.839, p=0.083).

5.8 Discussion

C. torquatus are predominantly quadrupedal animals (81.8% of scans). The next

most common type of locomotion observed was leaping (6.7%) followed by climbing

(5.7%) and descending (5.4%). Over 80% of traveling and 66.7% of feeding were associated with quadrupedal locomotion. Climbing (33.3%) also occurred during feeding. The use of climbing among C. torquatus corresponds with the morphological predictions that it is an important means of locomotion among this species. C. torquatus used climbing to access the trees and also while in the trees. This enabled individuals to move within the tree canopy to find new food sources or obtain foods on higher branches.

C. torquatus were on the ground for 45.5% of the scans. Quadrupedalism was the most common type of locomotion at all forest heights. The frequency of quadrupedal locomotion was lowest at the lower canopy level (6-10 meters, 39.7%), and it was at this level that the frequencies of all other types of locomotion were the highest. Leaping occurred most frequently in the lower (6-10 meters, 22.9%) and middle canopy heights (11-20 meters, 18.6%). Climbing was observed in all forest heights except the uppermost canopy layer, but it was most frequent in the lower canopy (15.7%). Descending was most frequently observed in the lower canopy (21.7%) followed by the upper canopy heights (13.6%).

287

C. torquatus showed differences in locomotion in the different zones of the

arboreal habitat, but they maintained an overall reliance on quadrupedal locomotion.

C. torquatus used descending (68.2%) and climbing (22.7%) while moving down and up vertical and diagonal tree trunks. C. torquatus was most frequently observed on the ground (45.5% of scans), but they also used other support types of all sizes. C. torquatus prefers branches (41.5%) over twigs (10.3%) and boughs (2.7%).

Overall locomotion of C. torquatus compared to C. atys

Figure 5.20 shows the locomotor profile of C. torquatus compared to C. atys from Taï, the only other Cercocebus species for which positional behavior data are available. First, I compare the data for all age and sex classes of C. torquatus combined for overall locomotion, and then I separate the C. torquatus adults and compare these results to the Taï results. Because there were significant differences in adult and non- adult locomotion among C. torquatus, I use only adults in the comparisons of locomotion by height and support use to C. atys. These are presented within each section.

C. torquatus and C. atys used different amounts of each locomotor behavior.

Both species used quadrupedalism most frequently, but C. torquatus was observed using quadrupedal running more often than C. atys. This is very likely an artifact of the habituation level of this study population. C. torquatus was also leaping far more often than C. atys. This trend persists even when only the adults are compared (Figure 5.21).

288

C. torquatus juveniles were observed leaping in the highest frequencies, and this added to the increased frequency of occurrences.

The magnitude of difference in locomotor behaviors becomes smaller when comparing C. torquatus adults with C. atys, but there are still noticeable differences in frequencies (Figure 5.21). C. torquatus was more quadrupedal than C. atys, and C. torquatus also used leaping more often. There were differences in the frequencies of climbing between both species. The fewer instances of climbing among C. torquatus adults is surprising given the structure of the beach habitat and the higher level of arboreality of the C. torquatus group. There may have been a sampling bias towards arboreal individuals. Individuals in the trees tended to make more noise, and therefore, they may have been chosen to begin the group scan samples. This would explain the lower frequencies of climbing observed in C. torquatus compared to C. atys.

As noted earlier, many factors such as diet and foraging strategy influence a species’ positional behaviors. The subtle variations in positional behaviors and habitat use between these two species are probably related to dietary preferences and the location of preferred food resources. For example, C. torquatus of all ages were observed leaping at higher frequencies than C. atys, and C. torquatus were found in arboreal contexts more frequently. This may relate to the higher component of fruit in the C. torquatus diet compared to C. atys (see also chapter 3). At least 60% of the C. atys diet is composed of seeds (McGraw et al., 2011). The majority of the seeds eaten by C. atys are Sacoglottis gabonensis seeds located on the forest floor. Ripe fruits

289

located in the tree canopy account for less than 10% of the C. atys diet. During this five

month study period, the C. torquatus diet was comprised of 54% seeds and 38% fruits.

Since C. torquatus are more frugivorous, they spend more time in an arboreal context than C. atys.

C. atys travel (80.4%) and forage (65.7%) most often on the forest floor; however, feeding routinely occurs on supports above or on the forest floor such as small trees or tree falls (McGraw, 1996a; McGraw, 2007). It is expected that when more positional behavior data for feeding and foraging in C. torquatus become available, it will indicate that they forage less frequently than C. atys on the forest floor. C. torquatus spend a large amount of time foraging and feeding in fruit trees such as

Manilkara and Dialium when they are in season (pers. obs). Nevertheless, C. torquatus were observed foraging for old Sacoglottis gabonensis seeds, larvae, fungi, and fruits on the forest floor.

Ontogeny of locomotor behaviors

There are significant differences in locomotor behaviors and support use across age classes in C. torquatus. Juveniles used non-quadrupedal locomotion far more frequently than adults and subadults. Juveniles also were observed more often in Zone

5, the area with small trees and lianas, and juveniles were observed on twigs more often than other age groups. The small size of juveniles allows them to travel on these smaller substrates. Juveniles were the least terrestrial group of C. torquatus. Juveniles were also observed using locomotor behaviors not seen in other groups such as arm suspend.

290

Subadults were similar to adults in the frequency that they used descend but

subadults used leap and climb slightly more often. Subadult locomotion is more like adult locomotion than that of juveniles, a trend observed in New World monkeys

(Bezanson, 2006). Smaller body size and proportions may make certain substrates or locomotor behaviors available or unavailable to juveniles, but it appears that size is not

the only variable in producing a locomotor behavior. If this were the case, there would

have been significant differences in locomotion between male and female adults. There

are multiple factors that determine primate locomotor behaviors (such as morphology, body size, predation risk, body proportions, etc.) (McGraw, 1996a). The appearance of locomotor behaviors in juveniles not seen in other groups may be a part of growing up and learning how to negotiate one’s environment. Once a primate reaches a certain age, their locomotor versatility dwindles and the adult pattern of locomotion emerges.

Height class and Locomotion

Based on qualitative observations from other studies in Cameroon (Astaras et al.,

2011; Mitani, 1989), C. torquatus appears to exhibit site specific diversity in height preference. An exact comparison among sites is difficult because the forest structures and available substrates were not quantified. Each habitat has difference resources, habitat structure, and forest architecture for C. torquatus to negotiate. Keeping in mind these disparities, there are several other factors that may influence height use and preference in different populations of the same species.

291

The differences between terrestrial and arboreal substrate use at each site may

be attributed to the location of favored resources and food competition. In describing

the movements of C. torquatus in Campo, Cameroon Mitani writes, “Mangabeys were

found to occur widely from the forest floor to a height of 40 m” (1989:314). They most

frequently used the ground for travel and social activities, but feeding was most

common at around 30 meters. C. torquatus from Sette Cama were observed very rarely

at the higher layers of the canopy (21-30 meters, 8.64%) and never in the emergent

layer (31+ meters). C. torquatus was seen most frequently at the lowest forest levels (0-

5 meters). The C. torquatus population in Campo ate fewer seeds and did not exploit as many terrestrial food items as C. torquatus in Sette Cama which may explain the differences in forest use.

In Korup National Park, Cameroon, C. torquatus was frequently observed in association with drills (Astaras et al, 2011). Here the foraging behavior of C. torquatus was seen as “… more arboreal than [drills] and is best described as semi-terrestrial”

(Astaras et al, 2011). At this site, C. torquatus altered its strata use when in association with the primarily terrestrial drills, presumably in response to possible feeding competition from another terrestrial forager. Each C. torquatus population is adapting to its available resources and competition for those resources.

Based on the limited data available at the time, Nakatsukasa described C. torquatus as the most terrestrial Cercocebus species (1994b). However, several

Cercocebus species are more terrestrial than C. torquatus. When comparing strata use,

292

C. atys uses the ground more frequently (67.24%) than C. torquatus adults (54.5%), and

C. torquatus adults use the other strata layers or heights more frequently than C. atys

(McGraw, 1996a; Figure 5.23). Data are also available on the degree of terrestriality for several other Cercocebus species. C. galeritus spends 51% of its time on the ground

(Homewood, 1976), and C. agilis varies in its degree of terrestriality by study site

(Mondika, CAR: 22% of time; Shah, 2003; Bai Hokou, CAR: 72% of the time; Devreese,

2010). C. sanje spends at least 68% of its feeding time on the ground or below 1 meter

(Mwamende, 2009). The amount of time spent on the ground among C. torquatus at

Sette Cama is further diminished when all age classes are included in the estimate (39% of the time).

Habitat Type and Locomotion

The locomotion of C. torquatus across different habitat types was conservative.

McGraw (1996b) also found no distinct differences in locomotion among C. atys in disturbed and undisturbed forests. Quadrupedalism dominated C. torquatus locomotion in both the terra firme and beach habitats. The semi-terrestrial adaptation of C. torquatus may enable it to maintain locomotor equivalence over the variety of habitats in Sette Cama. The ability to exploit both arboreal and terrestrial substrates and resources gives this genus an adaptive edge. For example, they can walk on the ground between trees and climb up vertical tree trunks when the gap between trees is too large to leap. Cercocebus also have the ability to eat terrestrial foods (such as seeds

293 and nuts) when fruits are not readily available. This option is not available to other primate genera such as the guenons.

There were, however, significant differences in locomotion among juveniles in the beach habitat compared to those in the terra firme habitat. This may relate to the smaller body size and length of juveniles compared to subadults and adults. There were fewer available substrates overall in the beach habitat (pers. obs.) compared to the terra firme habitat. Juveniles were observed using smaller supports overall such as lianas and small bushes more often than the other age classes. Therefore, this may have impacted how juveniles moved in the more open beach habitat.

As mentioned earlier, the amount of time C. torquatus spent in the beach habitat may have been underestimated. Therefore, a year-long study may yield somewhat different results. Furthermore, if a more arboreal species were studied, such as the sympatric guenon Cercopithecus cephus, differences in positional behaviors may become more apparent. For example, C. cephus was seen walking on the ground only in the beach habitat where less arboreal substrates are available (pers. obs). C. cephus was terrestrial for 11% of the time at another site in Gabon (Gautier-Hion and Gautier,

1974), but the range of terrestriality among guenons is variable (McGraw, 2002).

Interestingly, a comparison of two similarly sized guenon species of the cephus superspecies showed different locomotor profiles between Taï and Kibale National Parks

(McGraw, 2002). It may be shown that habitat differences more strongly impact only certain primate genera.

294

Support Use and Locomotion

C. torquatus, as with most catarrhines, did not follow the predictions of support use based on body size outlined by Fleagle and Mittermeier (1980). It was expected that larger individuals (adult males) would use the largest supports most frequently whereas smaller individuals (juveniles, subadults, and females) would use smaller substrates more often. Keeping in mind the overall differences in locomotion among age and sex classes, some differences do, however, appear between juvenile and subadult/adult support use. Juveniles were observed on twigs (18.8%) more often than both subadults (7.6%) and adults (5.1%). Juveniles were also observed on boughs (4.2%) more than another other group. Juveniles used quadrupedalism less frequently than the other groups on most supports. It may be that a combination of smaller body size, smaller body proportions, and locomotor inexperience contributes to the differences in juvenile locomotion and support use compared to subadults and adults. For example, juveniles were often observed clumsily climbing small lianas whereas adults were never observed in this behavior.

Although terrestrial substrates were the most common support for all ages and sexes combined (45.5% of scans), C. torquatus prefers branches (41.5%) in above ground contexts. Boughs were the least used substrate (2.7%). The frequency of leaping was

highest on small supports (23%). C. torquatus would hesitantly leap from the terminal

branches of one tree to another. Quadrupedalism was the most common type of

locomotion on all support sizes except for boughs. Descending was most often

295

observed on the largest substrates. Cercocebus are capable of negotiating large vertical

supports, as suggested by their morphologies, however, they appear to prefer terrestrial

substrates.

McGraw (1998a) also noted a preference for terrestrial substrates over all other

substrates in C. atys. However, different activities yielded differences in support use

among C. atys. For example, “When feeding in the trees, the mangabey, despite its size,

prefers branches and even twigs over boughs” (McGraw, 1998b:240). I expect that as

more feeding data become available for C. torquatus, the amount of branch use will

increase. Figure 5.24 compares support use in adult C. torquatus and C. atys, and there

are some distinct differences. C. torquatus uses terrestrial supports less often and arboreal supports (both branches and twigs) more frequently than C. atys. Again, this may be a reflection of dietary differences for each group and may explain the differences in overall locomotor frequencies.

As shown above, body size alone does not serve as an accurate predictor of support use. Support use and locomotor behavior is more likely a combination of multiple factors including body size, morphology, foraging strategy, predation, or polyspecific competition (McGraw, 1996a).

Lophocebus and Cercocebus

Morphological studies of Lophocebus and Cercocebus species find clear skeletal distinctions between these two groups associated with substrate preference

(Nakatsukasa 1994, 1996). C. torquatus has several features of the humerus and femur

296

related to terrestrial locomotion. Nakatsukasa (1994, 1996) considered C. torquatus the

most terrestrial of all Cercocebus species because their skeletons were the most terrestrially adapted.14 However, as shown above, the amount of time spent in an

arboreal context by C. torquatus has often been underestimated. Red-capped

mangabeys in Sette Cama spend a considerable amount of time in the trees. A

comparison of the positional behaviors of Cercocebus and Lophocebus provides valuable

insight into the differences between arboreal and semi-terrestrial locomotion. These

comparisons will help to define the difference between strictly arboreal primates and

primates that divided their time between the trees and the ground.

The only locomotor data for Lophocebus comes from Kibale National Park in

Uganda (Gebo and Chapman, 1995a). At this site, L. albigena uses quadrupedal

locomotion most frequently (46% of the time) during travel followed by climbing (31%) and leaping (21%) (Table 5.27). When comparing C. torquatus with L. albigena, C. torquatus uses leaping and climbing less frequently, as would be expected for more terrestrial animals and with their skeletal anatomies. C. torquatus relies extensively on quadrupedal movement, even when in an arboreal context.

The primary distinction between semi-terrestrial and arboreal locomotion is the amount of time spent in arboreal substrates. However, as shown by the different species of Cercocebus, even members within a semi-terrestrial genus vary in their

14 Data on the positional behaviors of Cercocebus species were mostly unavailable at the time of his study, and many still considered Lophocebus within the Cercocebus genus. Therefore, a comparison between albigena and torquatus would definitely suggest more terrestriality in the latter.

297 terrestriality. Semi-terrestrial locomotion appears highly dependent on environmental factors such as food availability (including preference and competition from sympatric primates) and predation pressure. Nevertheless, the morphological distinctions between Cercocebus and Lophocebus identified by Nakatsukasa (1994, 1996) translated to different frequencies in quadrupedalism, leaping, and climbing.

5.9 Future Directions

Studies of the morphology and positional behavior of members of the

Cercocebus-Mandrillus clade offers the potential to understand the transition from semi-terrestrial to terrestrial locomotion in a group of sympatric primates. There is a trend towards increasing terrestriality among Cercocebus species. Biogeographical reconstructions suggest that C. torquatus is the most derived of the Cercocebus species; yet C. atys is the most terrestrial Cercocebus mangabey. Future long-term locomotor studies in other sites may paint a more detailed picture of C. torquatus locomotion, but from this study, it appears that C. torquatus is more arboreal than many of its fellow clade members. This may reflect the niche separation from when C. torquatus was widely sympatric with mandrills and drills. Because Mandrillus occupies a primarily terrestrial niche, C. torquatus would have to be more arboreal because of competitive exclusion. The ecological flexibility of Cercocebus species enables them to adapt in the presence of competiting species.

It would be informative to study the positional behaviors of C. torquatus in sites such as Korup National Park, Cameroon where C. torquatus is sympatric with drills or in

298

Moukalaba-Doudou, Gabon where C. torquatus cohabitates with mandrills. In areas

where these species are sympatric, C. torquatus should be spending even more time in

the trees than observed in this study.

Another step towards elucidating the morphological trends within this clade is to

compare skeletal morphologies of Cercocebus species. For example: are there

morphological disparities between C. torquatus and C. atys and other Cercocebus

species? How do these species compare to mandrills and drills? Are their behavioral

differences morphological or purely environmental?

A preliminary qualitative investigation comparing the morphology of C.

torquatus and C. atys scapulae suggest that red-capped mangabeys are more morphologically adapted for terrestriality than sooty mangabeys. For example, sooty mangabeys feature a more superiorly inclined supraspinous fossa (Figure 5.24). This is associated with above the head arm movements during arboreal locomotion. Further investigation of features associated with terrestrial or arboreal locomotion (such as curvature of the scapular spine, humeral head width, degree of greater and lesser tuberosity extension) will reveal the extent of morphological differences among

Cercocebus species. The morphologies of Cercocebus species may reveal a clinal

distribution of traits related to terrestrial locomotion, similar to the clinal distribution of

craniomandibular traits (McGraw and Fleagle, 2006) with C. torquatus most closely

resembling Mandrillus. This would lend support to the hypothesis that these are sister

taxa.

299

The results of this positional behavior study on C. torquatus highlight some issues with extrapolating behaviors from skeletal morphology. If more long-term

studies corroborate the differences in substrate preference and positional behaviors

among Cercocebus species, the relationship between morphological form and

behavioral function among this clade is called into question. The form-function

relationship is the primary tool for reconstructing the behaviors of extinct primate taxa.

It may be that the interpretation of the form-function relationship of semi-terrestrial

species is more difficult because of their ability to exploit multiple areas of their

habitats.

As researchers continue to investigate positional behaviors among different

primates, it is becoming apparent that morphology alone cannot predict behaviors.

Primates lead complex lives that are influenced by many factors. For example, although

red colobus monkeys in the Taï Forest are morphologically committed to arboreal

locomotion, they have been observed walking on the forest floor when in association

with sooty mangabeys (McGraw and Bshary, 2002). This is just one instance of how

morphology may fail to predict the range of actual behaviors an animal can express. As

stated by Garber (2011):

Morphological design sets limits or boundaries on the range and mechanical efficiency of particular locomotor and postural patterns. For a particular species, these limits may be broad or narrow depending on phylogenetic, ontogenetic, ecological, and behavioral factors (562).

300

More positional behavior studies (combined with morphological analyses) are necessary

to fully understand the form-function complex in primate locomotion.

Finally, C. torquatus most closely resembles the earliest known representative of the Cercocebus-Mandrillus clade, Procercocebus antiquus (Gilbert, 2007). Despite the caveats introduced by this study for predicting positional behaviors from morphology for this clade, modern analogs remain a powerful tool for interpreting the behaviors of extinct species. Thus far, only cranial evidence of P. antiquus has been recognized

(Gilbert, pers. comm.), but the morphological similarities between P. antiquus and C. torquatus suggest that C. torquatus is the best approximation of how P. antiquus would have behaved. Therefore, P. antiquus may have used similar positional behaviors to C. torquatus and would have been a semi-terrestrial quadruped with adaptations for vertical climbing. Nevertheless, we need more data on the positional behaviors of other

Cercocebus species to better understand the semi-terrestrial adaptation and how it has evolved in this group of monkeys.

301

Forest Type Total # trees Average # Mean Tree Mean DBH trees/.1 ha Height (m) (cm) Beach 193 48.25 24 33.48 Terra Firme 260.5 60.72 26.73 34.6

Table 5.1: Total number of trees, average number of trees by 0.1 ha, average tree height, and mean DBH for the beach and terra firme habitat types.

Locomotor Behavior Total Individual Frequency Records Quadrupedal Walk 723 65.9 Quadrupedal Run 174 15.9 Leap 73 6.7 Climb 63 5.7 Descend 59 5.4 Other 5 0.5 Total 1097 100.00

Table 5.2: The number of scans for each locomotor behavior for all age and sex classes combined and the overall percentage of scans.

302

Age/Sex Class Total Individual Frequency Records Adult Male 157 14.3 Adult Female 120 10.9 Juvenile 330 30.1 Subadult 444 40.5 Unknown 46 4.2

Table 5.3: The total number of individuals scanned of each age and sex category. These numbers represent the total of each category from the entirety of scans. The frequency of each age and sex category is also presented.

Locomotor Behavior

% Total Age/Sex QW QR LP CL D OT Obs N Adult Males 77.7 11.5 3.8 1.9 4.5 0.6 14.3 157 Adult Females 87.5 5.8 0 2.5 4.2 0 10.9 120 Juvenile 52.1 20.3 9.1 10.3 7.3 0.9 30.1 330 Subadult 68 16 6.3 4.7 4.7 0.2 40.5 444 Unknown 47.8 23.9 19.6 4.3 4.3 0 4.2 46

Table 5.4: The frequency of each type of locomotion for each sex and age class and the total percent of locomotion observations by sex and age class. Each category is compared using the Fisher Exact test (p=0.05). The comparisons that are significant are in bold. Male x Female (Exact value=8.683, p=0.091), Juvenile x Subadult (Exact value=23.708, p=0.000), Adult x Juvenile (Exact value=65.483, p=0.000), Adult x Subadult (Exact value=20.751, p=0.001).

303

Locomotor Behavior

Activity QW QR LP CL D OT % Obs N Travel 66.1 15.6 6.7 5.7 5.4 0.5 99.3 1089 Feed 66.7 0 0 33.3 0 0 0.3 3 Forage 100 0 0 0 0 0 0.1 1 Social 0 100 0 0 0 0 0.4 4

Table 5.5: Overall locomotor frequencies by activity and total percent of each activity observed during locomotion.

Height (m) Average Frequency of Scans 0 39.4 1 - 5 30.08 6 – 10 10.4 11 – 20 11.44 21 – 30 8.64 31+ 0

Table 5.6: The average frequency of scans of individuals observed at each height for all scans combined.

304

Locomotor Behavior

Height QD LP CL D OT % Total N Obs 0 m 99.4 0.2 0 0 0.4 45.4 499 1 – 5 m 71.8 7.6 10.1 9.6 0.8 32.3 355 6 – 10 m 39.8 22.9 15.7 21.7 0 7.6 83 11-20 m 68.1 18.6 8.8 4.4 0 10.3 113 21-30 m 77.6 10.2 8.2 4.1 0 4.5 49

Table 5.7: Frequencies of locomotor behaviors at each height class in all individuals and percentage of total observations of locomotion at each height class.

Juveniles Subadults Adults Fisher's P Fisher's p Fisher's p 0 m 13.105 0.001 2.412 0.283 7.338 0.03 1 - 5 m 19.06 0.001 4.17 0.382 20.049 0 6 - 10 m 9.711 0.041 3.034 0.563 5.547 0.24 11 - 20 m 4.949 0.295 3.978 0.406 1.909 0.91 21 - 30 m 3.62 0.441 1.452 0.92 3.797 0.46

Table 5.8: Fisher’s Exact comparisons of locomotor behaviors by height between the age classes. The comparisons that are significantly different are in bold.

305

Locomotor Behavior

% Total Height QD LP CL D OT Obs N 0 m 99.3 0 0 0 0.7 54.5 151 1-5 m 83.1 4.2 2.8 9.9 0 25.6 71 6 – 10 m 58.3 8.3 16.7 16.7 0 4.3 12 11-20 m 84 4 4 8 0 9 25 21-30 m 83.3 5.6 5.6 5.6 0 6.5 18

Table 5.9: Locomotor frequencies of adults at each height class. Each category is compared using the Fisher Exact test (p=0.05). Each category is compared using the Fisher Exact test (p=0.05). The comparisons that are significant are in bold. Overall (Exact value=37.566, p=0.002), 0x1-5 (Exact value=24.456, p=<0.005), 0x6-10 (Exact value=30.021, p=<0.005), 0x11-20 (Exact value= 16.712, p=<0.005), 0 x 21-30 (Exact value=16.022, p=1.00), 1-5x6-10 (Exact value=5.955, p=1.00), 1-5x11-20 (Exact value=0.621,p=1.00), 1-5x21-30 (Exact value=1.282, p=1.00), 6-10x11-20 (Exact value=3.685, p=1.00), 6-10x21-30 (Exact value=2.864, p=1.00), 11-20x21-30 (Exact value=0.836, p=1.00).

306

Locomotor Behavior

% Total Height QD LP CL D OT Obs N 0 99.1 0.9 0 0 0 34.5 114 1 - 5 m 64.5 6.5 16.1 10.5 2.4 37.6 124 6 – 10 m 27.5 30 20 22.5 0 12.1 40 11-20 m 62.2 18.9 13.5 5.4 0 11.2 37 21-30 m 80 13.3 6.7 0 0 4.5 15

Table 5.10: Locomotor frequencies of juveniles at each height class. Each category is compared using the Fisher Exact test (p=0.05). None of the comparisons are significant. Overall (N/A), 0x1-5 (Exact value=52.56, p=1.00), 0x6-10 (Exact value=88.737, p=1.00)0x11-20 (Exact value=35.273, p=1.00), 0 x 21-30 (Exact value=11.099, p=1.00), 1- 5x6-10 (Exact value=23.849, p=1.00), 1-5x11-20 (Exact value=5.393,p=1.00), 1-5x21-30 (Exact value=3.30, p=1.00), 6-10x11-20 (Exact value=10.454, p=1.00), 6-10x21-30 (Exact value=11.743, p=1.00), 11-20x21-30 (Exact value=1.377, p=1.00).

307

Locomotor Behavior

% Total Height QD LP CL D OT Obs N 0 m 99.5 0 0 0 0.5 46.6 208 1 – 5 m 74.8 9.3 7.9 7.9 0 33.9 151 6 – 10 m 48.4 19.4 9.7 22.6 0 7 31 11-20 m 71.4 16.7 9.5 2.4 0 9.4 42 21-30 m 71.4 7.1 14.3 7.1 0 3.1 14

Table 5.11: Locomotor frequencies of subadults at each height class. Each category is compared using the Fisher Exact test (p=0.05). None of the comparisons are significant. Overall (N/A), 0x1-5 (Exact value=63.623, p=1.00), 0x6-10 (Exact value=70.585, p=1.00), 0x11-20 (Exact value=43.261, p=1.00), 0 x 21-30 (Exact value=26.381, p=1.00), 1-5x6-10 (Exact value=10.020, p=1.00), 1-5x11-20 (Exact value=3.224,p=1.00), 1-5x21-30 (Exact value=1.133, p=1.00), 6-10x11-20 (Exact value=8.119, p=1.00), 6-10x21-30 (Exact value=3.085, p=1.00), 11-20x21-30 (Exact value=1.983, p=1.00).

Zone Total Frequency Individual Records 0 499 45.5 1 22 2 2 18 1.6 3 192 17.5 4 0 0 5 366 33.4

Table 5.12: Total number of locomotion individual scans and their frequencies by tree zone. 0= ground, 1= vertical tree trunk, 2= inner branches adjacent to tree trunk, 3= terminal branches, 4= top of tree canopy, 5= lianas and treefalls adjacent to the tree

308

Locomotor Behavior

Zone QW QR LP CL D OT % Total N 0 75.4 24 0 0 0 0.4 45.5 499 1 4.5 0 4.5 22.7 68.2 0 2 22 2 55.6 0 11.1 27.8 5.6 0 1.6 18 3 57.8 11.5 23.5 4.7 2.6 0 17.5 192 5 61.5 8.7 6.6 12 10.4 0.8 33.4 366

Table 5.13: Frequency of locomotor behaviors by tree zone for all ages and sexes and total percentage of locomotor observations in each zone.

Locomotor Behavior

Zone QD LP CL D OT % Total N 0 99.3 0 0 0 0.7 54.5 151 1 14.2 14.2 42.8 28.5 0 2.5 7 2 100 0 0 0 0 2.2 6 3 83.3 10.4 2.1 4.2 0 17.3 48 5 84.6 0 3.1 12.3 0 23.5 65

Table 5.14: Frequency of locomotor behaviors of adults by tree zone. Each category is compared using the Fisher Exact test (p=0.05). The comparisons that are significant are in bold. All zones (Exact value=73.358,p=0.000), 0x1 (Exact value=47.072,p=0.000), 0x2 (Exact value=N/A, p=0.962), 0x3 (Exact value=21.356,p=0.000), 0x5 (Exact value=22.116,p=0.000), 1x2 (Exact value=8.494,p=0.009),1x3 (Exact value=17.689,p=0.000), 1x5 (Exact value=20.077,p=0.000), 2x3 (Exact value= 1.318,p=1.00), 2x5 (Exact value=0.717,p=1.00), 3x5 (Exact value=8.656,p=0.017).

309

Locomotor Behavior

Zone QW QR LP CL D OT % Total N 0 62.3 36.8 0.9 0 0 0 34.5 114 1 0 0 0 0 100 0 3 10 2 50 0 0 50 0 0 2.4 8 3 49.2 13.8 30.8 3.1 3.1 0 19.7 65 5 48.9 12 6.8 21.1 9 2.3 40.3 133

Table 5.15: Frequency of locomotor behaviors of juveniles by tree zone. Each category is compared using the Fisher Exact test (p=0.05). The comparisons that are significant are in bold. All zones (Exact value=64.131,p=0.000), 0x1 (Exact value=62.261,p=0.000), 0x2 (Exact value=25.391, p=0.000), 0x3 (Exact value=47.22,p=0.000), 0x5 (Exact value= 68.549, p=0.000), 1x2 (Exact value=18.310,p=0.000),1x3 (Exact value=40.269,p=0.000), 1x5 (Exact value=34.416,p=0.000), 2x3 (Exact value=14.246,p=0.002), 2x5 (Exact value=3.391,p=0.561), 3x5 (Exact value= 29.813,p=0.000).

Locomotor Behavior

Zone QD LP CL D % Total N 0 100 0 0 0 47.6 233 1, 2, 3 59.1 25 10.2 5.7 18 88 5 72 7.6 8.3 10.7 34.4 168

Table 5.16: Frequency of locomotor behaviors of subadults by tree zone. Zones 1, 2, and 3 were combined for the overall cross-tabulations because of the limits of the Fisher Exact test. Each category is compared using the Fisher Exact test (p=0.05). The comparisons that are significant are in bold. All zones (Exact value=126.313,p=0.000), 0x1 (Exact value= 47.385, p=0.000), 0x2 (Exact value=43.444, p=0.000), 0x3 (Exact value=76.731,p=0.000), 0x5 (Exact value= 81.033, p=0.000), 1x2 (Exact value=2.844,p=0.381),1x3 (Exact value=22.206, p=0.000), 1x5 (Exact value=14.919,p=0.001), 2x3 (Exact value=11.155,p=0.008), 2x5 (Exact value=11.330,p=0.006), 3x5 (Exact value= 16.797,p=0.001).

310

Support Size Total Frequency Individual Records Ground 499 45.5 Twig 113 10.3 Branch 455 41.5 Bough 30 2.7

Table 5.17: Total number of locomotion scans and their frequencies by support size for all ages and sexes.

Locomotor Behavior

Support QW QR LP CL D OT % Total N Ground 75.4 24 0 0 0 0.4 45.5 499 Twig 44.2 8 23 14.2 9.7 0.9 10.3 113 Branch 63.7 9.9 9.9 9.2 7 0.2 41.5 455 Bough 23.3 0 3.3 16.7 53.3 3.3 2.7 30

Table 5.18: Frequency of locomotor behaviors by support type for all ages and sexes combined and total percent of observations during locomotion on each support type.

311

Locomotor Behavior

Support Type QW QR LP CL D OT Total

Tree Trunk 4.5 0 4.5 22.7 68.2 0 100

Number of individuals 1 0 1 5 15 0 22 within scans

Table 5.19: The frequency of locomotor behaviors on vertical and horizontal tree trunks for all ages and sexes combined.

Locomotor Behavior

Support Type QW QR LP CL D OT % Total N Ground 87.4 11.9 0 0 0 0.6 54.5 151 Twig 57.1 0 14.3 0 28.6 0 5.1 14 Branch 81.9 6.7 2.8 2.8 5.7 0 37.9 105 Bough 14.2 0 14.2 42.9 28.6 0 2.5 7

Table 5.20: Frequency of locomotor behaviors by support type for adults. Each category is compared using the Fisher Exact test (p=0.05). The comparisons that are significant are in bold. All supports (Exact value=72.024,p=0.000), Ground x Twig (Exact value=32.134, p=0.000), Ground x Branch (Exact value=17.519,p=0.000), Ground x Bough (Exact value=47.072, p=0.000), Twig x Branch (Exact value=10.914,p=0.007), Twig x Bough (Exact value=7.177, p=0.051), Branch x Bough (Exact value=22.027,p=0.000).

312

Locomotor Behavior

Support Type QW QR LP CL D OT % Total N Ground 62.3 36.8 0.9 0 0 0 34.5 114 Twig 37.1 6.5 27.4 21 6.5 1.6 18.8 62 Branch 53.6 15 8.6 15 7.1 0.7 42.4 140 Bough 21.4 0 0 0 71.4 7.1 4.2 14

Table 5.21: Frequency of locomotor behaviors by support type for juveniles. Each category is compared using the Fisher Exact test (p=0.05). All comparisons are significant. All supports (Exact value=51.318,p=0.000), Ground x Twig (Exact value=81.323, p=0.000), Ground x Branch (Exact value=52.070,p=0.000), Ground x Bough (Exact value=58.312, p=0.000), Twig x Branch (Exact value=16.337,p=0.004), Twig x Bough (Exact value=28.640, p=0.000), Branch x Bough (Exact value=33.009,p=0.000).

Locomotor Behavior

% Support Type QD LP CL D Total N Ground 100 0 0 0 47.6 233 Twig 64.9 18.9 8.1 8.1 7.6 37 Branch 69.5 14.3 8.6 7.6 42.9 210 Bough 33.3 0 4 2 1.8 9

Table 5.22: Frequency of locomotor behaviors by support type for subadults. Each category is compared using the Fisher Exact test (p=0.05). Comparisons that are significant are bold. All supports (Exact value=N/A,p=N/A), Ground x Twig (Exact value=52.678, p=0.000), Ground x Branch (Exact value=97.216,p=0.000), Ground x Bough (Exact value=44.651, p=0.000), Twig x Branch (Exact value=0.822,p=0.842), Twig x Bough (Exact value=9.028, p=0.016), Branch x Bough (Exact value=12.382,p=0.003).

313

Habitat Total Individual Frequency Records Beach 88 8 Terra Firme 1009 92

Table 5.23: Total number of locomotion scans and their frequencies by habitat type for all ages and sexes.

Locomotor Behavior

Habitat QW QR LP CL D OT % Total N Beach 53.4 6.8 17 8 14.8 0 8 88 Terra Firme 70.3 12.6 6.9 6.5 3.3 0.4 22.4 246 Lagoon 65.9 18 5.4 5.2 5 0.5 65.9 763

Table 5.24: Frequency of locomotor behaviors by habitat type for all ages and sexes and the total percent of locomotor observations in each habitat type. There are no significant differences in locomotor behavior by habitat type (Exact value=9.315, p=0.450)

314

Locomotor Behavior

Habitat QW QR LP CL D OT % Tot N Beach 43.2 2.7 21.6 10.8 21.6 0 11.2 37 Terra Firme 64.2 12.3 9.9 9.9 3.7 0 24.5 81 Lagoon 49.1 26.4 14 6.6 6.1 1.4 64.2 212

Table 5.25: Frequency of locomotor behaviors by habitat type and total percent observations for juveniles. Each category is compared using the Fisher Exact test (p=0.05). Comparisons that are significant are bold. Beach x Lagoon (Exact value=24.468, p=0.000), Beach x Terra Firme (Exact value=14.796, p=0.003), Lagoon x Terra Firme (Exact value=9.985, p=0.064).

Locomotor Behavior

% Habitat QD LP CL D Total N Beach 60.7 21.4 7.1 10.7 5.7 28 Terra Firme 83.7 7.1 6.1 3.1 20 98 Lagoon 84.5 6.6 4.1 4.7 74 362

Table 5.26: Frequency of locomotor behaviors by habitat type and total percent observations for subadults. There are no significant differences in locomotion by habitat type (Exact value=15.839, p=0.083).

315

Locomotion N Q L CL Travel 2,328 46 21 31 Feed 1,583 48 11 40

Table 5.27: Locomotion of Lophocebus albigena from Kibale National Park, Uganda. Data from Gebo and Chapman 1995a. Data represent percentage of total time spent in each positional behavior. N= number of bouts, Q= quadrupedalism, L= leap, CL= climb

Figure 5.1: A comparison of Papionin scapulae reveals a taller suprascapular fossa and deeper inferior angle among Cercocebus and Mandrillus. (From Fleagle and McGraw, 2002:271).

316

C. torquatus C. atys L. albigena

Figure 5.2: The differences in degree of suborbital fossa depth among different mangabey species. (From McGraw and Fleagle, 2006).

C. torquatus M. leucophaeus

Figure 5.3: The similar degree of paranasal ridging between C. torquatus and M. leucophaeus. (From McGraw and Fleagle, 2006).

317

Figure 5.4: The coastal palm, or beach, forest of Sette Cama, Gabon.

318

Figure 5.5: A section of the “main trail,” or terra firme forest of Sentier Nature.

Figure 5.6: C. torquatus on the ground of the terra firme forest of Sette Cama, Gabon. 319

Figure 5.7: Vegetation map of the Sentier Nature Forest. Mature and swamp forest are combined as “terra firme” forest. (Map by Richard Moussopo).

Figure 5.8: C. torquatus quadrupedal walk.

320

Figure 5.9: C. torquatus quadrupedal run.

321

Figure 5.10: Climb.

Figure 5.11: Leap. (Photo by CERCOPAN).

322

Figure 5.12: Descend Bottom First.

Figure 5.13: Descend Head First. (Photo by Lucy Keith).

323

Figure 5.14: Tree zones; 0=ground (not marked), 1= tree trunk, 2= interior canopy branches, 3=terminal branches, 4= uppermost canopy, 5=areas adjacent to tree trunk including lianas and treefalls.

324

Figure 5.15: The hands of C. torquatus on the largest support type, a bough.

325

Figure 5.16: Adult female sitting on a branch.

Figure 5.17: C. torquatus gripping twigs, or the smallest supports available in an arboreal context.

326

Figure 5.18: The palm trees typical of the beach forest in Sette Cama.

327

Figure 5.19: C. torquatus eating a palm fruit in the discontinuous roots and branches associated with the zone nearest to the lagoon.

328

Locomotor Behavior of C. torquatus and C. atys (C. torquatus N=155, C. atys N=466)

65.9

QW 80.7

15.9 QR 5.7

C. torquatus 6.7 LP 1.02 Cercocebus atys

Locomotor behavior Locomotor 11 CL 12.5

0 20 40 60 80 100 Percentage of scans

Figure 5.20: A comparison of the locomotor profiles of all individuals of C. torquatus (this study) and C. atys from Taï National Park, Côte d’Ivoire. C. atys data are from McGraw 1996a. Numbers represent percentage of time spent in each positional behavior and the data for C. torquatus are for all age and sex classes combined. I merged the categories of “climb” and “descend” for C. torquatus because McGraw did not distinguish between these behaviors.

329

Locomotor Behavior: Adults

Other

Leap

C. atys Climb C. torquatus Locomotor Behavior Locomotor Quadrupedal

0 20 40 60 80 100 % Scans

Figure 5.21: The locomotor profiles of adult C. torquatus (N=155) and C. atys (N=466). C. atys data are from McGraw 1996a.

330

Strata Use

Canopy

Understory

C. atys Shrub C. torquatus

Ground

0 20 40 60 80 % of scans

Figure 5.22: The strata use of adult C. torquatus compared to C. atys. I transformed my values of height class and tree zone use to correspond with McGraw’s strata divisions (1996a). Ground= 0 meters or substrates directly near the ground such as fallen logs; Shrub= substrates up to 5 meters; Understory= the tree canopy between 5 and 20 meters; Canopy= 20 – 40 meters; Emergent= 40+ meters. Neither C. torquatus nor C. atys were observed in the emergent layer.

331

80 Support Use 70 % 60

50 S c 40 C. torquatus a 30 n C. atys s 20 10 0 Ground Twig Branch Bough Other Support Type

Figure 5.23: Support use during locomotion for adult C. torquatus and C. atys. C. atys data are from McGraw 1996a. Note the categories of vertical trunk and bough were combined in this study and therefore, I combined these categories for C. atys.

332

Figure 5.24: A comparison of C. torquatus (G3) and C. atys (2106) scapulae. Note the more superiorly inclined supraspinous fossa in C. atys. This feature is associated with above head reaching during arboreal movement.

333

Chapter Six: Posture

6.1 Introduction

This chapter continues from the previous chapter’s examination of the

positional behavior of C. torquatus in the Sentier Nature forest, Sette Cama, Gabon.

Postures comprise an important part of any primate’s positional behavior repertoire since they are employed during periods of feeding, resting, and social behavior.

Postures are known to covary with a species’ foraging strategy, activity patterns,

support use, and the spatial distribution of food (McGraw, 1996a, 1998). Morphological

studies suggest that Cercocebus mangabeys are semi-terrestrial, hard-object foragers

that display numerous morphological adaptations for this unique feeding niche (Fleagle

and McGraw, 1999, 2002). These skeletal features are associated with extensive

flexion/extension movements of the forelimbs from a seated or standing position.

This study examines the postural behavior of C. torquatus in different ecological

and ontogenetic contexts to ascertain the degree of intraspecific postural plasticity. I

hypothesize that the most commonly used postures remain constant regardless of

environment. I predict that non-adult C. torquatus will use a wider range of postures

than adult C. torquatus. The identification of postural trends among C. torquatus will also help elucidate if the feeding and foraging postures of this species correspond with

334

morphological predictions of postural behavior. These data will then be compared to

data from other studies on Cercocebus species and the more arboreal Lophocebus

mangabey in effort to understand how foraging strategy influences postural diversity.

6.2 Background

Positional behavior studies are tools for reconstructing the movements of extinct primate species and understanding how a primate’s morphology influences its interactions with the physical environment. The study of primate movements is divided into locomotion and posture. Locomotion involves… “gross displacement of the animal relative to its surroundings” (Rose, 1974:201) during activities such as traveling or feeding. Most positional behavior studies focus on locomotion because of its presumed importance in shaping the postcranial anatomy and a species’ adaptations (McGraw,

1998).

Postural behaviors, on the other hand, involve little or no displacement of the body (Rose, 1974). During postures, the trunk remains stationary and movement is restricted to the limbs (Prost, 1965). Postures occur during feeding or foraging (periods of searching for or consuming foods that involve little to no trunk movement), resting

(lack of movement usually associated with sleeping or time between traveling), and social behaviors (grooming or touching other individuals without significant trunk displacement) (Aronsen, 2004). Some common postures used by primates include: sitting, quadrupedal standing, reclining, suspension, forelimb supported stand, etc.

(Hunt et al., 1996).

335

Posture is an important component of a primate’s behavioral repertoire and

overall fitness (Fleagle, 1999; McGraw and Scuilli, 2011). The role of postures in feeding

and foraging make postural behaviors critical to an animal’s survival. For example, some

lemurs and New World primate species evolved claw-like nails which facilitate clinging

postures for gummivory and insectivory on large vertical trunks (Garber, 1991; Garber,

2011). However, many primates feed on fruits and leaves located on the thin, unstable

terminal branches of trees (Grand, 1972). The evolution of suspensory and grasping

postures allows larger bodied primates to extend their feeding spheres and access foods

while using more stable substrates. One of the largest New World primates, the black

spider monkey (Ateles paniscus), spends over half of its feeding time using prehensile tail assisted suspensory postures in the tree crown periphery that allow them to collect foods at or below body level (Youlatos, 2002).

Although it is often thought that posture has less of an effect on skeletal

morphology than locomotion, “…posture is rarely a passive state, and behaviors which

do not involve actual movement of the limbs may nevertheless involve significant

musculoskeletal stresses” (McGraw, 1998:230). Indeed, certain postures have been

associated with particular skeletal features among extant and extinct primates. For

example, among lemurs, the length of the lumbar region of the spine and the lumbar

vertebral bodies varies depending upon the predominant postures used (Shapiro and

Simons, 2002). Lemurs using quadrupedal locomotion and pronograde postures have

longer vertebral bodies than species that use orthograde postures (Shapiro and Simons,

336

2002). This reflects the need for spinal flexibility among quadrupeds. Prosimian and

platyrrhine vertical clingers and leapers feature a dorsally projected ischium that is

associated with leaping from vertical postures (Fleagle and Anapol, 1992). In contrast,

species that leap from pronograde postures have less dorsal projection of the ischium.

These form-function relationships can be applied to the fossil record to recreate the

postures of extinct taxa. For example, analyses of the pelvis of the Eocene primate

species Notharctus and Smilodectes suggest they used similar positional behaviors to

modern vertical clinger and leapers and probably used orthograde postures (Fleagle and

Anapol, 1992).

Ischial tuberosities, found only among catarrhines, are an important pelvic

adaptation associated with sitting (Napier, 1967; McGraw and Scuilli, 2011). The

evolutionary function of this feature has been debated to be either an adaptation to

arboreal sleeping or for terminal branch feeding in above-branch primates (Rose, 1974).

In their comparison of ischial tuberosity size among cercopithecids, McGraw and Scuilli

(2011) found that tuberosity size was largest among those primates that feed most

often in the terminal branch setting. Therefore, ischial tuberosity size can inform

researchers as to the feeding strategy and postures of extinct primate species.

Rose (1974) recognized the importance of posture both functionally and

behaviorally when he noted that the majority of a primate’s time is spent in postural

activities (McGraw, 1998). For example, Colobus guereza (the guereza or black and white colobus monkey) spends the majority of its time in above branch postures and

337 locomotion makes up only one fifth of overall positional behavior (Morbeck, 1977).

Additionally, locomotion and postures often grade into one another such as when quadrupedal standing leads to quadrupedal walking (Prost, 1965; Garber, 2011).

Therefore, postural behaviors not only potentially impact primate musculoskeletal morphology, but postures also account for a substantial portion of a primate’s life

(Prost, 1965; McGraw, 1998).

Postural Behavior: The influence of maintenance activity and foraging strategy

McGraw (1996) acknowledged the dearth of postural information for primates, and in particular, primates that utilize above-branch feeding postures. He also identified the lack of a theoretical framework for understanding postural differences among groups of primates. Postural behaviors are possibly influenced by a number of factors including maintenance activity and foraging strategy, habitat type, and substrate availability.

Postures only occur during certain maintenance activities, and the type of postures used depends on the musculoskeletal adaptations of the different primate taxa. The number and type of postures employed both within and between primate species should be the most variable during foraging (Garber, 2011). The use of various postures enables a primate to adapt to varieties in food availability and resource distribution. Primates with suspensory adaptations, such as New World monkeys, are most often observed using suspended postures such as arm-hang, tail-suspend, etc. during feeding and foraging (Mendel, 1976; Gebo, 1992; Youlatos, 2002). This allows

338 these primates to reach fruits and foods on slender terminal branches. Cercopithecines usually only use postures like forelimb-supported stand or bipedal standing during feeding (Rose, 1974; McGraw, 1996a, 1998b). However, sitting dominates all feeding postures among a wide range of primate taxa including lemurs (Dagasto, 1995), capuchins (Gebo, 1992), howler monkeys (Gebo, 1992; Mendel, 1976; Prates and Bicca-

Marques, 2008), colobus monkeys (Morbeck, 1977; McGraw, 1996a, 1998b), long-tailed macaques (Cant, 1988), chimpanzees (Hunt, 1992; Doran, 1993) and orangutans (Cant,

1987).

Sitting, reclining, or sprawling postures are most often associated with resting or social behaviors. Above-branch quadrupeds frequently use their hands or feet as additional supports while sitting in the trees. “…[T]he animal sits on a stable triangular base the apices of which are formed by the two feet and the ischial callosities” (Rose,

1974:208; Figure 6.1). Rose (1974) suggests that terrestrial primates should adopt more standing postures and sit with abducted hindlimbs. In general, colobines use reclining postures during rest more often than cercopithecines (Morbeck, 1977; McGraw, 1998).

In his study of the Taï Forest cercopithecids, McGraw found variation in postures between colobines and cercopithecines (1996, 1998, 2002). These interspecific differences were associated with the spatial distribution of their preferred foods.

Primates that feed on insects or fruits, which tend to be more patchily distributed foods, should adopt transitional postures (such as quadrupedal or bipedal stand) that allow for more efficient movement between feeding patches whereas folivores should use more

339 permanent postures (such as sitting). For example, the least insectivorous guenon, C. petaurista, was observed sitting most often compared to the other sympatric guenon species in Taï (McGraw, 2000). Colobines use more sitting and reclining postures than guenons which is associated with their low quality folivorous diet and their mobile hip and shoulder joints (McGraw, 2003). Therefore, primates with similar body sizes may adopt different postures depending upon the location of their preferred foods.

Postural Behavior: Differences between the sexes

Just as body size was predicted to influence locomotor behaviors, it may also influence a species’ postural behaviors. Postural capabilities impact the ability to feed and obtain different food resources, and body size potentially limits the types of substrates available to an animal. Primates tend to be sexually dimorphic, with males exceeding females in body size and weight. Therefore, one might expect to observe differences in how each sex uses postures and substrates. “…[L]arger animals would either use larger substrates than smaller animals, or engage in relatively more frequent suspensory behavior” (Doran, 1993:100). Because of the restrictions of the arboreal environment, body size and weight should influence a primate’s decision on where

(such as substrate choice) and how to feed in the trees. Nevertheless, studies provide conflicting evidence as to the degree of postural differences between the sexes among sexual dimorphic species.

Sexually dimorphic species are useful for investigating the impact of body weight and size on posture because this controls for any phylogenetic differences in postcranial

340

morphology that may impact positional behaviors (Cant, 1987). Studies among great

apes have found that species with significant size dimorphism between the sexes display

slight postural differences and use substrates in different frequencies (Cant, 1987;

Doran, 1993); however, most studies do not show significant variation in postures used

between the sexes. When sex differences in postures are observed, other variables

such as predation pressure and food availability have a more profound effect on

postures than body size.

Among Sumatran orangutans, females used suspensory below branch feeding

postures more often than males, which can weigh two times as much as females (Cant,

1987). Male orangutans used larger supports and employed above-branch postures

more frequently than females. There also were significant differences in the postures

used by adult male and female chimpanzees in Taï despite a similar trend in overall

postural behaviors (Doran, 1993). Females were observed sitting more often than males

during resting, and females spent more postural time above ground than males. Males

also used larger substrates than females. Some of these differences in postures were

attributed to increased predation pressure for females due to their solitary foraging

practices.

Sex differences in postural behaviors have also been observed in several Old

World monkey species. Chatani (2003) observed differences in the amount of time spent in different postures during resting among Japanese macaques (Macaca fuscata).

Male macaques sat more often whereas females used the lying posture more often.

341

Chatani (2003) attributed these differences not to body size but to differences in

grooming behaviors between female and male Japanese macaques. There were also

significant differences in postures between the sexes in the ursine colobus and Lowe’s

monkey from Ghana (Schubert, 2011). Schubert (2011) attributes the contrast in

postures among males and females to differences in body size, nutrition, and social

roles.

Several other studies found no significant differences in the postures used by

males and females (Gebo, 1992; Gebo and Chapman, 1995b; Remis, 1998; Aronsen,

2004). Despite their high degree of body size dimorphism, male and female lowland

gorillas employ similar postural behaviors during feeding, and sitting was the most

common posture among both sexes (Remis, 1998). Gebo and Chapman (1995b) and

Aronsen (2004) observed very little differences in the postures employed by male and female cercopithecids in Kibale National Park. Among New World monkeys, male and female adult howler monkeys (Alouatta palliata) had nearly identical postural behaviors, and white-faced capuchin (Cebus capucinus) male and female adults differed only slightly in their use of sitting and reclining (Gebo, 1992). Overall, the majority of studies suggest that postures are conservative within adults of the same species.

Postural Behavior: Ontogeny

Compared to other mammals, the period of growth and development is extended among primates. During this time, young animals learn to negotiate both their social and physical environments (Workman and Covert, 2005). A growing primate

342

must figure out how to forage independently, develop socially, and avoid predation. In

the meantime, they must also adapt to changes in body mass, body proportions, and

motor skills (Bezanson, 2009). Selection acts throughout an individual’s lifetime, and

therefore, this also includes the positional behaviors used during growth and

development (Carrier, 1996).

The goal of ontogenetic studies of positional behavior is to “…test functional

relationships between growth-related changes in positional behavior (and anatomy)

with respect to the demands imposed by structural or ecological factors” (Lawler,

2006:262). A comparison of adult and non-adult positional behaviors can help elucidate

if and why individuals of various ages negotiate their environments differently and how

they adapt.

Although most positional behavior research has focused on adult individuals, the

studies that address the ontogeny of positional behaviors have found significant

differences in postures used by the different age groups. Among platyrrhines, postural

differences were observed between juvenile and adult mantled howler monkeys

(Alouatta palliata) (Mendel 1976; Bicca-Marques and Calegaro-Marques, 1993; Prates

and Bicca-Marques, 2008; Bezanson, 2009). Juvenile howler monkeys were observed

using tail/hindlimb suspend or tail suspend postures during feeding 10% more often

than adults (Mendel, 1976). Sitting was more common among adult howler monkeys

than infants, and the use of suspensory postures declined in older individuals (Bicca-

Marques and Calegaro-Marques, 1993; Prates and Bicca-Marques, 2008). In a

343 comparative study of the ontogeny of positional behavior between mantled howler monkeys and white-faced capuchins (Cebus capucinus), Bezanson (2009) observed that juvenile capuchins used postures in similar frequencies to adults but the howler monkey postures differed between age groups.

Studies among catarrhines also indicate a varied postural repertoire between adults and non-adults. Juveniles in several species of Asian langurs used suspensory postures more often than adults and used two postures not seen in adults (Workman and Covert, 2005). Non-adult rhesus macaques (Macaca mulatta) were observed in bipedal stand, quadrupedal stand, and hang postures significantly more often than adults (Wells and Turnquist, 2001). Standing postures enabled the shorter individuals to see at greater heights and hanging was employed during periods of play or exploring.

Eakins and McGraw (2010) noted differences in hindlimb postures among captive silvered langurs (Trachypithecus cristatus) of different age groups. Older individuals engaged in propped-foot postures more often than younger individuals. Together, these studies suggest that postural behaviors are influenced by the changes associated with growth and development.

Postural behavior: The influence of substrate and support size

Of all the variables that impact postural behaviors, support type should be the most influential because of the limitations associated with substrates of different size, strength, and availability. This is particularly salient in an arboreal context where primates must maintain their balance and stability on a variety of supports. The

344

majority of arboreal primates’ foods are located in the smaller, terminal branches of the trees and this setting “place[s] certain demands on an animal’s positional capabilities”

(Ripley, 1967; Rose, 1974:205). The postures used in arboreal contexts are a compromise to incorporate variables like substrate size and type, maintenance activity, and species specific morphological adaptations (Doran, 1993). Studies reveal that diet and foraging behaviors are more influential on substrate choice during postures than body mass (Garber, 1984; Dagasto, 1994; Gebo and Chapman, 1995b; McGraw, 1998;

Youlatos, 2002).

Postures typically occur during feeding, resting, or social behaviors, and postural behaviors depend on the features of the substrate used in each activity. During arboreal feeding, substrate choice is more limited because of the location of food sources on smaller substrates such as twigs or branches (Grand, 1972; Doran, 1993).

Therefore, arboreal primates are forced to use smaller substrates during feeding and foraging compared to other maintenance activities. McGraw (1998) observed significant

differences in the substrates used by the six cercopithecids during feeding in the Taï

National Forest. The largest arboreal species, Colobus polykomos and C. badius, used

the intermediate sized substrates, or branches, the most frequently. The medium sized

olive colobus (C. verus) used twigs and branches during the majority of feeding. When

sooty mangabeys (Cercocebus atys) fed in the trees, they preferred medium and small

substrates; however, they were most often observed on the ground. This is different

than other more terrestrially adapted species, such as Theropithecus, that do not have

345

suspensory adaptations or mechanisms to distribute their weight over small supports

(Rose, 1974).

Substrate choice is less limited during resting and social behaviors (in other

words, primates are not looking for foods located on small, terminal branches) so the

frequency of the use of larger substrates is increased during these activities (McGraw,

1998). As noted by McGraw (1998), “…although monkeys of all sizes spend considerable

time foraging in the terminal branches, even the smallest cercopithecids move to more

stable supports when they have finished feeding” (245).

Postural behavior: The influence of habitat type

As mentioned above, positional behavior studies should address the possibility

of within species variation in positional behaviors since they may vary by habitat or

forest type (Gebo and Chapman, 1995a; Bergeson, 1996; Youlatos, 2002; Aronsen,

2004). Habitat studies address the flexibility or conservation of positional behaviors in

different contexts and potentially impact the validity of relying upon extant species to

reconstruct behaviors of extinct species. Although many studies suggest that postures

are conservative among species in different habitat types or field sites (Mittermeier,

1978; McGraw, 1996a; Youlatos, 2002), several studies found variation among postural frequencies between habitats. Gebo and Chapman (1995a) found slight differences in the frequencies of postures used by red colobus monkeys across primary, secondary, and pine habitats in Kibale National Park. The frequency of sitting was highest in the primary forest and vertical clinging was observed more often in the pine forest

346

compared to the primary and secondary forests. However, Gebo and Chapman admit:

“[C]ommon positional behaviors are still common and rare behaviors occur infrequently

across these comparisons” (1995a:80). Dagasto (1995) observed slight differences in

the postures used by red-bellied lemurs in two different habitats in Ranomafana

National Park. There were variations in the amount of time spent sitting and lying among the two sites. Aronsen (2004) also observed intraspecific differences in the amount of bipedal standing and vertical clinging between habitats among colobines within the Kibale National Forest.

Despite the subtle intraspecific variations observed between several primate populations in different habitats, researchers suggest that differences in foraging strategy may exert a greater influence on postural behaviors than does habitat structure

(McGraw 1996a, 1998).

Postural data for Cercocebus species

Cercocebus mangabeys are characterized as semi-terrestrial primates that

frequently climb vertical tree trunks (Fleagle and McGraw, 1999, 2002). They feature

many anatomical specializations for terrestrial, hard-object foraging such as enlarged

forelimb muscle attachment sites that are associated with extensive pronation and

supination movements from seated or standing postures and molarized premolars that

help crack hard nuts.

Despite the anatomical information available, postural data are only available for

one Cercocebus species, C. atys. C. atys postural behaviors are dominated by sitting

347

(80.9%) and quadrupedal standing (15.7%) both overall and during all maintenance activities (McGraw, 1996a, 1998b). They rarely use supported standing (1.9%) and

“other” postures (1.5%). Results from other Cercocebus species will determine if this is the typical postural pattern among semi-terrestrial primates.

Jones and Sabater Pi (1968) provided anecdotal information on the postures used by C. torquatus compared to L. albigena. They suggested that sitting was less important in C. torquatus than L. albigena. “C. torquatus assumes a sitting position less frequently than [L. albigena]. In C. torquatus, the rump, feet, and hands support the body from below whereas L. albigena… uses a spread-eagled and sprawled out sitting posture” (Jones and Sabater Pi, 1968:104). However, no systematic postural behavior data are available for C. torquatus. This study will be the first to compare Cercocebus and Lophocebus postural behaviors.

6.2 Research Questions

Non-locomotor behaviors have often been ignored in positional behavior studies, and those studies that do address postures present equivocal results on the impact of differing ontological and ecological contexts on postural behaviors.

Furthermore, the degree of differences in postures among semi-terrestrial and arboreal primates has not been identified. Nakatsukasa (1994, 1996) recognized morphological distinctions among Lophocebus (arboreal) and Cercocebus (semi-terrestrial) species related to locomotion. Since these genera are skeletally adapted to their particular substrates, they should show differences not only in locomotion but also postures.

348

Lophocebus and Cercocebus mangabeys also share similarities in body sizes, frugivorous

diets (for most Cercocebus species) but differ in degree of arboreality (Shah, 2003). In

order to expand our knowledge of postures among Cercocebus species, and

cercopithecines, in general, I examined the postural behaviors of C. torquatus in Sette

Cama, Gabon to answer the following questions:

• What is the postural behavior of C. torquatus, and how does it compare to other

Cercocebus species?

• Does the use of postures change throughout the process of growth and

development in C. torquatus?

• Does the use of postures vary across architecturally distinct habitat types in C.

torquatus?

• How does posture differ among arboreal and semi-terrestrial primates? How do

these different foraging strategies impact postural behaviors?

The results of this study will be compared to postural data on Lophocebus (Gebo

and Chapman, 1995a) to help elucidate any differences between the mangabey genera.

6.3 Predictions

1. As seen among other cercopithecines, sitting will be the most common posture

used by C. torquatus. When resting, C. torquatus will rarely use sprawling or lying postures. Quadrupedal standing and forelimb supported postures should be most common during feeding or foraging activities.

349

Sitting is the most common posture in the majority of primates. Cercopithecines also rarely use lying or sprawling postures seen among colobines (McGraw, 1998).

Therefore, sitting should be the most common postural behavior among C. torquatus during every non-locomotor maintenance activity. Given their above-branch arboreal and terrestrial adaptations, I do not expect C. torquatus to use suspensory postures.

Cercopithecines use quadrupedal stand and postures such as “stand/forelimb- suspend” during feeding and foraging (Gebo and Chapman, 1995a; McGraw 1998b:242).

This allows the primates without suspensory adaptations to reach foods on terminal branches. Therefore, C. torquatus should most frequently be observed using forelimb support postures such as “supported stand” when feeding in arboreal contexts or on lianas. I predict that C. torquatus will use the quadrupedal stand posture most frequently during terrestrial feeding. This allows the red-capped mangabeys to use their forelimbs to search for fallen fruits and seeds such as Sacoglottis gabonensis in the leaf litter without having to alternate between standing and sitting postures when moving between feeding sites. Feeding among cercopithecines tends to be rapid and mobile

(McGraw, 1998). Therefore, it is more energetically efficient to feed from standing postures that allow quick movements.

2. Postures will not differ between male and female adults, but juveniles should employ a wider range of postures not seen in subadult and adult repertoires.

Most studies comparing adult cercopithecids found no differences in postures between the sexes (Gebo and Chapman, 1995b; Aronsen, 2004). Therefore, I do not

350

predict any significant differences in postures used by males and females despite their

size differences. However, I expect that juveniles will employ a wider range of postures

(such as arm or hindlimb suspension) than subadults and adults because of their smaller

body size and flexibility. Indeed, research on the ontogeny of positional behavior finds a

wider postural repertoire among infants and juveniles compared to older animals

(Mendel, 1976; Workman and Covert, 2005; Prates and Bicca-Marques, 2007; Eakins

and McGraw, 2010).

3. The postures of C. torquatus will not differ significantly at different forest

heights or in the different tree zones. However, C. torquatus will use larger supports

for resting (branches and boughs) than feeding or foraging.

I predict no significant differences in postures at different forest heights or in the

different tree zones. However, I expect C. torquatus will use quadrupedal stand most

often during terrestrial foraging, and sit during resting more often in the trees than in

the ground. When inactive on the ground, I predict that C. torquatus will use

quadrupedal standing more often than sitting. Quadrupedal standing is an alert posture

that allows quick movement to higher forest levels at any sign of danger (Rose, 1974). It

is also less energetically expensive to transition into locomotion directly from standing

postures rather than standing up and sitting back down. Standing is also more efficient

when feeding on insects (which are mobile) or patchily distributed terrestrial resources.

C. torquatus should rest on larger substrates (boughs and branches) most frequently. McGraw (1996) noted the tendency of C. atys to sit on fallen trees or

351

branches rather than sit on the ground. During foraging, I predict that C. torquatus will use branches most often (when not on the ground) to reach foods on terminal branches from either a seated or standing posture.

4. Postural behaviors will be conservative across the different habitat types.

I expect no significant differences in the postures used in the lagoon/terra firme and beach forests. In general, cercopithecines use a limited range of postures compared to other primate groups (McGraw, 1996a). Because of the low amount of variation and flexibility in overall postural behaviors used by mangabeys, it is not expected that their postures will significantly vary in different habitat types. McGraw (1998) did not observe variation in postures by habitat type among the Taï primates.

Sitting will be the primary posture in both habitats followed by quadrupedal standing. I do, however, anticipate that the “other” postures such as supported stand will be more prevalent in the combined forest because of the higher fruit availability in this habitat type. Forelimb supported postures are associated with feeding and foraging.

6.4 Methods

Study site and Subjects

Data were collected on a group of red-capped mangabeys (N=70) in the Sentier

Nature forest of Sette Cama, Gabon from May 2009 to September 2009. This forest is a protected area located in the Gamba Park Complex in southwestern Gabon. Annual rainfall is 2093 mm (Lee et al., 2006). The annual temperature is 24˚-28˚ C, and there

352 are two dry seasons from June to September and January to February. The forest covers

254 ha and is bordered by the Atlantic Ocean on the west side and the Ndougou Lagoon on the east side.

Two habitat types were distinguished for this study—coastal palm beach forest and terra firme/lagoon combined forest. No significant differences were found in the overall frequencies of positional behaviors used in either the terra firme or lagoon habitat types (see Chapter 4).

The beach forest is characterized by Hyphenae guineensis palm trees, scrub bushes, and an open canopy. The terra firme/lagoon combined forest features more tree species, extensive undergrowth and lianas, and a canopy that varies from completely closed to open. The combined forest is larger in area than the beach forest.

The two habitat types differ significantly in mean DBH and tree distribution. For a more detailed description of the different habitat types and their characteristics, refer to chapter 2.

Behavioral Data Collection

Data were collected five days a week for a period of nineteen weeks. The days of the week in which data were collected often varied due to weather conditions and the presence of elephants and buffalo in the forest. My field assistant and I went into the forest two times a day: in the morning from 7:00 am to 11:30 am and in the afternoon from 2:00 pm until dusk. The monkeys spent mid-day resting in the inaccessible zone, and therefore, we were unable to obtain data during these hours.

353

Behaviors were studied using ten minute group scans every twenty minutes

(Altmann, 1974). Group scans are the most appropriate method of data collection when

interested in comparing behaviors across different age and sex classes. The number of individuals recorded in each scan ranged from 1 to 36 and the average number of individuals sampled per scan was 9.85. Every effort was made to sample all individuals of the group during each scan; nevertheless, each group scan represents only a subset of the entire C. torquatus group/subgroup under study. Issues of habituation, visibility, and large group spread made whole group scans not feasible at this site.

During each group scan, for each individual seen, the data collected were: sex, age class (adult, subadult, juvenile), maintenance activity (travel, feed, forage, rest, socio-sexual, other), height (visually estimated in meters), positional behavior

(locomotion and posture), forest zone, support size, and habitat type (see Chapter 2 for more detailed descriptions). The sex of subadults and juveniles were not noted because of visibility issues. It is also possible that subadult males were erroneously classified as adult females based on size similarities.

Postural behaviors are the positions taken during stationary periods like resting or feeding and foraging. Postures involve movements of the limbs without a major displacement of body weight. The postures identified for this study include: quadrupedal stand (QS), bipedal stand (BS), sitting (SI), lying (LY), suspend (SP), droop

(DP), and supported stand (SS) (definitions based on McGraw, 1996a). Quadrupedal stand was pronograde posture with support from all limbs (Figure 6.2). Bipedal stand

354 included orthograde posture with support from only the hindlimbs (not pictured).

Sitting was an orthograde posture with the body weight supported by the ischial callosities or the lower body (Figure 6.3). Lying included any posture where the trunk or limbs support body weight on a substrate (Figure 6.4). Suspend involved below substrate postures with the body weight supported by any combination of forelimbs and hindlimbs (not pictured). Droop is similar to lie except the limbs hang below the trunk (Figure 655). Supported stand involves the hindlimbs supporting most of the body weight with one or both of the forelimbs above the head (Figure 6.6).

The mangabey’s location within the tree was recorded to determine which postural behaviors are used in different areas of the tree (McGraw, 1996a). Trees were divided into 5 zones and the ground was considered a separate zone (0). This provides an estimate of position within or around a tree. Support size (bough, branch, twig) was also noted for each posture. Refer to chapter 5 for definitions of the tree zones and support types (see also figure 5.14).

Vegetation Sampling

In order to determine the densities and distributions of tree species in Sentier

Nature and compare habitat types, 13- 100m x 10m vegetation transects were placed along the 3 main trails (see Chapter 2). A total of 1.3 ha were surveyed by the vegetation sampling. The diameter at breast height and height (meters) were taken for all trees and lianas within each transect. The results of the vegetation transects are presented in Chapters 2 and 4.

355

6.6 Data Analysis