SOCIAL ORGANISATION AND ECOLOGICAL BASIS
FOR SUPERGROUP FORMATION IN
RWENZORI COLOBUS
Alexandra Courtney Miller, BSc (Hons)
This thesis is presented for the degree of
Doctor of Philosophy of the University of Western Australia
School of Human Sciences
Anatomy and Human Biology
2019 THESIS DECLARATION
I, Alexandra Courtney Miller, certify that:
This thesis has been substantially accomplished during enrolment in the degree.
This thesis does not contain material which has been accepted for the award of any other degree or diploma in my name, in any university or other tertiary institution.
No part of this work will, in the future, be used in a submission in my name, for any other degree or diploma in any university or other tertiary institution without the prior approval of
The University of Western Australia and where applicable, any partner institution responsible for the joint-award of this degree.
This thesis does not contain any material previously published or written by another person, except where due reference has been made in the text.
The work(s) are not in any way a violation or infringement of any copyright, trademark, patent, or other rights whatsoever of any person.
The research involving animal data reported in this thesis was assessed and approved by The
University of Western Australia Animal Ethics Committee. Approval #: RA/3/100/1468
The work described in this thesis was funded by ‘Research group: GRUETER,’ project grant number: 10301036, Primate Conservation Inc. and the Postgraduate Student Association of the
University of Western Australia
This thesis contains published work and/or work prepared for publication, some of which has been co-authored.
Signature: Alexandra C Miller
Date: 26/08/2019
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ABSTRACT
Primates display a wide variety of social systems. A few primate species form “supergroups” which are shaped by a range of social and ecological selective pressures. Some supergroups of primates are socially organised into multilevel societies composed of multiple discrete social units nested within a larger social matrix. A characteristic of multilevel societies is that the higher levels can include hundreds of individuals. Among primates thus far, these societies have been observed in only a few taxa. In the high-altitude, mountainous forest of Nyungwe
National Park, Rwanda, Rwenzori black-and-white colobus (Colobus angolensis ruwenzorii) form supergroups and were hypothesised to exhibit multilevel social organisation. This conjecture is based on similarities to Chinese snub-nosed monkeys in terms of large group size, montane habitat and seasonal consumption of lichen. Previous studies on the habituated supergroup have investigated the diet, activity and ranging patterns of the Rwenzori colobus.
Here I present the first data on the ‘anatomy’ of a supergroup numbering 500+ individuals.
This study aims to 1) determine the social organisation of the supergroup (multi-male, multi- female, vs multilevel), 2) examine the extent to which members of this group experience direct and indirect feeding competition, and 3) quantify the resource requirements of the supergroup, with a particular focus on the use of fallback foods during periods of preferred food scarcity.
Rwenzori colobus were observed over a period of 13 months in 2016 and 2017. I extracted the social network structure from the time-stamped spatio-temporal distribution of passing individuals in a travelling progression identified to age-sex class. Core multi-male units
(MMUs) with a mean of 1.73 adult males and 3.11 adult females, as well as one-male units, all-female units and bachelor units composed of adult and sub-adult males made up the substructure of the supergroup. In addition, proximity scans showed that adult males were in proximity to other adult males and sub-adult males more often than expected by chance, and
III close-proximity resting clusters contained a mean of two adult-males. These results suggest that the Rwenzori colobus exhibit an internally sub-structured multilevel society with predominantly MMU core units as well as some one-male units (OMUs). This pattern differs from that observed in other nonhuman primates forming multilevel societies such as snub- nosed monkeys (Rhinopithecus spp.), geladas (Theropithecus gelada), Guinea baboons (Papio papio) and hamadryas baboons (Papio hamadryas).
Due to the large group size of over 500 individuals, the Rwenzori colobus supergroup presents an opportunity to investigate the ecological preconditions underlying supergrouping. I used the patch depletion method to study feeding competition, comparing intake rate with movement rate in food patches. The colobus exhibited within-band scramble competition over young leaves, but not over mature leaves or fruit. Moreover, larger groups were able to occupy food patches for longer than smaller groups, indicating between-group contest for food patches.
These findings suggest it may be the lack of competition for high-quality mature leaves, or the abundant lichen, that allows the formation of supergroups.
Lastly, I investigated how the Rwenzori colobus supergroup responds to periods of resource scarcity. Specifically, I compared preferred food availability with consumption of potential fallback foods. Fruticose lichen (Usnea sp.) contributed >50% of the diet in months when preferred foods were less available, suggesting that these lichens constitute a fallback food for
Rwenzori colobus supergroups. However, in a number of other montane forests in Burundi and
Tanzania with similar tree species as well as fruticose lichen, Angolan colobus form small groups suggesting that lichen and high-quality leaves may create a resource base necessary to support colobus supergroups, but factors such as forest size, fragmentation, degradation and hunting by humans may impact group sizes.
IV
Table of Contents
THESIS DECLARATION II
ABSTRACT III
CONTENTS V
LIST OF FIGURES X
LIST OF TABLES XII
ACKNOWLEDGEMENTS XIV
AUTHORSHIP DECLARATION XVIII
CHAPTER ONE: General Introduction...... 1
Social organisation of colobines...... 2
Angolan colobus...... 3
High elevation colobines...... 4
Multilevel societies: Hierarchical structuring...... 5
Case study: Hamadryas baboons...... 6
Case study: Geladas...... 7
Case study: Snub-nosed monkeys...... 7
Evolution of multilevel societies...... 8
Bachelor threat...... 9
Fission-fusion...... 10
Cultural transmission...... 12
Ecological conditions needed for supergroup formation...... 12
Thesis objectives and organisation...... 15
Project significance...... 16
V
CHAPTER TWO: Structure of a supergroup: A multilevel society containing multi-male units...... 18
Abstract...... 19
Introduction...... 19
Methods...... 24
Data collection...... 24
Progressions...... 25
Proximity scans...... 25
Data analysis...... 26
Social network data...... 26
Selecting an optimal window size...... 27
Proximity scans: Nearest neighbour...... 30
Proximity scans: Close-proximity resting...... 30
Results...... 31
Group size and composition...... 31
Social organisation...... 31
Distribution of unit sizes...... 34
Networks...... 35
Nearest neighbour...... 37
Proximity indices...... 39
Close-proximity resting...... 40
Discussion...... 40
Supplementary data...... 47
VI
CHAPTER THREE: Feeding competition inferred from patch depletion...... 52
Abstract...... 53
Introduction...... 54
Methods...... 59
Study site...... 59
Study species...... 59
Patch depletion method...... 60
Data analyses...... 61
Patch depletion...... 61
Patch level variables...... 62
Results...... 62
Patch descriptors, consumption and group sizes...... 62
Testing for within-group scramble competition: patch depletion method...... 64
Dietary switching...... 66
Group size and patch occupancy...... 67
Between-group contest...... 68
Discussion...... 69
CHAPTER FOUR: Diet and use of fallback foods by Rwenzori colobus: Implications for supergroup formation...... 74
Abstract...... 75
Introduction...... 75
Methods...... 79
Study site and species...... 79
VII
Observational data collection...... 82
Phenological monitoring and vegetation sampling...... 82
Food availability index...... 83
Data analysis...... 85
Diet description...... 85
Diet seasonality...... 85
Preferred and fallback foods...... 85
Results...... 86
Phenological patterns...... 86
Diet description...... 87
Seasonal variation in dietary composition...... 90
Preferred and fallback foods...... 91
Discussion...... 96
Supplementary data...... 101
CHAPTER FIVE: General discussion and conclusions...... 105
Summary of thesis aims and findings from each chapter...... 106
Chapter Two: Social structure...... 107
Chapter Three: Supergroup formation in the absence of feeding competition...... 108
Chapter Four: Ecological basis for supergroup formation...... 109
Supergroups: Habitat or taxon specific?...... 109
Future directions: Multilevel societies...... 112
Defining multilevel societies...... 112
Multilevel and fission-fusion...... 113
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Are multilevel societies socially complex environments?...... 114
Conclusions...... 116
Summary...... 117
REFERENCES...... 119
IX
List of Figures
Figure 2.1: A hypothetical sequence of time-stamped passing individuals...... 29
Figure 2.2: Box plot for sizes (number of individuals) of mixed-sex units of Rwenzori colobus (n=261)...... 34
Figure 2.3: Frequency distribution for unit sizes (n=294) of Rwenzori colobus resulting from the network approach and Louvain clustering...... 35
Figure 2.4: Progression capturing 141 individuals on 17-08-2017...... 36
Figure 2.5: A multi-male unit with three adult males, six adult females, two juveniles, one infant and three unidentified individuals surrounding them...... 37
Figure S2.1: Map of Nyungwe National Park indicating locations and sizes of sighted unhabituated groups of Rwenzori colobus (not the followed supergroup)...... ……. 48
Figure S2.2: Plot of the F statistic for k-means analysis against cluster number for the data on unit size for Nyungwe National Park...... 49
Figure S2.3: Clustering within each window network, for a single progression of Rwenzori colobus monkeys recorded on 20-07-2017...... 50
Figure S2.4: Network divided into sub-networks by window network...... 51
Figure 3.1: Box plot for intake rate (bites/min) of different food types consumed by Rwenzori colobus in patches. Number of 1-minute observations per food category: 1) young leaves, 2) mature leaves, 3) fruit, 4) flower parts, and 5) lichen ...... 64
Figure 3.2: Changes in intake rate (bites/min) and distance moved (m/3 min) between first (start) and last quarter (end) of patch occupancy for: all patches combined, young leaves, mature leaves and fruit for Rwenzori black-and-white colobus in Nyungwe National Park, Rwanda...... 65
Figure 4.1: Map of Rwanda (right) and Nyungwe National Park (left) by K. Meisterhans and C. C. Grueter; adapted from Nyungwe National Park Management Plan 2012-21...... 81
Figure 4.2: Monthly variation of temperature at rainfall at Nyungwe National Park, Rwanda, between July 2016 and August 2017...... 81
X
Figure 4.3: Availability of mature leaves, lichen, young leaves, fruit, and flower parts, for tree species eaten by Rwenzori black-and-white colobus in Nyungwe National Park...... 87
Figure 4.4: The percentage of monthly diet feeding on lichen, fruit, leaves and other (flower parts, herbaceous vegetation, bark, clay, dead wood, epiphytes); data based on scans...... 91
Figure 4.5: Seasonality in the time spent feeding on important species/plant parts from September 2016 to August 2017...... 94
Figure 4.6: a) Consumption of lichens in relation to availability of preferred food for Rwenzori
colobus in Nyungwe; Pearson correlation between FAIPREF and the percentage of monthly consumption of fruticose lichen, and b) Rwenzori colobus feeding on bunches of the hair-like fruticose lichen (Usnea sp.)...... 95
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List of Tables
Table 2.1: Composition of mixed sex groups, male-only groups, and female-only groups and mean number of all age-sex classes within groups...... 33
Table 2.2: Chi square tests comparing observed to expected proximity records for adult Rwenzori colobus with other age-sex classes as their nearest neighbour (≤5 m) when the group not travelling (rest, feed, forage, move, vigilant, groom, play, mate, aggress)...... 38
Table 2.3: Chi square tests comparing observed to expected proximity records for adult Rwenzori colobus with other age-sex classes as their nearest neighbour (one nearest neighbour per scan) when the group is travelling...... 39
Table 2.4: Proximity indices (PI) for adult males and adult females with other age-sex classes as their nearest neighbour (≤5 m) (one nearest neighbour record per scan)...... 39
Table 2.5: Number of each age/sex class individuals participating in 148 close-proximity resting clusters (n=148)...... 40
Table S2.1: Age-sex class of individuals...... 47
Table 3.1: Tree species constituting feeding patches, number of patches per tree species and plant parts consumed per tree species by Rwenzori colobus during feeding events.... 63
Table 3.2: Changes in mean (x) intake rate (bites/min) and mean (x) distance moved (m/3 min) between first (start) and last quarter (end) of patch occupancy for: all patches combined, young leaves, mature leaves and fruit for Rwenzori black-and-white colobus in Nyungwe National Park, Rwanda...... 66
Table 3.3: Differences in the composition of food items during the 1st compared to the 4th quarter of the patch occupancy period for different dietary items: young leaves, mature leaves, fruit, lichen, and flower parts...... 67
Table 3.4: LMM investigating the effect of mean group size and food availability (DBH) on patch feeding time (minutes) in Rwenzori colobus in food patches...... 67
Table 3.5: LMM investigating the effect of mean feeding group size and food availability (DBH) on patch feeding time (minutes) in Rwenzori colobus in food patches...... 67
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Table 3.6: LMM investigating the effect of mean group size and food availability (DBH) on patch occupancy time (minutes) in Rwenzori colobus in food patches...... 68
Table 3.7: LMM investigating the effect of mean feeding group size and food availability (DBH) on patch occupancy time (minutes) in Rwenzori colobus in food patches...... 68
Table 4.1: Annual consumption (% of feeding scans) of all species consumed during scans, ranked most to least consumed...... 88
Table 4.2: Important species in Rwenzori colobus diet...... 93
Table 4.3: Pearson correlation matrix comparing availability of plant parts and consumption of potential fallback foods by Rwenzori colobus...... 87
Table S4.1: Diet of C. angolensis at Nyungwe and other sites………………………...... … 101
Table S4.2: The food item preference ranks for all plant parts consumed by Rwenzori colobus; monthly percentage in the diet, average diet and availability rank, number of months in which they were consumed and average preference rank (most preferred to least preferred)...... 102
Table S4.3: Phenological availability and consumption of preferred food parts...... 104
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ACKNOWLEDGEMENTS
Cyril Grueter thank you for giving me the opportunity to conduct this research in the beautiful country of Rwanda. It has been extremely beneficial working with a researcher who has such a wealth of experience in field-based research. Thank you for your supervision. It was great to be a part of your Lab.
Debra Judge thank you for your supervision during my PhD and providing advice throughout.
You provided me with valuable feedback on conference presentations and writing, which improved the quality of my work.
This fieldwork would not have been possible without the wonderful “Team Colobus”. Grace
Uwingeneye you were an excellent companion throughout this project from beginning to end and assisted in so many different aspects of the research and day-to-day activities. It was great to have a teammate who shares a passion for conservation and research. Best of all you are a true friend and ‘Rwandan sister’. You certainly enriched my time in Rwanda. Thank you to
Dieudonne Ndayishimiye for your hard work in the field, and for your extensive knowledge of plant species and colobus. We learned a lot together, spending many hours huddled under a single umbrella, surviving swarms of biting insects, getting lost, and walking hundreds of kilometres along the trails of Nyungwe National Park. Our time was further enriched by the great music playing on your mobile! Thank you also to Fidele Muhayayezu for the generous assistance with plant species identification and training of research assistants, and also for dropping off mandazis and papayas at 4 am. Thank you to Sara, Epiphany, Adelphine and
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Saratierre, and especially Nshimiye for looking out for us in camp and providing great friendship.
Many thanks to the Rwanda Development Board (RDB) and Rwanda Education Board
(Mineduc) for kindly permitting me to conduct this 13-month study. I am extremely thankful to Antoine Mudakikwa, and the Nyungwe National Park Wardens; Pierre Ntihemuka,
Innocent Ndikubwimana and Kambogo Ildephonse for their continual support and logistical assistance. Your cooperation ensured the success of this project. A big thank you to the fantastic team of RDB colobus trackers for their field support and guiding; Emmanuel, Francis,
Philomen, Simon, Emmanuel, Boston, Sylvester, Gasper, Japhet, Pascal, Venuste, Jack, and Abraham. Thank you to the Wildlife Conservation Society Rwanda team for the cooperation throughout the field period, and to WCS staff member Ferdinand, for assisting us with plant identification and assistance setting up the phenology trails. Thank you also to affiliates at the Center of Excellence in Biodiversity and Natural Resource Management
(CoEB), it was great to connect in Rwanda and receive feedback on conference presentations, and especially to Beth Kaplin for the support in Rwanda and providing feedback on manuscripts.
I was fortunate to be joined in the field by a number of great research assistants and interns throughout the project. Thank you to Reduine Mukamazimpaka, Evariste Ahishakiye and
Frank Dush. A very special mention to Tite Tuyisingize. You are a wonderful person and researcher. Thank you for joining the project in the last month to assist with colobus research and habitat survey. Also to Ash Miller and Kevin Kalani for joining me in the forest for a
XV number of months and enduring the early mornings, stinging plants, rain, golden showers of monkey pee and vertical slopes. You were a fantastic addition to the team.
I am grateful for the financial support provided by an Australia Government Research Training
Program (RTP) Scholarship, University of Western Australia, and UWA Postgraduate Student
Association, and for the project funding provided by the School of Human Sciences. I also gratefully acknowledge funding from Primate Conservation Inc., and thank my sponsors
CooperVision, Southern Tarpaulins, SteriPen, Qatar Airways and Osprey for their generous contribution of equipment.
Thank you to the Office of Research Enterprise staff at the University of Western Australia for coordinating and promoting a Chuffed Crowdfunding Project. I thank the following for contributing to the crowdfunding project: Fariba Ahmadi, Lucy Barrett, Roberta Bencini,
Laura, Grant & Indi Booth, Robert Bouwer, Greg Brindle, Kirsten Bruce, Rosalyn Bruce,
Aimee Chapman, Amanda Coad, Sue Dardis, Kyle Douglas, Judy Elswothy, Deborah Evans,
Matt Genevieve, Cathy Greatrex, Lucas Harris, Cassie Haselhurst, Layli & Thomas Hosking,
Toni Jones, Shamim Kasiri, Arash, Felicity & Lily Kalani, Ghodrat Kalani, Nasrin and
Ardeshir Kalani, Alexandra Kirkby, Shirley Landquist, Peta, Ben, Georgia, Molly & Declan
Lockwood, Julie Matthews, Leon Mauger, Ron McCathie, Vicki McGrath, Ashlyn Miller, John
Miller, Kelly Miller, Michele Miller & John Wright, Peta Miller, Jonathon O’Donnell David
O’Connor, Jonathon O’Donnell, Stephanie O’Sullivan, David Piggott, Mark Queern, Janet
Renner, Anne Robinson, Zarinne Seow, Warwick Smith, Alex Taucher, Kimia Tajoldini &
Elliott Tilbury, Kathleen Tucker, Hannah Uren, Penny Wong, Gunvor Velure, Ilan Warchivker,
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Connor Weightman, Margaret Woodall-Bond and anonymous contributors. Your support of the project early on was a tremendous help.
Thank you to the Bioanthropology lab group including, Jaya Matthews, Samantha Green,
Melanie Mirville, Tash Coutts, Phoebe Spencer, Chiara Sumich, Jen Hale, Kathy
Sanders, Debra Judge and Cyril Grueter, for providing feedback on presentations throughout. A big thanks to Jaya and Samantha, it has been great sharing an office during the writing phase, celebrating, commiserating, and sharing stories has helped boost morale. I also thank Denise Murphy for the support before and during field-work.
And last but not least to my friends and family for the continual support throughout this challenging chapter. Thank you to Alex (+ bub Grace) and Hannah for advice, hugs and encouragement shared over cinnamon buns and coffee. Mum and Dad thank you for so much support over the years, and for joining me in the field to see what this colobus stuff was all about. I always knew you were there when I needed it. Thanks to my sister Ash, for joining me for a few months in the forest, trekking over countless mountains, enduring mice in the tent and bringing Nutella to camp. It was so much fun with you there! Biggest thanks to my wonderful husband Kevin. You were a rock throughout my entire PhD, I am so thankful for your encouragement to follow my dreams, heading into the forests of Africa for the second time. It was a blast having you join me in the forest for a few months. You were a great scribe, made some fab alterations to camp, shared my passion for Akabanga chilli oil on beans and helped create some great memories.
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AUTHORSHIP DECLARATION: CO-AUTHORED PUBLICATIONS
This thesis contains work that has been submitted or prepared for publication.
Details of the work: The structure of a supergroup: Rwenzori black-and-white colobus (Colobus angolensis ruwenzorii) form a multilevel society containing multi-male units Location in thesis: Chapter Two Student contribution to work: The candidate and Cyril Grueter designed the study. The candidate collected the data in the field over a 13-month period in Nyungwe National Park in 2016-2017. The candidate and Shahadat Uddin collaborated to select optimal window sizes for the 40 progressions analysed using the two-step method described in the manuscript. The candidate applied the subsequent clustering algorithm on the resulting dataset, and created the network diagrams in Gephi. The section ‘Proximity scans: Nearest neighbour’, and ‘Proximity scans: Close-proximity resting’ were analysed by the candidate. The candidate wrote the paper. Cyril Grueter, Debra Judge and Beth Kaplin provided feedback on the writing. Co-author signatures and dates:
Cyril Grueter: 02/07/19
Debra Judge: 03/8/19
Shahadat Uddin:
Beth Kaplin: 27/07/2019
Details of the work: Feeding competition inferred from patch depletion in supergroups of Rwenzori black-and- white colobus monkeys (Colobus angolensis ruwenzorii) in Rwanda Location in thesis: Chapter Three Student contribution to work: The candidate and Cyril Grueter designed the study. The candidate collected the data in the field in Nyungwe National Park in 2016-2017. The candidate analysed the data and wrote the paper. Cyril Grueter, Debra Judge and Beth Kaplin provided feedback on the writing. Co-author signatures and dates:
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Cyril Grueter: 02/07/19
Debra Judge: 03/8/19
Beth Kaplin: 27/07/2019
Details of the work: Seasonal importance of lichen to a supergroup of Rwenzori colobus (Colobus angolensis ruwenzorii) in Rwanda Location in thesis: Chapter Four Student contribution to work: The candidate and Cyril Grueter designed the study. The candidate collected the data in the field in Nyungwe National Park in 2016-2017. The candidate analysed the data and wrote the paper. Cyril Grueter and Debra Judge provided feedback on the writing. Co-author signatures and dates:
Cyril Grueter: 02/07/19
Debra Judge: 03/8/19
Student signature:
Date: 22/08/19
I, Cyril Grueter certify that the student’s statements regarding their contribution to each of the works listed above are correct.
Coordinating supervisor signature:
Date: 02/07/19
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CHAPTER ONE:
GENERAL INTRODUCTION
1
Chapter One: General Introduction
Social organisation of colobines
The colobines are medium-sized primates separated into two groups based on geographical distribution and morphological features: the African Colobinae and the Asian Colobinae. They occupy a wide range of habitats throughout Africa and South and South-East Asia respectively
(Anandam et al. 2013; Oates and Davies 1994; Zinner et al. 2013), including: high-elevation montane (Nijman 2014), limestone hills (Zhou et al. 2013), riverine forest (Matsuda et al.
2010), mangroves and peat swamps (Nowak 2012), arid coastal forest (Nowak and Lee 2013), and human-modified habitats (Moore et al. 2010). They are the only primates that have large multi-chambered sacculated stomachs with symbiotic microbiota specialised for the ruminant digestion of fibrous leaf material such as cellulose (Oates and Davies 1994; Zhou et al. 2014).
In general, the colobines exhibit dietary flexibility, but they are characterised by a more folivorous diet than other primates, including leaves, fruits, flowers, seeds, bark, lichens and invertebrates (Zinner et al. 2013).
Primates, including the colobines, exhibit great social system diversity (Sterck 2012), shaped by food abundance and availability, predation, disease, infanticide, and human activities
(Chapman et al. 2014; Hrdy 1977; Newton 1988; Treves and Chapman 1996; van Schaik and
Hörstermann 1994; Watanabe 1981). The colobines exhibit various forms of social organisation, i.e. the size, composition and cohesiveness of social groups (see Kappeler and van Schaik 2002): 1) one-male, one-female groups, e.g. Siberut langur (Presbytis siberu; Tilson and Tenaza 1976), 2) independent one-male units [OMUs], e.g. Hose’s and grizzled langurs
(P. hosei; Nijman 2010; P. comata; Nijman 2017), 3) larger multimale-multifemale groups
[with one to two males, multiple females and offspring], e.g. red langur (P. rubicunda;
D'Agostino et al. 2016), 4) intermediate modularity (Grueter et al. 2012a), where OMUs
2 aggregate under certain conditions, e.g. golden and capped langurs (Trachypithecus geei;
Mukherjee and Saha 1974; T. pileatus; Stanford 1991), and 5) multilevel or modular organisation, e.g. snub-nosed monkeys (Rhinopithecus spp.; Kirkpatrick and Grueter 2010), and proboscis monkeys (Nasalis larvatus; Matsuda et al. 2010). Multilevel organisation has been documented in three genera of Asian colobines comprising the douc langurs (Pygathrix spp.; Rawson 2009), proboscis monkeys (Yeager 1990) and snub-nosed monkeys (Qi et al.
2014; Zhang et al. 2006), but not in any African colobine. Amongst the African colobines
(Colobini: Colobus, Procolobus and Piliocolobus; Groves 2001), most form one-male/ multifemale groups or multimale/ multifemale groups (Fashing 2001b; Struhsaker 1975).
However, the Rwenzori colobus (Colobus angolensis ruwenzorii), inhabiting forested regions in the Albertine Rift, forms large supergroups (Fimbel et al. 2001), which are predicted to form multilevel societies but further research is required to determine their social organisation
(Fashing et al. 2007a).
Angolan colobus
Angolan black-and-white colobus (Colobus angolensis) are found in Africa and include seven subspecies (C. a. angolensis, C. a. cordieri, C. a. cottoni, C. a. palliatus, C. a. prigoginei, C. a. ruwenzorii, C. a. sharpei), distributed throughout Angola, Democratic Republic of the
Congo, Burundi, Uganda, Rwanda, Kenya and Tanzania (Anderson et al. 2007; Kingdon 2015;
Zinner et al. 2013). Angolan colobus are known to occur in a diverse range of habitats such as montane forest, lowland dry forest, and coral rag forest (Bocian 2013; Dunham 2017; Vedder and Fashing 2002). In Kenya, Angolan colobus are only present in a number of small fragmented forests in the southwestern region of the country (McDonald and Hamilton 2010;
McDonald et al. 2019). Angolan colobus populations exist at sea level and also range in mountainous regions; notably, two subspecies occupy high-altitude areas, the Rwenzori colobus (Vedder and Fashing 2002) and Peters' Angola colobus (C. a. palliatus; McDonald and
3
Hamilton 2010). These high-altitude populations of Angolan colobus occur in a number of forests in Eastern Africa, including Nyungwe National Park in Rwanda, Kibira National Park in Burundi, and Mahale and Udzungwa mountains in Tanzania (Hakizimana 2014; Marshall
2007; Nishida et al. 1981; Vedder and Fashing 2002). The Rwenzori colobus occupying the montane forest of Nyungwe National Park in Rwanda form the largest groups of any black- and-white colobus, moving in a supergroup of over 500 individuals. Rwenzori colobus also occupy other regions in eastern and central Africa (Bocian 2013; Hakizimana 2014; Inogwabini et al. 2000; Nishida et al. 1981), but permanent supergroups are a unique occurrence in
Nyungwe.
High-elevation colobines
Primates living in high-altitude forests face the challenges of occupying a less productive landscape than lower-lying areas. High-altitude forests are characterised by decreased plant and animal density, and scarce or physically or chemically altered resources; for example, smaller, thicker and harder leaves are found at higher altitudes (Bruijnzeel and Veneklaas 1998;
Grow et al. 2013; Richards 1952; Walsh 2005). In Asia, a number of snub-nosed monkey and langur species occupy mountainous regions in the south and central regions of China, and in the Himalayas, ranging from 2,500-3,000 m above sea level, with some species ranging above
4,000 m a.s.l (Nijman 2014). In Africa, two species of black-and-white colobus inhabit high- elevation ranges: the guereza (Colobus guereza), which ranges up to 3,300 m a.s.l in Ethiopia
(Dunbar and Dunbar 1974), and the Angolan colobus in Nyungwe National Park in Rwanda
(1600-2950 m a.s.l), Kibira National Park in Burundi (1,600-2,666 m a.s.l), Kahuzi-Biega
National Park in Democratic Republic of Congo (600–3,308 m a.s.l) and Mahale (1,850-2,350 m a.s.l) and Udzungwa mountains (≤2200 m a.s.l) in Tanzania (Bocian 2013; Hakizimana
2014; Inogwabini et al. 2000; Nishida et al. 1981; Vedder and Fashing 2002). The shared similarities of high-altitude dwelling Angolan colobus in Nyungwe with Chinese snub-nosed
4 monkeys, in terms of large group size, habitat (montane forest) and diet (seasonal lichen consumption) (Grueter et al. 2009b), leads to the prediction that the Rwenzori colobus form multilevel societies (Fashing et al. 2007a).
Multilevel societies: Hierarchical structuring
The terms ‘multilevel’, ‘modular’ or ‘hierarchically structured’ refer to a form of group organisation composed of several discrete social units nested within a larger social matrix of up to several hundred individuals (Fisher and Pruitt 2019; Grueter et al. 2012a; Kummer 1984;
Stammbach 1987). Multilevel societies have been described in a wide range of mammalian taxa, including humans (Homo sapiens; Hamilton et al. 2007; Zhou et al. 2005), African papionins (Papio hamadryas, Papio papio, Theropithecus gelada; Fischer et al. 2017; Schreier and Swedell 2009; Snyder-Mackler et al. 2012b), Asian colobines (Nasalis larvatus,
Rhinopithecus spp., Pygathrix nigripes; Grueter et al. 2017a; Kirkpatrick and Grueter 2010;
Yeager 1992), elephants (Loxodonta africana, Elephas maximus; De Silva and Wittemyer
2012; Wittemyer et al. 2005b), giraffes (Giraffa camelopardalis; VanderWaal et al. 2014), prairie dogs (Cynomys ludovicianus; Hoogland 1995), equids (Equus hemionus, Equus burchelli; Feh et al. 2001; Rubenstein and Hack 2004), and cetaceans (Orcinus orca, Physeter macrocephalus, Tursiops spp.; Cantor et al. 2012; Connor et al. 1992; Tavares et al. 2017;
Whitehead et al. 2012). ‘Core units’ represent the lowest level of social organisation, and in some taxa additional organisational tiers also exist between the core unit layer and the larger band. These additional tiers are taxon-specific, such as clans in hamadryas baboons, which are modules of associated units that exhibit spatiotemporal cohesion for periods when the larger band cleaves into smaller entities (Schreier and Swedell 2009; Städele et al. 2015).
Multilevel societies within the order Primates were first described by Kummer (1968) when studying an African papionin, the hamadryas baboon (Papio hamadryas) which inhabits the
5 sparse grasslands of Ethiopia. A common feature among multilevel societies is the extremely large number of individuals, often forming supergroups of hundreds of individuals, and up to
1000 individuals in the case of the gelada herds in the highlands of Ethiopia (Mac Carron and
Dunbar 2016; Snyder-Mackler et al. 2012b). Different nonhuman primate multilevel societies also differ in intra-unit bonding patterns and philopatry (Matsuda et al. 2012). The following three subsections describe case studies detailing the 1) ecological functions of hierarchical layers, and 2) patterns of association among core unit members, in the three most exhaustively studied primate multilevel society forming species/genus: hamadryas baboons, geladas, and snub-nosed monkeys.
Case study: Hamadryas baboons
Hamadryas baboons exhibit a multilevel structure across their range in Eritrea, Ethiopia,
Yemen and Saudi Arabia, with the OMU, band and troop recorded at all sites studied (Al-
Safadi 1994; Kummer 1968; Swedell 2002b, 2002a; Zinner et al. 2001a, 2001b). However, the clan level, lying between the OMU and band, has been recorded only at Erer-Gota and Filoha,
Ethiopia (Abegglen 1984; Schreier and Swedell 2009; Sigg et al. 1982). Different functions have been attributed to the hierarchical layers in hamadryas baboons; the OMU represents the primary reproductive unit (Schreier and Swedell 2012), the clan serves as a cooperative entity linked by male relatedness and a functional group during temporary or permanent group fissioning (Abegglen 1984; Schreier and Swedell 2012), the band is an ecological unit that has evolved to reduce predation risk and facilitate resource defence (Abegglen 1984; Kummer
1968; Schreier and Swedell 2012), and troops are aggregations at localised sleeping cliffs
(Schreier and Swedell 2009). Within the one-male unit, females are non-philopatric, do not form dominance hierarchies, and are generally weakly bonded (Kummer 1968; Swedell 2002a;
Swedell 2006). Males remain in their natal OMU (Sigg et al. 1982; Swedell et al. 2011) and forcibly transfer females within the band via overt aggression or abduction methods (Pines and
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Swedell 2011; Swedell et al. 2011). Bands also contain follower and solitary males, which are often sub-adult or young adult males that are affiliated with a particular OMU (Chowdhury et al. 2015; Pines et al. 2011).
Case study: Geladas
Geladas form multilevel societies across their range encompassing the Simien Mountains, Bole
Valley and Arsi (Mori et al. 1999; Ohsawa and Dunbar 1984). Their multilevel society is composed of the OMU or reproductive unit (Crook 1966), team, band (Dunbar and Dunbar
1975; Snyder-Mackler et al. 2012b), herd (Kawai and Iwamoto 1979), and community. Based on evidence of limited recognition between individuals at the band level, it has been suggested that the community layer may not be socially motivated, but an aggregation of individuals that end up in proximity due to predator threat or limited sleeping sites (Bergman 2010). Gelada females are philopatric, and exhibit linear and stable dominance hierarchies within units (le
Roux et al. 2011; Snyder-Mackler et al. 2014). In addition, although units may include two adult males, only one is reproductively active (Dunbar and Dunbar 1975; Snyder-Mackler et al. 2012a).
Case study: Snub-nosed monkeys
The snub-nosed monkeys (Rhinopithecus spp.) inhabiting China, Vietnam and Myanmar consist of five species: one lowland species in Vietnam, the Tonkin snub-nosed monkey (R. avunculus), three species inhabiting montane regions of China, the Guizhou snub-nosed monkey (R. brelichi), the Sichuan snub-nosed monkey (R. roxellana), black-and-white snub- nosed monkey (R. bieti; Kirkpatrick 1995), and one species inhabiting montane forests bordering Myanmar and China, the black snub-nosed monkey (R. strykeri; Geissmann et al.
2011; Liedigk et al. 2012; Ma et al. 2014; Yang et al. 2018). All snub-nosed monkeys exhibit multilevel social organisation (Chen et al. 2015; Kirkpatrick and Grueter 2010). Most studies
7 on snub-nosed monkeys have described only two levels of social organisation: the OMU and the band (R. bieti; Grueter et al. 2017a; R. roxellana; Zhang et al. 2006). However, Qi et al.
(2014) report social tiers above the band level, a supra-band structure of the golden snub-nosed monkeys multilevel society known as the ‘troop’, composed of spatially proximate bands, and also a ‘herd’ layer, containing reproductive units and non-reproductive units. However, field- based observational data on individual interactions among different tiers are needed to validate these proposed definitions. The OMUs leader males nested within the band have also been shown to exhibit a linear dominance hierarchy (Zhang et al. 2008). Despite both sexes dispersing from the natal OMU upon maturity (Chang et al. 2014; Guo et al. 2015), female kin bonding within OMUs is facilitated by occupancy of the same natal OMU or females’ decisions to transfer to units with kin relatives (Guo et al. 2015), and males disperse further and more frequently between bands than do females (Chang et al. 2014).
Evolution of multilevel societies
In nonhuman primates, the evolution of multilevel societies is hypothesised to have arisen through two different pathways in the papionins and the colobines (Grueter et al. 2012a), via the Fission Model [papionins], and the Fusion Model [colobines] (sensu Qi et al. 2014).
Papionin multilevel societies most likely evolved from the breakup of ancestral multi-male, multi-female groups into smaller units under harsh conditions facilitating more efficient foraging (Bercovitch 1990; Dunbar 1983, 1988b; Dunbar 1988a; Jolly 2009), and/or the benefits of male protection from harassment may have favoured substructuring (Grueter et al.
2012a). However, colobine multilevel societies are thought to be evolved through fusion/amalgamation of ancestrally independent OMUs (Grueter and van Schaik 2010; Qi et al. 2014). The Fusion Model, involving an aggregation of separate units into a larger band, has been explained by several hypotheses: 1) The bachelor threat hypothesis (Grueter and van
Schaik 2010), 2) the predator defence hypothesis (Zhang et al. 1999), and 3) the inbreeding
8 avoidance hypothesis (Zhang et al. 2012). In the following subsections, I discuss three evolutionary hypotheses explaining the formation and maintenance of multilevel societies: 1) bachelor threat, 2) fission-fusion and 3) cultural transmission.
Bachelor threat
The main lines of evidence for the bachelor threat hypothesis are that all-male units (AMUs) are almost always present in multilevel societies (Kirkpatrick 1998; Yeager 1990), an overthrow of dominant males is often accompanied by infanticide (Agoramoorthy and Hsu
2005), the presence of bachelor males incited aggression from dominant males (Grueter and van Schaik 2010), and when bachelor presence is high, unit association increases and within- band cohesion is more likely (Grueter and van Schaik 2010). Bachelor males forming AMUs function as ‘social predators’ in primate societies including – amongst others – geladas, hamadryas baboons, and snub-nosed monkeys (Beehner and Bergman 2008; Dunbar and
Dunbar 1975; Grueter and van Schaik 2010; Pappano et al. 2012), and are hypothesised to be a shaping force forming multilevel societies (Grueter et al. 2012a; Qi et al. 2017; Rubenstein
1986). Bachelor males are subadult and adult males not associated with a one-male unit
(OMU), and are typically members of an AMU (Grueter et al. 2012a; Pappano et al. 2012).
Bachelor males pose two direct types of threats to the fitness of breeding individuals: (1) they may replace the dominant breeding male, effectively ending his reproductive tenure, and (2) they may commit infanticide, reducing the fitness of breeding males and females (Hrdy 1977).
To mitigate this cost, breeding males associate and form coalitions to avoid harassment, cuckoldry, risk of take-over and infanticide from unattached bachelor males (Qi et al. 2017;
Rubenstein and Wrangham 1986; Xiang et al. 2014). For example, at Shennongjia Nature
Reserve, central China, co‐operation was observed among males of different OMUs, in the form of coordinated chasing, joint vigilance, and patrolling behaviour directed at lone bachelor males trying to enter an OMU (Xiang et al. 2014).
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Fission-fusion
During the Pliocene, a period of progressively drying conditions and contraction of forest habitat, the theropithecines and hominins independently dispersed into open savanna habitat
(Campbell 1979; Jolly 1972; Reed and Rector 2007; Sponheimer and Lee-Thorp 2003). Rather than aggregating in permanently large groups, residential groups of hunter-gatherers dispersed and re-aggregated over time (Binford 1980; Grove 2009; Grove et al. 2012; Layton and O’Hara
2010), and it is theorised that fission-fusion evolved early on in the course of human evolution
(Aureli et al. 2008). Limited resources often force hominid groups to fission and radiate widely to efficiently forage (Lee 1972). In nomadic !Kung hunter-gatherer societies inhabiting the arid
Kalahari desert, families converge at water holes during the dry season before splitting and radiating widely during the wet season (Lee 1972). This has also been observed amongst
Australian Western Desert Aboriginal groups, clustering around water holes in times of drought
(Gould 1969). This nomadic sequence is remarkably similar to that of nonhuman primates such as the hamadryas baboons sharing communal sleeping cliffs before fissioning out in smaller groups during the day to feed and later converging at water sources (Schreier and Swedell
2012).
All multilevel primate societies display fission-fusion dynamics (Aureli et al. 2008; Kirkpatrick et al. 1999; Majolo et al. 2018; Nie et al. 2009; Qi et al. 2014; Schreier and Swedell 2012;
Snyder-Mackler et al. 2012b), and there is a continuum of the frequency of such events; more frequent in some taxa, or species, than others (Kirkpatrick and Grueter 2010). Fissioning adjusts group size with diminished food availability and reduces feeding competition, a behavioural strategy which allows animals to exploit the benefits of group living with reduced costs (Aguilar-Melo et al. 2018; Asensio et al. 2008; Chapman et al. 1995; Kummer 1971).
Multilevel societies exhibit fluidity in group size, aided by the natural fissure points surrounding stable core units [and at higher levels such as the clan], which allow multilevel
10 societies to fission and coalesce, and maximally exploit fluctuating resources, dispelling the costs of group living (Aureli et al. 2008; Korstjens et al. 2006; Kummer 1968; Kummer 1971;
Lehmann et al. 2007; Schreier and Swedell 2012). By employing fission-fusion, primates can form larger groupings that are reproductively viable (Korstjens et al. 2006; Lehmann et al.
2007). Societies displaying fission-fusion dynamics are generally considered to be socially complex as the social landscape is dynamic, with group composition changing on an hourly or daily basis, thus increasing the number of ‘random’ interactions requiring social knowledge
(Connor et al. 2000; Marino 2002). However, multilevel societies [with stable subgroup membership] may be ‘simpler’, with evidence suggesting that mutual assessment strategies
[that don’t require social knowledge, e.g. badge of status for the core males] are employed in multilevel societies as opposed to the required social knowledge of individuals (Benítez et al.
2017; Koda et al. 2018).
Species exhibiting multilevel social organisation often inhabit harsh or unpredictable environments, e.g. snub-nosed monkeys exploit temperate forests that experience severe winters with low food availability, and hamadryas baboons inhabit semi-desert habitats in northern Africa experience harsh conditions with sparse resources (Kummer 1968; Swedell et al. 2011; Zinner et al. 2001a). In the Filoha region of Ethiopia, seasonally abundant doum palm fruit lead to bigger bands of hamadryas baboons than observed at other sites (Abegglen 1984;
Al-Safadi 1994; Biquand et al. 1992; Kummer et al. 1981). This seasonally abundant fruit results in large fluctuations in groups size on a temporal scale; however, during low resource periods with only Acacia thorn shrubs to eat, the large bands fission into clans, a social grouping layer only present at this site (Schreier and Swedell 2009; Swedell 2002b; Swedell et al. 2008). Fissioning into smaller subgroups may also be linked to the availability of a high- quality seasonal food source; for example, a snub-nosed monkey band split into subgroups to exploit young bamboo shoots in Yunnan, China (Ren et al. 2012). The spatial cohesion of
11 subgroups within different multilevel societies varies, and low cohesion facilitated by fission- fusion may ensure more efficient foraging (Asensio et al. 2008). For example, some species such as hamadryas baboons may be separated by several kilometres throughout daily foraging and reconvene at sleeping cliffs (Stammbach 1987).
Cultural transmission
An alternate scenario is that multilevel societies can arise via cultural transmission (Cantor et al. 2015). Culture is recognised as socially-learned behaviours that are shared within subgroups of a population persisting over time (Cantor et al. 2019). Culture can shape social organisation by predisposing individuals to a shared likeness or identity (Cantor and Whitehead 2013). The formation of multilevel societies of whales (Physeter macrocephalus) in some oceans (but not others) is attributed to predation, resources, anthropogenic effects and culture (Whitehead et al. 2012). Cantor et al. (2015) propose that social learning biases and maintains localised communication signals. Whales use linguistic differentiation to maintain social segregation within the structure of their multilevel social organisation, with units interacting most with those who share their vocal dialect (Cantor et al. 2015; Gero et al. 2016; Van Cise et al. 2018).
This phenomenon is functionally similar to that in humans wherein social boundaries are formed based on culture, with language assisting in delineating these boundaries (Barth 2010;
Nettle and Dunbar 1997).
Ecological conditions needed for supergroup formation
Amongst primates large group size is rare, with groups of over 200 members recorded in few taxa: humans (Homo sp.; Aiello and Dunbar 1993; Hill and Dunbar 2003), hamadryas baboons
(Papio hamadryas; Kummer 1984), Guinea baboons (Papio papio; Fischer et al. 2017;
Sharman 1981), geladas (Theropithecus gelada; Dunbar 1984), mandrills (Mandrillus sphinx;
Abernethy et al. 2002), drills (Mandrillus leucophaeus; Gartlan 1970), snub-nosed monkeys
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(Kirkpatrick and Grueter 2010), and Rwenzori black-and-white colobus (Fashing et al. 2007a).
A range of factors influence primate group sizes, including feeding competition (Teichroeb and
Sicotte 2009), resource base (Chapman et al. 1995), predation (Struhsaker 2000), hunting pressure by humans (Hadi et al. 2009; Watanabe 1981), logging history (Struhsaker 1997), forest type (Dunbar 1987), forest degradation (Mbora et al. 2009), and infanticide (Chapman and Pavelka 2005). Grouping occurs when the benefits of aggregating outweigh the costs of close proximity with conspecifics (Alexander 1974; Krause and Ruxton 2002; Markham et al.
2015). Supergroups are the extreme form of grouping, facilitated by a range of ecological factors in primates (Dunbar 1992b; Grueter et al. 2012a; Swedell and Plummer 2012). Living in a large group is costly, and, according to the ecological constraints hypothesis, travel time/distance is the key constraint on group size (Chapman and Chapman 1996, 2000a;
Chapman and Pavelka 2005; Gillespie and Chapman 2001). Larger primate groups travel further per day, and generally spend more time feeding than do smaller groups (Majolo et al.
2008) because feeding competition increases with increasing group size (Isbell 1991; Janson and van Schaik 1988). Thus, ecological preconditions for large group size include an abundant resource base and relaxed feeding competition (Dunbar 1992a; Grueter et al. 2012a; Swedell and Plummer 2012). In the case of hamadryas baboons at Filoha in Ethiopia, it was the presence of an abundant food source (i.e. doum fruits) which allowed for larger group sizes compared to other sites (Schreier and Swedell 2012). The wide temporal and spatial availability of this staple food resource reduced the ecological costs of grouping, allowing for the formation of supergroups (Grueter et al. 2012a).
The Cody/Altmann harvest efficiency model (Altmann 1974; Cody 1971; Rodman 1988) suggests that feeding as a group, as opposed to numerous separate entities, increases overall feeding efficiency by minimising the re-visitation of already depleted patches. This explains the tendency of large group associations (Terborgh 1983). However, in the case of a multilevel
13 supergroup, large numbers of associated subunits travelling in close proximity would likely increase the chance of units crossing feeding paths, offsetting the proposed benefits of preventing visits to depleted patches (Grueter and van Schaik 2010).
Despite primate populations being able to persist in heavily altered ecosystems (Chapman et al. 2018), the pristine conditions required for supergroup formation are becoming rare, with increasing levels of habitat fragmentation and forest loss (Grueter et al. 2012b). For example,
Li et al. (2002) describe the disappearance of snub-nosed monkeys from low-altitude plains areas and some mountainous regions over the last 400 years [where they presumably formed supergroups in the past], marooning remaining populations in forested mountainous regions.
In addition, hunting pressure by humans can lead to reduced group sizes, as observed in red and black-and-white colobus in the Udzungwa Mountains of Tanzania (Marshall et al. 2005), and simakobu monkeys (Simias concolor) on the Mentawai Islands Regency, Indonesia (Hadi et al. 2009).
Most primates forming supergroups display fission-fusion dynamics that function to regulate group size in accordance with fluctuating resource abundance (Aureli et al. 2008; Kirkpatrick et al. 1999; Majolo et al. 2018; Nie et al. 2009; Qi et al. 2014; Schreier and Swedell 2012;
Snyder-Mackler et al. 2012b). However, fallback foods – “foods whose use is negatively correlated with the availability of preferred foods” (Altmann 1998; Marshall and Wrangham
2007, p. 1220) – can sustain groups during lean ‘in-between’ times as they are abundant year- round (Hanya et al. 2004; Knott 2005; Lambert et al. 2004). Fallback foods facilitate the persistence of supergroups when preferred foods are scarce; for example, snub-nosed monkeys feed on lichen and remain in large groups even during winter (Grueter et al. 2009b), and supergroups of geladas rely on underground plant storage organs (tubers) as fallback foods during the dry period (Jarvey et al. 2018).
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Thesis objectives and organisation
This thesis investigates the socioecology of a supergroup of Rwenzori black-and-white colobus in Rwanda. Primate species forming “supergroups” are shaped by a range of social and ecological selective pressures, and in some cases, supergroups of primates are socially organised into multilevel societies composed of several discrete social units nested within a larger social matrix. The unusual supergroups of Rwenzori colobus in Nyungwe NP were first investigated by Fashing et al. (2007a), Fimbel et al. (2001), and Vedder and Fashing (2002).
These studies improved our understanding of activity and ranging patterns, and costs of large group size (Fashing et al. 2007a), diet (Vedder and Fashing 2002), and ecological basis for large group size (Fimbel et al. 2001). However, this initial research has left unanswered questions about the social organisation and resource requirements of the supergroups present, and highlighted the potential for future research on the Rwenzori colobus supergroups.
Understanding the social organisation and resource requirements of this supergroup is a central focus of my research. The shared similarities with Chinese snub-nosed monkeys in terms of large group size, montane habitat use and seasonal consumption of lichen (Grueter et al.
2009b), leads to predictions that the Rwenzori colobus form multilevel societies (Fashing et al.
2007a). The data used in this study include long-term data collected over 13 months, based on daily observations of a habituated supergroup of Rwenzori black-and-white colobus (Colobus angolensis ruwenzorii) in the mountainous forest of Nyungwe National Park, Rwanda. In this study, I examine three elements of the socioecology of the Rwenzori colobus supergroup. In
Chapter Two, I examine the social organisation of the Rwenzori colobus supergroup inhabiting
Nyungwe National Park, aiming to establish whether they form a multilevel society with internal hierarchical groupings, or a multi-male multi-female society. As the supergroup contained between 300-500 individuals, I was not able to individually identify individuals.
Therefore, I utilise a method novel for primates but previously ‘ground-truthed’ on tagged birds
15 and reef sharks (Jacoby et al. 2016; Psorakis et al. 2012), to extract social network structure from the time-stamped spatio-temporal distribution of passing individuals in a progression. In
Chapter Three, I investigate the ecological preconditions underlying supergrouping. I measure feeding competition using the patch depletion method (Snaith and Chapman 2005), comparing intake rate coupled with movement rate in food patches. Finally, in Chapter Four, I investigate the ecological preconditions necessary for supergrouping by examining how a supergroup uses resources in periods of resource abundance compared to periods of resource scarcity.
The chapters in this thesis are written in the form of manuscripts for publications: thus, each chapter is proceeded by a review of the literature and relevant background information.
Project significance
Preliminary research has been conducted on Rwenzori colobus in Nyungwe National Park by
Fimbel et al. (2001), Fashing et al. (2007a) and Vedder and Fashing (2002), specifically studying diet, activity, ranging patterns, and leaf quality. These studies leave unanswered questions regarding the structure and organisation of the supergroups that are unusual amongst
African colobines. For the supergroup of Rwenzori colobus in Nyungwe, this is the first research project studying social structure and organisation. Nyungwe is the only known place where black-and-white colobus form permanent supergroups (Fashing et al. 2007a), and is an important site for the conservation of Rwenzori colobus supergroups. Temporary supergroups of 100+ individuals are known to form at Lake Nabugabo, Uganda, but the band is less cohesive than at Nyungwe (Stead and Teichroeb 2019). Early observations by Oates (1974) in the Sango
Bay Forests, Uganda, suggested group structure was different to that of Colobus guereza, with large groups of ~30-51 individuals observed containing several adult males, and “the largest group was judged to consist of three smaller groups associating closely together” (Oates 1994, p. 96). The groups observed by Oates in 1972 may be the same population as studied by Stead
16 and Teichroeb (2019). The absence of supergroups of Angolan colobus at other montane sites in Eastern Africa is of interest. This suggests that supergroup formation may reflect a site- dependent interplay among forest size, fragmentation, degradation, and hunting pressure by humans. The findings of this study will contribute significantly to the understanding of multilevel social systems, expand the documentation of multilevel societies into the African group of colobines, and broaden the scope of ecological settings where we find multilevel systems.
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CHAPTER TWO:
STRUCTURE OF A SUPERGROUP: A MULTILEVEL
SOCIETY CONTAINING MULTI-MALE UNITS
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Chapter Two: Structure of a supergroup: A multilevel society containing multi-male units
Abstract
Primates display broad diversity in their social organisation. The social groups of a few primate species are organised in a multilevel fashion, with large groups composed of multiple, core one-male units. A characteristic of multilevel societies is that the higher levels can include hundreds of individuals. The Rwenzori black-and-white colobus (Colobus angolensis ruwenzorii) in the montane forests of Rwanda form supergroups and have been suspected of exhibiting multilevel social organisation. Here I present the first data on the ‘anatomy’ of a supergroup numbering 500+ individuals. I identified subgroups within the supergroup based on progression data, extracting the social network structure from the time-stamped spatio- temporal distribution of passing individuals identified to age-sex class, and selecting an optimal time window for each network using the two-step approach developed by Uddin et al. (2017).
I detail the existence of core units – multi-male units (MMUs) with a mean of 1.73 adult males and 3.11 adult females, as well as one-male units (OMUs), all-female units and bachelor units composed of adult and sub-adult males. More than two-thirds of units are MMUs, containing multiple males. These grouping patterns conform to a multilevel society with predominantly multi-male core units, a social system that has recently also been described for a population of the same taxon in Uganda. Individual identification is, however, required to corroborate these preliminary conclusions.
Introduction
Primates exhibit a diversity of social systems, including semi-solitariness individuals, pairs, and larger groups of varying sizes and composition, which vary widely in cohesion, patterns of social interaction, dispersal, and mating systems (Kappeler and van Schaik 2002).
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Understanding social organisation, i.e. the size, composition and cohesiveness of social groups, is especially relevant as it is the most fundamental aspect of social systems, giving rise to the diversity of mating systems and social structure, i.e. social relationships emerging from repeated interactions (Kappeler 2019). Variation in these components is seen across and within species, and even within populations (Koenig et al. 2013). A variety of ecological and social selective factors such as abundance and quality of food resources, predation, disease and infanticide shape adaptive individual decisions and result in different types of social systems
(Alexander 1974; Dunbar 1988a; Isbell 2017; Rubenstein and Wrangham 1986; Sterck 1997; van Schaik 1989).
Multilevel or modular societies represent a complex form of group organisation composed of multiple discrete social units nested within a larger social matrix of up to several hundred individuals (Grueter et al. 2012a; Kummer 1984; Stammbach 1987). This organisation has been described in humans (Hamilton et al. 2007), non-human primates (Schreier and Swedell 2009;
Snyder-Mackler et al. 2012b), elephants (Wittemyer et al. 2005a), equids (Rubenstein and
Hack 2004), giraffes (VanderWaal et al. 2014), and cetaceans (Cantor et al. 2015). Multilevel societies range from simple two-level societies seen in zebras (Equus burchelli), composed of the core breeding unit and the larger herd (Rubenstein and Wrangham 1986), to highly complex elephant (Loxodonta africana) societies with up to six organisational tiers (Wittemyer et al.
2005a).
In primates, multilevel societies were first described by Kummer (1968) in hamadryas baboons
(Papio hamadryas) and have since been documented in three primate clades: African papionins, Asian colobines and hominins. Multilevel societies in primates comprise multiple socially and spatially distinct one-male units (OMUs) that congregate to form higher-level social groupings (Schreier and Swedell 2009). Hierarchical layers present in every multilevel society include the OMU and the larger band (Grueter et al. 2012a; Kawai and Iwamoto 1979;
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Snyder-Mackler et al. 2012b). However, in some taxa additional organisational levels exist between the unit and band level (Grueter et al. 2012a; VanderWaal et al. 2014; Wittemyer et al. 2005b). For example, in hamadryas baboons, ‘clans’ are formed when bands subdivide into temporary associations (Schreier and Swedell 2009). An important diagnostic feature of multilevel societies is the oftentimes extremely large number of individuals that reside within them. The band level – analogous to the group level in non-modular primates – can number up to 400+ individuals as in hamadryas baboons, and the highest levels which are aggregations
(pseudosocial groups) and not individualised groups (sensu Immelmann and Beer 1989) can contain up to 1000 individuals as in geladas (Mac Carron and Dunbar 2016; Snyder-Mackler et al. 2012b).
Among the colobines, multilevel social organisation has been documented in three genera in
China and Indochina: the doucs (Pygathrix spp.; Rawson 2009), proboscis monkeys (Nasalis larvatus; Yeager 1990) and snub-nosed monkeys (Rhinopithecus spp.; Qi et al. 2014; Zhang et al. 2006). Most African colobine populations form relatively small one-male, multi-female groups, or multi-male, multi-female groups (Fashing 2001b; Struhsaker 1975). However, in the high-altitude, mountainous forest of Nyungwe National Park, Rwanda, Rwenzori black- and-white colobus (Colobus angolensis ruwenzorii) form a large supergroup (Fimbel et al.
2001), with over 500 individuals (Miller, pers. obs.). At a lowland site in Uganda (Lake
Nabugabo), Rwenzori colobus form temporary associations of over a hundred individuals
(Arseneau-Robar et al. 2018; Stead and Teichroeb 2019), and concurrent research being conducted in Uganda suggests the presence of a multilevel social organisation (Stead and
Teichroeb 2019). Additionally, a study at the same site on proximity and grooming patterns of
Rwenzori colobus reveals opposite-sex bonding and weak same-sex bonds within dyads
(Arseneau-Robar et al. 2018). Chinese snub-nosed monkeys share a possible socioecological convergence with the Rwenzori colobus based on similarities in large group size, habitat
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(montane forest) and diet (seasonal lichen consumption) (Grueter et al. 2009b). Hence,
Rwenzori colobus are predicted to form multilevel societies similar to the supergroups of snub- nosed monkeys (Fashing et al. 2007a).
Grueter and Zinner (2004) identified Rwenzori colobus as a possible test case of the
‘demographic’ hypothesis, which predicts that social stress and increased competition in very large groups with many unfamiliar individuals is detrimental to individual female primate fitness. As females bear the costs of pregnancy and lactation, they are particularly susceptible to factors affecting energetic status (Trivers 1972). As a result, larger groups are expected to form subunits of ‘familiar’ individuals and are thus incompatible with a non-modular type of social organisation (Grueter et al. 2012a).
Studying social dynamics underlying multilevel societies is complicated by the very large number of individuals involved, but methods have been developed to deduce the existence (or lack thereof) of multilevel societies such as analyses of group progressions (Grueter et al.
2017a; Hongo 2014) and proximity patterns (Bowler et al. 2012; Zhang et al. 2012). Proximity has been used as an indicator of connectedness within social networks in many gregarious animal populations (Croft et al. 2008; King et al. 2011; Whitehead 2008). For example, in golden snub-nosed monkeys (Rhinopithecus roxellana), Zhang et al. (2012) confirmed the existence of a multilevel society by creating social networks based on spatial proximities, and
Qi et al. (2014) used spatial association data from satellite telemetry to identify the structural components of the society. Thus, proximity-based associations and social network analysis have been used to identify the underlying social dynamics of non-human primates (Guan et al.
2013; Qi et al. 2014; Zhang et al. 2012).
Quantitative analytical tools previously applied to species with stratified social organisations include cluster analysis and social network analysis (Qi et al. 2014; Snyder-Mackler et al.
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2012b; Wittemyer et al. 2005b; Zhang et al. 2012). Social network analysis examines the structure of relationships between entities (i.e. individuals, groups, classes, phenotypic traits, organisations), using “nodes” (or vertices) and “edges” (or links, connections or arcs) to understand dynamics, with edges representing any interactions between the nodes (i.e. based on proximity or behavioural interactions) (Farine and Whitehead 2015). Recently, techniques have been designed to extract social network information from spatio-temporal time series data or longitudinal networks (Uddin et al. 2017). Social network dynamics have been investigated by recording continuous streams of time-stamped observations on arriving individuals using spatio-temporal proximity as a basis for determining associations (Blonder et al. 2012; Jacoby et al. 2016; Psorakis et al. 2012). Recent approaches make it possible to construct social networks from spatio-temporal data by ‘time-slicing’ the data stream using a fixed time window (Δt) which delimits the basis for biologically or statistically meaningful connections within the network (Krings et al. 2012; Uddin et al. 2017). Time-stamped activity that falls within each window is aggregated, and time window size can vary from seconds to years depending on the taxon being studied.
I hypothesised that the supergroups of Rwenzori colobus in Rwanda have a multilevel type social organisation, with a minimum of two social tiers: spatially distinct one-male, multi- female units (OMUs), and the larger band. Assuming that this multilevel social organisation emerges from the spatial and temporal order of monkeys passing in a single file, I used a method that extracts a social network from the spatio-temporal data stream (i.e. time-series data) to determine if there were distinct subgroups in the network indicative of multilevel organisation, and if so, what their composition was.
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Methods
Data collection
Data collection took place in Nyungwe National Park, south-western Rwanda (2°15’-2°55’ S,
29°00’-29°30’E, elevation 1600-2950 m above sea level. Nyungwe covers 1013 km2, including primary and secondary forest, and is considered to be one of the largest and most biologically diverse montane rainforests in Africa (Plumptre et al. 2002). Within Nyungwe National Park there is one habituated supergroup of Rwenzori colobus, which ranges throughout the Park, and is tracked regularly by the Rwanda Development Board (RDB) trackers. The colobus tolerate human presence comfortably at a distance of approximately ≥15 m. There are other groups of unhabituated Rwenzori colobus within the Park, which were occasionally encountered, but no staff or researchers follow these groups (Figure S2.1). Data on the habituated supergroup were collected by my research assistant and I over 13 months from 19th
July 2016 to 22nd August 2017 for a total of 1180 hours. Colobus follows began at ~08:00 until
~17:00 across all months (mean number of days per month: 11.1, range: 7-14; mean number of consecutive day follows per month: 7.1, range: 2-14). The supergroup was at all times split into equally sized sub-units, discernable in the field when travelling in progressions, when resting in clusters, and when clumped in trees while feeding.
The supergroup or band (largest unit) was observed to separate into smaller groups, each with
>200 individuals for periods of a few hours to a few months during the study period. When such a fission occurred, we stayed with the larger group (the research team only followed one group or band at a time). Each group had at least one individual we could identify, and groups ranged in separate regions of the National Park, ≥2 km apart. On days with chimpanzee attacks
(19th July 2016, 26th November 2016, 20th February 2017, 21st May 2017, 19th June 2017), the band, or the smaller groups, further splintered into multiple parties of 50-150 individuals, which
24 typically rejoined the same afternoon or the following day (May attack), or following the June attack, partially rejoined to a 200+ individual band, while others remained separated for the remaining study period. We also observed a temporary fusion (one day) of 50-100 unhabituated individuals with the study group. The newcomers were noticeably warier than the habituated group members.
Progressions
Progressions occurred as the group travelled, often in single file along branches where canopy was sparse. We time-stamped individual monkeys as they moved single file through the trees identifying at the level of age-sex class using binoculars (Leica© 8x50 BA Binoculars), noting the time (hour:minute:second) that the individual passed a fixed point during the progression.
I watched the progression with binoculars and dictated to my research assistant who recorded the information. Each scanned individuals was classified into the same age/sex classes as the proximity scan method (see Table S2.1 for age-sex classifications).
Proximity scans
Systematic data on proximity and activity patterns were collected via instantaneous scan sampling (Altmann 1974) taken at 15‐min intervals. Due to the sparse tree density in Nyungwe and open valleys, hundreds of individuals were often visible at once, so we did not scan all individuals at once. Instead, I divided the field of view into 30 m sections and shifted focus from left to right. Within each section I randomly selected one focal individual (from all age– sex classes, excluding infants; Table S2.1) and estimated interindividual distances between the focal individual and all its visible and identifiable neighbours (Bowler et al. 2012) within 30 m
(distance category from focal; contact, 0-3 m, 3-5 m, 5-10 m, 10-15m, 15-20 m, 20-30 m). I then initiated the next scan at the first visible individual outside and to the right of the previously scanned area, including all visible individuals, recording information from each of
25 them (see below). If an individual was observed departing a scanned section into a yet-to-be scanned section, or once all visible individuals from the vantage point had been scanned, sampling ceased. For each individual I recorded age, sex (Table S2.1), and activity (feed
(including food species and plant part), rest, feed, forage, move, vigilant, groom, play, mate, aggress). I aimed to collect a minimum of 10 scans per day (mean number of scans per day:
8.3 (±SD 3.7), range: 2-23).
To rule out the possibility that close male-male associations are an artefact of sampling bachelor groups – which are unlikely as only a few small bachelor groups were observed in the field – I used a sub-set of the scans in which 1) there was ≥1 adult or sub-adult male and ≥1 adult or sub-adult female in the scan, 2) there was ≥1 individual resting within 5 m of the focal, and 3) the majority of individuals in the scan were resting. I used preliminary observations to determine the 5 m cut-off, as I observed the colobus forming visually distinct clusters in the field while resting and I predicted that the majority of sub-group members would be spread <5 m apart in a single tree. It is important to note that despite proximity and progression protocols being conducted on the same day, they did not overlap and were conducted independently.
Data analysis
Social network data
I extracted the social network information from the time-stamped spatio-temporal distribution of passing individuals that could be identified at the level of the age-sex class. By time- stamping individuals to the second, I gathered precise spatio-temporal data that can be used to map spatial association patterns between age-sex classes. This approach of extracting social structure and networks from spatiotemporal data streams has been used with individually tagged wild birds (Psorakis et al. 2012), and the temporal co-occurrence of tagged reef sharks
(Jacoby et al. 2016). Individuals that pass in close temporal proximity to one another are more
26 likely to be associated in a biologically meaningful way (Grueter et al. 2017b; Krause et al.
2013). Individuals that pass along a branch within seconds of one another are more likely to be associated than those that are separated by minutes or hours, for example, Grueter et al. (2017a) observed sequentially arriving Yunnan snub-nosed monkey (Rhinopithecus bieti) males in separate social units were separated by less than 35 seconds. Over the study, I recorded 420 progressions, totalling 179 hours. Each progression event was scored on the observation quality resulting from a combination of factors (lighting, proximity of monkeys to observers, height, angle of observation, weather, progression speed), and quality scores were later used to select optimum progression data for analysis. To extract the highest quality information, I excluded progressions with: 1) quality scores of <7/10, 2) when monkeys were passing by >1 route, and
3) <30 individuals were recorded (n=40, final sample size). The progressions do not reflect grouping sizes, (i.e. a group of 300 individuals may take multiple routes to pass a canopy gap with only a portion of the individuals in the progression being monitored). It is highly unlikely that the same individual was recorded more than once in a single progression, as data were collected during directional travel periods.
Selecting an optimal window size
Longitudinal networks are often represented as static networks, where edges and nodes are aggregated within a time window of size Δt (Ribeiro et al. 2013). Window size selection is a key consideration in the design of any longitudinal network study, as a poorly selected window size can lead to inaccurate conclusions (Uddin et al. 2017). The selected window size splits the underlying longitudinal network into equally spaced window networks. For example, if the duration of a longitudinal network is 20 days, then a window size of two days will split that longitudinal network into 10 window networks. If the selected time window Δt is too small it will not capture all-important connections, and if it is too large it will cause the network to
27 contain biologically irrelevant connections (e.g. individuals in separate social units with no social affinity) (Figure 2.1).
To select the appropriate window for the visualisation of a longitudinal network, I adapted the two-step method developed by Uddin et al. (2017). In the first step, I used node-level measures
(e.g. degree centrality) to quantify node activity in a network. In order to explore a longitudinal network using node-level measures (e.g. degree centrality), I needed to observe each node at different times. However, the dataset that I used in this study did not have any node-level information. The study subjects were observed based on their different characteristics (e.g. age and sex). I can quantify a node-level measure (e.g. degree centrality) for a node in a snapshot but cannot quantify the same measure for the same node across different snapshots. For this reason, I followed a network-level measure (i.e. degree centralisation) in the two-step procedure as suggested by Uddin et al. (2017) to determine the optimal window size. The degree centralisation is a measure that gives a normalised value for a network (i.e. snapshot or window network) by using the degree centrality values of all its member actors.
The degree centralisation is a group-level construct that measures how variable or heterogeneous the actors’ degree centralities are within a network (Wasserman and Chapman
2003). The degree of an actor represents the number of connections that actor has with the remaining network actors. For a given candidate value for the optimal window size of a progression, I first calculated the degree centralisation for all window networks. Then I calculated the standard deviation of these degree centralisation values. For each candidate value, I calculated the corresponding standard deviation value. I considered the candidate value that resulted in the minimum standard deviation value as the optimal window size for the underlying progression, because the minimum standard deviation value confirms a minimal difference concerning the connectivity cohesion among different window networks.
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I then followed a clustering approach to explore groupings within each window network. In detecting groups within a window network, I followed the principle that actors within the same group are more connected among themselves and less connected with actors from other groups.
To explore groupings within each window network, I applied the Louvain Method (Blondel et al. 2008), using the open-source software Gephi v.0.8.2 (Bastian et al. 2009). I visualised the
1 networks using the temporal distances between monkeys (nodes) ( (N2-N)), and then 2 spatialized the data using the Force-Atlas 2 algorithm, set node size to 1, edge weight influence to 0, and selected stronger gravity.
Figure 2.1. A hypothetical sequence of time-stamped passing individuals. (a) The data stream is segmented based on a calculated time window of size Δt, where Δt is calculated for each data stream or progression by adapting the two-step method developed by Uddin et al. (2017).
Individuals (red or blue square icon) that fall within Δt are assumed to be associated, due to spatio-temporal proximity. If there are no nodes/individuals in a time window, i.e. second from left in (a), it is not considered as a window network. (b) Individuals that fall within the same
29 window network represent a grouping, and groupings were further investigated using a clustering approach. Illustration adapted from Krause et al. (2013).
Proximity scans: Nearest neighbour
I used instantaneous scan data to quantify frequencies of age-sex classes as nearest neighbours, using only scans when the nearest neighbour was ≤5 m from the focal individual. I also extracted nearest neighbour data from progression data, we identified the ‘nearest neighbour’ of each time-stamped ‘subject’ as either the preceding or following animal in the progression, whichever passed by closer in time to the subject. I pooled all individuals of an age-sex category for analyses and separated them by activity state: (1) scan data – feeding, resting and socialising, and 2) progression data – travelling (recorded during travel periods). The proximity index was calculated as:
푓 (퐵) + 푓 (퐴) 퐴 퐵 퐹 (퐴) + 퐹 (퐵)
Where, for age-sex classes A and B, F (A) is the total number of scans of A, F (B) is the total number of scans of B, f A (B) is the number of scans in which B was the nearest neighbour of
A when A was scanned, and f B (A) is the number of scans in which A was the nearest neighbour of B when B was scanned (Arseneau-Robar et al. 2018). Expected frequencies were based on group demographic information collected during total group counts. Separate sets of proximity indices were calculated for adult male (focal) to all age-sex classes, and adult female (focal) to all age-sex classes.
Proximity scans: Close-proximity resting
I used a sub-set of the scans in which the activity was resting with at least one male and female in the scan to ensure I was investigating mixed-sex groups, and not bachelor groups.
Individuals included within the scan (i.e. within 30 m of the focal), but not within 5 m of the
30 focal were disregarded. I chose 5 m because groups of colobus, especially during resting, are often in separate trees, or if in the same tree are >15 m apart. In addition, evidence from other multilevel society forming species suggests that members from the same unit will often huddle into a cluster with close proximity while resting (Zhang et al. 2011). The purpose of setting the proximity to ≤5 m is to distinguish internal unit males from peripheral or “follower” males; in snub-nosed monkeys (Rhinopithecus beiti) it was rare (~1% of scans) to find more than one male resting in the same tree (Grueter et al. 2017a).
Results
Group size and composition
A total of 512 individuals were counted crossing a road in February 2017, representing the most complete group count during the study period. I identified 94% (n=486) of the individuals to age-sex class. There were 110 adult males, 168 adult females, 23 sub-adult males, 30 sub- adult females, 13 sub-adult males or females, 45 juveniles, 97 infants, and 26 unknown individuals. Adult male: female ratio was 1:1.5, and infant: adult-female ratio was 1:1.7.
Social organisation
The 40 progressions analysed (30 hours of observation) included 2674 observed individuals, with a range of 36 to 178 individuals per progression (no individual could be recorded more than once in a single progression due to the directional travel). To ensure the progressions represent a random selection from the population, I performed 40 chi-square tests, comparing the observed age/sex composition of each progression to the expected composition obtained from the most complete progression. Out of 40 samples (6 age-sex classes, across 40 progressions), the age/sex class distributions which deviated from expected frequencies were only those of sub-adult males. Results for five age/sex classes (adult male, adult female, sub-
31 adult female, juvenile, infant) conforming to expected frequencies suggest that the progression data represents a reliable random sample of the population subset.
The minimum length of a progression was 8 minutes 22 seconds (n=35 individuals), and the maximum length was 4 hours, 14 minutes, 53 seconds (n=87 individuals). The average unit of difference between two windows was 211 seconds (n=291), and optimal window sizes ranged from 89 to 774 seconds (speed of the moving progression of monkeys was a key factor resulting in different optimal window sizes).
From the independent analysis of the 40 progressions, I identified 294 social units (>2 individuals), 25 pairs, and 31 solitary individuals. I recorded 89 one-male units (OMUs), 128 multi-male units (MMUs), 44 mixed-sex units (no adult males, but containing sub-adult male/s), 12 all-male units (AMUs) and 21 all-female units (AFUs). Mixed-sex units (OMUS and MMUs; with at least 1 male or sub-adult male, and adult female or sub-adult female/s), were the most common subgroup type (n=261), and contained a mean of 9.34 individuals (±SD
4.51), and a mean of 1.73 adult males (±SD 4.51) and 3.11 adult females (±SD 1.84) (Table
2.1).
The mean number of females in MMUs was 3.65 (±SD 2.02; n=128) which was significantly higher than in OMUs (2.04 ±SD 1.43; n=89; F (1, 215)=11.35, p<0.001). Of the OMUs (n=89),
59 of these units contained a single adult male, and the remaining units contained one adult male as well as sub-adult male/s.
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Table 2.1. Composition of mixed-sex groups (≥1 male or sub-adult male, and adult female or sub-adult female), male-only groups (≥2 adult male or sub-adult male), and female-only groups
(≥2 adult female or sub-adult female) and mean number of all age-sex classes within groups.
Group selection is based on optimal window selection and subsequent clustering using the
Louvain modularity algorithm.
Mixed-sex groups Male-only groups Female-only groups N 261 12 21 Mean (±SD) Group size 9.3 (±4.5) 4.3 (±1.7) 5.2 (±1.7) Adult males 1.7 (±1.4) 1.9(±1.2) - Adult females 3.1 (±1.8) - 2.4 (±0.8) Sub-adult males 1.3 (±1.3) 1.9 (±1.6) - Sub-adult females 0.5 (±0.7) - 0.6 (±0.9) Juveniles 0.6 (±0.8) 0.3 (±0.6) 0.7 (±0.9) Infants 1.6 (±1.4) - 1.3 (±1.2)
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Figure 2.2. Box plot for sizes (number of individuals) of mixed-sex units of Rwenzori colobus
(n=261, ≥1 male or sub-adult male, and adult female or sub-adult female). Units were identified post-analysis from 40 progressions combining optimal window size and Louvain modularity algorithm in group selection. The middle line within the box represents the median, the top line represents the 75th percentile, and the bottom line represents the 25th percentile. The overlaid unfilled circles represent each mixed-sex group (n=261).
Distribution of unit sizes
I examined the distribution of unit sizes evident in the clustering distribution of unit sizes (Mac
Carron and Dunbar 2016). I plotted the distribution of the 294 units (>2 individuals), including all age-sex classes, mixed-sex and single-sex units, and use k-means clustering to identify natural groupings. The number of clusters was optimised at six (Figure S2.3: F5,30=302.8, p<
0.001); mean values are shown by vertical dashed lines in Figure 2.3. These clusters are at unit sizes 3, 7, 15, 21 and 29 individuals, with 185 of units containing ≤10 individuals, and only four units larger than 20 individuals.
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Figure 2.3. Frequency distribution for unit sizes (n=294) of Rwenzori colobus resulting from the network approach and Louvain clustering. Vertical lines mark the mean values for the six clusters identified by a k-clusters analysis: the cluster centroids are at approximately 3, 7, 9,
15, 21, and 29 individuals.
Networks
I visualised the networks with the highest modularity scores from the Louvain clustering algorithm (Figure 2.4, Figures S2.3 & S2.4). As visualised for the first progression, internal community structure has been identified by the network analyses and Louvain algorithm. I visualise a progression capturing 141 individuals (Figure 2.4), where I observe multiple adult males in several units, with multiple adult females, sub-adult males and other group members.
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Figure 2.4. Progression capturing 141 individuals on 17-08-2017, with a duration of 1.02 hours
(calculated optimal window size Δ=228 seconds, 141 nodes; mothers and infants separated to individual nodes following analysis for better visualisation of group composition; modularity score=0.891). Dark blue nodes denote adult males, light blue nodes denote sub-adult males, red nodes denote adult-females, small grey nodes denote infants, and larger grey nodes denote all other individuals; sub-adult females, pubescent males, juveniles. Edge thickness represents the strength of the connection between two nodes; the thicker the edge, the closer the individuals in the progression.
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Figure 2.5. A multi-male unit with three adult males, six adult females, two juveniles, one infant and three unidentified individuals surrounding them. Photo: Alexandra Miller.
Nearest neighbour
Of 1,257 scans when activity state was not travel (rest, feed, forage, move, vigilant, groom, play, mate, aggress), nearest neighbours (≤5 m) could be identified in 669 cases, and from progressions (n=40) when activity state was travelling, nearest neighbour could be identified in 2,942 cases, collected throughout the study period, which were considered free from visibility bias and used in the analysis. In 266 scans in which adult males were the focal individuals, adult males were more often nearest neighbours to adult males (X²=12.15, df=1, P
<0.001), sub-adult males (X²=25.00, df=1, P <0.001) and infants (X²=8.17, df=1, P <0.001) than expected (Table 2.2). However, the type of activity seemed to influence the nearest neighbour of females. In 311 scans in which adult females were the focal individuals, adult
37 females were more often nearest neighbours than expected to adult females (X²=33.64, df=1,
P <0.001), sub-adult females (X²=10.66, df=1, P <0.05), juveniles (X²=5.83, df=1, P <0.05) and infants (X²=174.45, df=1, P <0.001) (Table S2). However, when travelling sub-adult males were the nearest neighbour of adult females (X²=104.54, df=1, P <0.001) more often than expected (Table 2.3).
Table 2.2. Chi square tests comparing observed to expected proximity records for adult
Rwenzori colobus with other age-sex classes as their nearest neighbour (≤5 m) (one nearest neighbour record per scan) when the group not travelling (rest, feed, forage, move, vigilant, groom, play, mate, aggress) (n= 669), comparing observed to expected frequencies with a chi- square test. Expected values calculated from the age/sex proportions in largest group progression.
Adult female scan focal X2 Adult male scan focal X2 Adult female-adult male 1.16 Adult male-adult male 12.15** Adult female-adult female 33.64** Adult male-adult female 0.04 Adult female-sub-adult male 1.89 Adult male-sub-adult male 25.00** Adult female-sub-adult female 10.66* Adult male-sub-adult female 0.04 Adult female-juvenile 5.83* Adult male-juvenile 8.17* Adult female-infant 174.45** Adult male-infant 13.75** P <0.05*, P <0.001**
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Table 2.3. Chi square tests comparing observed to expected proximity records for adult
Rwenzori colobus with other age-sex classes as their nearest neighbour (one nearest neighbour per scan) when the group is travelling, comparing observed to expected frequencies with a chi- square test. Expected values calculated from the age/sex proportions in largest group progression. Infants were excluded as they are carried during travel periods.
Adult male scan focal X2 Adult female scan focal X2 Adult male-adult male 1.75 Adult female-adult male 7.30* Adult male-adult female 0.23 Adult female-adult female 0.13 Adult male-sub-adult male 65.96** Adult female-sub-adult male 104.54** Adult male-sub-adult female 10.08** Adult female-sub-adult female 1.52 Adult male-juvenile 6.37* Adult female-juvenile 5.44* P <0.05*, P <0.001**
Proximity indices
When adult males were focal individuals, adult males were most often in close proximity
(proximity index=0.32), followed by adult females (proximity index=0.26). When adult females were focal individuals, juveniles/infants were most often in close proximity (proximity index=0.57), followed by adult males (proximity index=0.26) (Table 2.4).
Table 2.4. Proximity indices (PI) for adult males and adult females with other age-sex classes as their nearest neighbour (≤5 m) (one nearest neighbour record per scan)
Adult female scan focal PI Adult male scan focal PI Female-adult male 0.26 Male-adult male 0.32 Female-adult female 0.15 Male -adult female 0.26 Female-sub-adult male 0.10 Male -sub-adult male 0.16 Female-sub-adult female 0.05 Male -sub-adult female 0.08 Female-juvenile/infant 0.57 Male-juvenile/infant 0.14
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Close-proximity resting
In a filtered sub-set of proximity scans involving mixed-sex resting clusters (n=148; individuals resting within 5 m of the focal), 61% contained more than one adult male, and 76% contained more than one adult or sub-adult male (Table 2.5). An average of two adult males were recorded in resting clusters, and as many as six adult males resting within 5 m of the focal in mixed-sex groups (Table 2.5).
Table 2.5. The number of each age/sex class individuals participating in 148 close-proximity resting clusters (n=148), i.e. individuals resting within ≤5 m of the focal individual. I used the sub-set of the scans where 1) majority of individuals in the scan were resting, 2) there was at least one male and female in the scan, 3) ≥1 individuals were resting within 5 m of the focal.
Adult Adult Sub- Sub- Juvenile Infant Male male female adult adult male female Number of resting clusters 138 147 63 29 48 110 148 Number of clusters with 90 108 24 3 11 49 112 >1 (% of total) (61%) (73%) (16%) (<1%) (<1%) (33%) (76%)
Mean number of 1.94 2.50 0.65 0.24 0.42 1.22 2.59 individuals per resting ±1.16 ±1.50 ±0.92 ±0.56 ±0.70 ±1.01 ±1.50 cluster (S.D) Maximum number of 6 8 4 4 4 4 8 individuals per resting cluster Minimum number of 0 0 0 0 0 0 1 individuals per resting cluster
Discussion
I applied a subgroup detection algorithm to timestamped observations of sequentially passing individuals in a progression of Rwenzori colobus which partitioned the supergroup of 300-
500+ individuals into highly distinct subgroups; these varied in composition but were predominantly MMUs, followed by OMUs. Combined with anecdotal information of subgroups being spatially distributed across different trees during resting I tentatively conclude
40 that these colobus form a multilevel society. A concomitantly conducted study at Lake
Nabugabo in Uganda also provides evidence of Rwenzori colobus living in a multilevel society
(Stead and Teichroeb 2019). The alternative hypothesis – that these supergroups represent large multimale-multifemale groups – is less tenable given the strong modularity detected in the social network. However, the data are silent on whether OMUs and MMUs consist of the same individuals over time; individual identification is needed to demonstrate that particular individuals form stable subunits. It could also be argued that the subgroups identified are unstable parties characteristic of societies with atomistic fission-fusion dynamics (i.e. with constant or frequent changes in size, composition and cohesion of groups, see Grueter et al.
(2012a). However this argument does not hold water in light of the observation that the subunits had a relatively consistent age-sex class composition and that I never observed a subunit being detached from the other subunits (separately foraging subunits are commonly seen in societies with fission-fusion dynamics (see Goodall 1968; White 1996)). Moreover, the relatively strong modularity detected in the social networks is incompatible with atomistic fission-fusion.
In addition to the longitudinal network analysis, I analysed proximity patterns and the composition of resting clusters in mixed-sex units. These analyses provide further evidence that the majority of colobus subunits were MMUs. Adult males were in proximity to other adult males and sub-adult males more often than expected by chance, and close-proximity resting clusters contained a mean of two adult males. This is a different pattern to the OMUs with loosely attached males observed in other species forming multilevel societies such as snub- nosed monkeys, geladas and hamadryas baboons (Grueter et al. 2017a; Schreier and Swedell
2009; Snyder-Mackler et al. 2012a). I was unable to distinguish leader vs follower males, and it remains unclear if such differentiated male roles, as found in both geladas and hamadryas baboons (Dunbar 1984; Pines et al. 2011; Snyder-Mackler et al. 2012a), occur in Rwenzori colobus. It is unlikely that these relative proximities are solely due to the presence of associated
41 males in bachelor groups, as the vast majority of units observed were of mixed sex- composition, and the analyses of resting clusters were based on mixed-sex scans only. The finding of all-female units in the progression order may be an artefact of travel periods, as I did not observe all-female units during resting periods.
It is interesting to note that the median-size of mixed-sex units (Figure 2.2) corresponds closely to the mean group size for black-and-white colobus in general across multiple species (mean:
10.1 individuals) (Teichroeb et al. 2003). This correspondence implies that the Rwenzori colobus core units coalesce into the larger band. However, we cannot rule out the possibility that further tiers of organisation exist within this multilevel society, as described for other primates (e.g. Schreier and Swedell 2009). Concurrent research being conducted on Rwenzori colobus at Lake Nabugabo, based on follows of 12 identifiable core units, suggests the presence of a multilevel social organisation with a mixture of MMUs and OMUs (Stead and Teichroeb
2019).
A multilevel society with predominantly multi-male units may have originated from the merger of ancestral solitary units, as presumed for the emergence of Rhinopithecus multilevel societies, or alternatively via the sub-structuring of a multimale-multifemale groups (Grueter et al.
2012a). Among the five species of black-and-white colobus, unit structure is relatively heterogeneous, and multi-male units are relatively common, having been observed in all five species, across varied environments from eastern to western Africa (Dunham and Lambert
2016; Fashing 2001a; Fleury and Gautier-Hion 1999; Korstjens et al. 2005; Teichroeb and
Sicotte 2009). However, the Angolan black-and-white colobus subspecies inhabiting the dry coastal forests of Kenya and Tanzania (C. a. palliatus) forms small groups of 2-13 individuals, and MMUs are less frequently seen than the central and western African colobines (Dunham and Lambert 2016). In Kakamega Forest, Kenya, the majority of groups of guerezas were multi-male, and groups often had overlapping home ranges (Fashing 2001a). In Budongo
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Forest, Uganda, guerezas mainly formed OMUs, whose home ranges overlapped extensively in home range, and on occasion mixed together socially (Suzuki 1979). In Lopé National Park,
Gabon, multi-male groups of black colobus (Colobus satanas; Fleury and Gautier-Hion 1999), often had overlapping home ranges, and adjacent groups were found in association more than expected by chance, typically around food patches (Fleury and Gautier-Hion 1999). Perhaps overlapping home ranges of multi-male units, similar to C. satanas and C. guereza, and eventual cohesion into permanently fused groups when resources permit, gave rise to what I now observe in Rwanda: a putative multilevel society sub-structured into mainly MMUs.
Potential selective pressures favouring multilevel social organisation in this species include the social benefits of enhanced protection against predators and social threats, potentially bachelor males (Grueter and van Schaik 2010). Bachelor groups in Nyungwe seem to be less common and smaller than in snub-nosed monkeys (Grueter 2009; Huang et al. 2017), I observed a few all-male groups of approximately five individuals, thus perhaps in this population predators pose more of a risk than bachelors males. Chimpanzees form a considerable threat to Rwenzori colobus in Nyungwe, with multiple hunts observed throughout the study period. Elsewhere in
Africa, red colobus (Procolobus sp.) are generally the target primate species of chimpanzees
(Watts and Mitani 2002); however, no red colobus occur in Nyungwe. The threat of chimpanzees at this site may form a substantial selective pressure favouring multilevel social organisation and larger group sizes, similar to what is observed in red colobus, with larger groups recorded in forests where chimpanzees are a threat (Stanford 1998). However, the benefit of increasing group size as a response to the threat of predation saturates beyond a certain point, which may lie well below 500 (Grueter and van Schaik 2010; Hamilton 1971), and the supergroup would certainly be easier to detect than small groups. It should be noted that I observed a fissioning ‘flight’ response on several occasions when chimpanzee attacks occurred, resulting in smaller group sizes. As a result of long-term fission-fusion the size of
43 the study group varied over time; for half the year the typical grouping size was between 100-
300, and for half the year, group sizes climbed to 300+ individuals. It is this minimum group size of roughly 100 that may be a response to predation, but extreme groupings of 300+ individuals may be an opportunistic response to increased food availability, or perhaps for socialising.
Primate multilevel societies display variable levels of male-male tolerance, which is an important stepping-stone in the evolution of association among reproductive competitors
(Goffe et al. 2016; Grueter et al. 2012a). The occurrence of multi-male groups may arise because of the benefits provided by male-male cooperation, or the inability of dominant males to exclude rival males and monopolise a large number of females (Ostner and Schülke 2014;
Port et al. 2018). Wild Guinea baboons (Papio papio) living in a multilevel society display high levels of male-male spatial tolerance, support in agonistic interactions, and occasionally male-male grooming, potentially maintained by male philopatric ties (Fischer et al. 2017; Goffe et al. 2016). In geladas, dominant males share reproductive benefits with subordinate males co- residing within their unit, potentially as a compromise for sharing the costs of unit defence
(Snyder-Mackler et al. 2012a). Gelada MMUs are less frequently targeted by bachelor groups than OMUs, males in MMUs have longer tenure, and females in MMUs produce more surviving offspring than those in OMUs (Snyder-Mackler et al. 2012a). In hamadryas baboon society, male-male tolerance is seen at the clan level which represents the product of associations among several OMUs and solitary males, aided by the existence of kin relationships among males (Abegglen 1984; Schreier and Swedell 2009; Städele et al. 2015).
OMU leader males also frequently tolerate follower males which may assist with unit defence and/or infant protection and thereby enable leaders to prolong retention of females (Chowdhury et al. 2015). In the present study, Rwenzori colobus males within the same unit were observed
44 grooming each-other and sitting in close proximity, such affiliative behaviours are infrequently observed in other primate multilevel societies.
The male-male tolerance observed in multi-male units of Rwenzori colobus may have a breadth of socioecological benefits. The presence of supernumerary males in other primates can reduce the risk of takeovers (Port et al. 2010; Snyder-Mackler et al. 2012a), improve access to resources (Pope 2000), or provide more efficient predator deterrence (van Schaik and
Hörstermann 1994). Additionally, the limited monopolisability model posits that monopolisation of females by a single male becomes difficult with a larger numbers of females and when multiple females have synchronous estrus cycles, which may benefit subordinate males in securing matings (Bradley et al. 2005; Charpentier et al. 2005). This model also predicts the positive association between number of females and males in units, so OMUs are likely to contain fewer females than MMUs (Srivastava and Dunbar 1996). I found that groups containing multiple adult males contained more adult females than in groups with one adult male, which supports the limited monopolisability model (Srivastava and Dunbar 1996; Sterck and van Hooff 2000), but does not exclude the possibility that primary males also benefit from co-residing with secondary males.
Groups comprising of multiple males may be beneficial in group defence against predators.
Stanford (1998) found that the ratio of adult males to females in red colobus was much higher in populations where chimpanzees are sympatric with red colobus. A comparison of Asian,
African and New World folivorous monkeys also showed that the number of adult males per adult female was greater in areas where there are monkey-hunting predators (van Schaik and
Hörstermann 1994). Given the presumably substantial protection that living in a supergroup affords the Rwenzori colobus, it is unclear if the commonness of multi-male subunits bears any functional relationship to predation. Nevertheless, in this study multiple adult males were observed to engage in coordinated behaviour, participating in joint defence against
45 chimpanzees, although it is unknown whether the co-acting males were drawn from the same or different subunits.
This study was intended to unravel the social organisation of the Rwenzori colobus, and provides preliminary evidence that these primates are organized into multilevel societies based on primarily multi-male, multi-female core units, a conclusion that is supported by recent findings from a site in Uganda (Stead and Teichroeb 2019). However, in order to unequivocally conclude that these colobus are structured in a multilevel fashion with stable subgroup membership and that the basal units are genuine multi-male units (in which both males are reproductive) data on social interactions among individually identified group members are required. This study may act as a springboard for future studies that would focus on some of the emergent outcomes of social organisation, such as mating systems, social bonds, and dispersal regimes.
46
Supplementary data
Table S2.1. Age-sex class of individuals.
Age-sex class Identifying characteristics Adult male Fully grown male, visible penis and testicles with an unbroken, white patch between the testicles and anus and fused ischial callosities Adult female Fully grown female, may have physical signs of having produced offspring (i.e. protruding nipples), genitalia situated between unfused ischial callosities Sub-adult male Same characteristics as adult male body size is larger than female but smaller than fully mature adult male Sub-adult female Same characteristics as adult female, but no sign of having produced offspring. Body size is smaller than adult female, but larger than juvenile female Pubescent male Body size is similar to adult female, visible penis and testicles, fused ischial callosities Juvenile Smaller than sub-adult individuals but larger than infant, travels independently Infant Newborn infant (white) (0-3 months), slightly older colobus (~3 months) (grey), older infant (black-and-white) (~6+ months) normally carried by adult female
47
Figure S2.1. Map of Nyungwe National Park indicating locations and sizes of sighted unhabituated groups of Rwenzori colobus (not the followed supergroup). G1: ~100 individuals
(sighted 24/10/2016), G2: ~50 individuals (sighted 17/08/2017) fused with supergroup for ~1-
2 hour/s, G3: ~50 individuals (sighted 8/08/2017), G4: ~40 individuals (sighted 23/09/2016) observed next to Mayebe camp. With the exception of G2, the unhabituated groups were found while attempting to locate the main supergroup following break days between data collection periods.
48
Distribution of unit sizes
I used a k-means cluster analysis in SPSS, varying k between two and eight, to select the optimal division of the distribution into clusters, the optimal cluster number for the data set was six clusters (F6,30=302.85) p<0.0001. The optimal model fit of six clusters, is indicated by the maximum F statistic (Figure S2.2).
Figure S2.2. Plot of the F statistic for k-means analysis against cluster number for the data on unit size for Nyungwe National Park. The number of clusters is optimised at six.
Networks I visualised the two networks with the highest modularity scores from the Louvain clustering algorithm (Figures S2.3 & S2.4). As visualised for the first progression, internal community structure has been identified by the network analyses and Louvain algorithm, resulting in 16 communities or ‘units’ identified by the Louvain algorithm (Figure S2.3). Figures S2.3 and
49
S2.4 provide a visual depiction of the same progression of 178 individuals (165 nodes; mothers carrying infants represent a single node), where each coloured community or unit contains ≥1 adult male (Figure S2.3).
Figure S2.3. Clustering within each window network, for a single progression of Rwenzori colobus monkeys recorded on 20-07-2017, captured 178 individuals (optimal window size
Δ=512 seconds, duration=2.1 hours, 165 nodes; mothers carrying infants represent a single node). Nodes (n=165) are coloured by modularity class using the Louvain algorithm
(modularity score=0.9).
50
Figure S2.4. Network divided into sub-networks by window network (two-step method; see
Methods: Selecting an optimal window size (Uddin et al. 2017)) and modularity class (Louvain clustering in Gephi©). Nodes (n=165) are represented as black for adult-males and grey for all other individuals and edge thickness represents the strength of the connection between two nodes; the thicker the edge, the closer the individuals in the progression. Same progression as
Figure S2.3, progression details listed above.
51
CHAPTER THREE:
FEEDING COMPETITION INFERRED FROM PATCH
DEPLETION
52
Chapter Three: Feeding competition inferred from patch depletion
Abstract
Competition for food is often a cost associated with living in a group, and can occur both within and between groups. Several socioecological factors can determine the degree of competition, which may occur in an indirect (scramble) or direct (contest) form. I investigated feeding competition in a supergroup of Rwenzori colobus monkeys (Colobus angolensis ruwenzorii) in Nyungwe National Park, Rwanda. The supergroup, numbering >500 individuals, forms a multilevel society comprised of at least two tiers of social organisation (uni-male/multi-female and multi-male/multi-female units) and offers an opportunity to investigate whether freedom from scramble competition allows these monkeys to form supergroups. I utilised the patch depletion method to study competition (Snaith and Chapman 2005), measuring intake rate coupled with movement rate to assess if patches become depleted of food items over the occupancy period. Within patches, the colobus displayed scramble competition for young leaves, but not for mature leaves or fruit. When individuals fed on young leaves, over time intake declined and effort increased, indicating individuals scramble for young leaves as they are consumed in the patch. However, this pattern did not occur when feeding on fruit, suggesting the colobus are not scrambling for this food source. Opposing forces may impact this supergroup: within-band scramble occurring for certain foods, whereas between-group contest competition may explain why larger groups (units/or aggregations of units) were able to occupy patches for longer. Although feeding competition exists for select resources, the lack of competition observed for mature leaves may enable Rwenzori colobus to live in a supergroup of hundreds of individuals in this montane forest.
53
Introduction
Living in a group presents a variety of costs and benefits to group members (Clutton-Brock
2016; Janson and Goldsmith 1995; Schulke and Ostner 2012). Larger groups can be beneficial to group members through enhanced protection from predators and conspecifics (Clutton‐
Brock et al. 1999; Fitzgibbon 1990; Grueter and van Schaik 2010; Olson et al. 2013; Pulliam
1973; Roberts 1996; Turner and Pitcher 1986), a competitive advantage when defending resources (Fashing 2001b; Wrangham 1980), and access to alloparental care (Riedman 1982).
However, group living has its set-backs, such as the increased potential for disease transmission
(Alexander 1974; Altizer et al. 2003; Brown and Brown 1986; Cross et al. 2005; Freeland
1976) and reduced foraging efficiency (which is an indicator of feeding competition) (Gillespie and Chapman 2001; Snaith and Chapman 2007).
The cost of feeding competition drives diversification in the size and structure of groups
(Alexander 1974; Rubenstein 1986; Schulke and Ostner 2012; Wrangham 1980) and the temporal fluidity of groups (Gaulin et al. 1980; Kummer 1971). Competition for resources may be direct (contest), or indirect (scramble) (Alcock 1980; Janson 1988). Contest competition occurs as one or more individuals impede others from utilising a resource by means of subtle or aggressive interactions (Grueter et al. 2016; Janson and van Schaik 1988; Koenig and
Borries 2002; Shopland 1987; Vogel 2005; Wrangham 1980), and can occur within and/or between groups (Scarry 2013; Su and Birky 2007). For example, within-group contest competition occurred between individual Taiwanese macaques (Macaca cyclopis) in food patches in the form of agonistic behaviour (Su and Birky 2007), and between-group contest occurred in tufted capuchin monkeys (Sapajus nigritus) where groups containing more males were better able to defend their core area from other groups (Scarry 2013). Scramble competition occurs when the resource at stake is freely available, but the uptake by some limits the eventual uptake by others and can occur both within and between groups (Chapman and
54
Chapman 2000b; van Schaik and van Hooff 1983). For example, red colobus monkeys
(Piliocolobus tephrosceles) feeding on leaves moved further to forage (higher foraging effort) when there were more individuals in a patch (Snaith and Chapman 2005).
Leaves are widely available in rainforests and provide a food source to many folivorous primates (Harris 2006; Julliot and Sabatier 1993). However, many folivorous primates prefer fruits, seeds, flowers and young leaves over mature leaves (Chapman and Chapman 2002;
Koenig et al. 1998; Milton 1979; Remis 1997; Rogers et al. 1990; Yeager and Kool 2000), and most tropical trees display seasonal variation in availability of young leaves and fruits, especially where rainfall seasonality is pronounced (Kaplin et al. 1998; Reich and Borchert
1984; van Schaik and Pfannes 2005; Wright and van Schaik 1994). Howlers (Alouatta sp.) are probably the most folivorous of the New World monkeys (Julliot and Sabatier 1993; Silver et al. 1998), and guerezas (Colobus guereza) are arguably the most folivorous of the Old World primates (Harris 2006; Oates 1977a); nevertheless, for both taxa, fruit provides an important seasonal food source at least for some populations (Fashing 2001a; Julliot and Sabatier 1993).
All African colobines are considered to be mostly folivorous, with the exception of C. satanas, however dietary variation exists between species and between populations. The most folivorous populations of each species include: C. vellerosus at Boabeng-Fiema (79% leaves)
(Saj and Sicotte 2007), C. polykomos on Tiwai Island (58% leaves) (Dasilva 1994), C. angolensis at Nyungwe National Park (72% leaves) (Fimbel et al. 2001), and C. guereza at
Kibale (>80%) (Clutton-brock 1975; Harris and Chapman 2007; Oates 1977b; Wasserman and
Chapman 2003). Other highly folivorous Old World primates include western red colobus
(Piliocolobus badius) at Tai National Park, Cote d’Ivoire (75% leaves) (McGraw et al. 2016) and proboscis monkeys (Nasalis larvatus) at Sukau, Bornean Malaysia (>70% leaves)
(Boonratana 2003). Like the African colobines, for howlers (Alouatta sp.), the degree of folivory can vary between populations and species (Dias and Rangel-Negrín 2015), but a diet
55 composed of >80% leaves has been recorded for multiple species and populations; A. caraya and A. guariba in Brazil, A. palliata in Costa Rica, Mexico and Honduras, A. pigra in Belize and Mexico, and A. seniculus in Columbia (Dias and Rangel-Negrín 2015).
The ecological constraints model proposes that – all else being equal – within-group feeding competition increases with group size (Chapman et al. 1995; Janson 1988; Milton 1984;
Wrangham et al. 1993). Larger group sizes often are linked to increased daily path lengths and more extensive home ranges, as more individuals deplete resources more rapidly (Chapman and Chapman 2000a; Isbell 1991; Janson and Goldsmith 1995; Suzuki 1979; Teichroeb and
Sicotte 2009). For example, larger groups of red colobus travelled more and rested less than a smaller group suggesting larger group sizes lead to increased levels of within-group scramble competition (Gillespie and Chapman 2001). However, contrasting with earlier hypotheses that within-group scramble competition is either weak or absent among folivores (Clutton-Brock and Harvey 1977; Isbell 1991; Janson and Goldsmith 1995; van Schaik and van Hooff 1983;
Yeager and Kirkpatrick 1998), the pressures associated with living in a large group may be more similar for folivores and frugivores than once thought (Majolo et al. 2008; Sayers 2016;
Snaith and Chapman 2007).
A small number of primate species form extremely large supergroups numbering hundreds of individuals, including the geladas (Theropithecus gelada) in Ethiopia (Snyder-Mackler et al.
2012b), hamadryas baboons (Papio hamadryas) on the Horn of Africa (Schreier and Swedell
2009), snub-nosed monkeys (Rhinopithecus spp.) in China (Kirkpatrick and Grueter 2010), mandrills (Mandrillus sphinx) in Gabon (Rogers et al. 1996) and Rwenzori black-and-white colobus (Colobus angolensis ruwenzorii) in Rwanda (Vedder and Fashing 2002). The ability to cleave and coalesce along social fissure lines (such as between units or clans) is key to alleviating within-group competition in multilevel societies in response to fluctuating food abundance (Kummer 1971; Schreier and Swedell 2012). For example, a band of hamadryas
56 baboons broke into smaller social groupings (clan or unit) when preferred food was unavailable, or food was less available (Schreier and Swedell 2012), thus reducing levels of food competition.
In the high-altitude, mountainous forest of Nyungwe National Park, Rwanda, Rwenzori colobus form large supergroups (Vedder and Fashing 2002) with over 500 individuals (Miller, pers. obs.) and at a lowland site at Lake Nabugabo in Uganda, Rwenzori colobus also form temporary associations of over a hundred individuals (Arseneau-Robar et al. 2018). However, this is a relatively unusual occurrence for black-and-white colobus, as elsewhere in Africa, they typically live in relatively small groups of 2 to 20 individuals (Fashing 2006; Oates 1994).
Based on recent research in Nyungwe (Chapter Two) and Nabugabo (Stead and Teichroeb
2019), these colobus are organised into a multilevel society with uni-male/multi-female and multi-male/ multi-female units, a social organisation not observed in other African colobines.
Fimbel et al. (2001) showed that the high-quality foliage which was higher in nutritional quality
(protein : fibre) than other African sites may facilitate supergrouping with limited intragroup feeding competition. Feeding competition in the form of within-group scramble is observed in populations of red colobus (Snaith and Chapman 2005) and black-and-white colobus
(Teichroeb and Sicotte 2009) with group sizes far smaller than those observed in Nyungwe. It is unknown whether resource-based competition exists within the supergroups of Rwenzori colobus in Rwanda, but the increased feeding and moving time and reduced resting time of
Rwenzori colobus at this site, compared to other populations of black-and-white colobus
(Fashing et al. 2007a), suggest intragroup scramble competition may occur.
The Marginal Value Theorem proposes that when foraging becomes uneconomical in a patch, and the patch is no longer worth exploiting, animals will move to a new patch (Chapman 1988;
Charnov 1976; Pyke 1984; Snaith and Chapman 2005). Snaith and Chapman (2005) utilised
‘the patch depletion method’ method to quantify scramble competition within groups of red
57 colobus in Kibale National Park, Uganda. According to this method, scramble competition is indicated by slowed intake of resources coupled with increased movement effort to uptake resources. This method was also later utilised by Tombak et al. (2012) to study feeding competition in guerezas, also in Kibale. One strength of this method is that it does not rely on comparisons between groups in order to estimate scramble competition, as comparing groups of different sizes may be confounded by differences in the temporal or spatial supply of food in different habitats (van Schaik and van Noordwijk 1988).
Herein, I investigate the levels of feeding competition within a supergroup of Rwenzori colobus in Nyungwe National Park, Rwanda. Using the patch depletion method, I aimed to examine intake rates and movement rates of Rwenzori colobus feeding in patches of different food items
(young leaves, mature leaves and fruit) to assess if this large supergroup, or foraging groups within the supergroup, experience scramble competition. This multilevel supergroup is divided into units with a mean of 9.3 individuals (Chapter Two). As multiple ‘units’ often occupied patches I refer to these congregations of individuals in patches as ‘groups’. I also draw inferences about between-group contests which can interact with within-group scramble to affect foraging efficiency (Grueter et al. 2018; Janson and van Schaik 1988; Koenig 2000;
Stevenson and Castellanos 2000; Teichroeb and Sicotte 2018). Specifically, the presence of scramble competition would be supported if 1) individuals have both a diminished intake rate and an increased movement rate throughout patch occupancy, and 2) patch occupancy time increased in larger food patches and/or for smaller groups. In contrast, a diminished intake rate associated with a decreased movement rate will be indicative of satiation rather than scramble competition. Between-group contest is indicated if groups are displaced from a patch, coupled with immediate uptake by new individuals. The supergroup of Rwenzori colobus present in
Nyungwe provides a unique opportunity to investigate the impact of between-unit/group contest and within-band scramble competition at different levels of social organisation, in an
58 arboreal African colobine with an unusual social organisation and grouping pattern compared to previously studied colobines.
Methods
Study site
This study took place in Nyungwe National Park, south-western Rwanda (1013 km²; 2°15’-
2°55’ S, 29°00’-29°30’E, elevation 1600-2950 m) from July 2016 to August 2017. Nyungwe is a mosaic of primary and secondary forest patches and is carpeted in most parts by a thick herbaceous layer (Kaplin et al. 1998). The forest has two rainy seasons (September to
November, and January to March; monthly rainfall > 100 mm) and two dry seasons (April to
August, and December, monthly rainfall < 100 mm), total annual rainfall was 1671 mm
(Nyirambangutse et al. 2017). Based on climate data collected from the Uwinka Meteostation
(2° 28' 43'' S, 29° 12' 00'' E, elevation 2465 m), the mean temperature for the study period (July
2016 to August 2017) was 14.9°C.
Study species
In Nyungwe National Park there is one habituated supergroup of Rwenzori colobus (Colobus angolensis ruwenzorii), typically consisting of at least 250-300 individuals, and peaking at 512 individuals in February 2017 (Chapter Two). My field assistant and I followed the habituated supergroup of Rwenzori colobus for 1180 hours over a period of 13 months. We collected data on patch depletion over nine months (November 2016-July 2017), arriving to the group at
~08:00 and following it until ~17:00 (mean number of days per month: 11.1, range: 7-14; mean number of consecutive day follows per month: 7.1, range: 2-14). The colobus tolerated human presence comfortably at an average distance of ≥15 m. The band size fluctuated throughout the study period, at times splintering into smaller parties of ~50 individuals on days when they were being hunted by chimpanzees. When fission occurred, we stayed with the larger group
59
(the research team followed only one group or band at a time). Other smaller unhabituated groups of ~50 individuals also have ranges overlapping with the large habituated focal group but were not followed during this study.
Patch depletion method
We observed feeding by Rwenzori colobus in patches using the patch depletion method
(Charnov 1976; Snaith and Chapman 2005; Tombak et al. 2012). For this study, a patch is defined as a single tree, and includes all food items which may occur in/on the tree including tree leaves, fruit, flowers, foliose or fruticose lichen, epiphytes, and any vines (stems and leaves) growing on the tree. Observed patches were chosen opportunistically as colobus individuals entered a tree to feed. I randomly selected a feeding individual, and observed it for
3 minutes. Each minute I recorded the intake rate (number of bites), and after 3 minutes my research assistant recorded total distance moved (realised path length in estimated metres) in the 3-minute period (foraging effort). Intake (bite/s) was monitored using binoculars (Leica©
8x50 BA Binoculars); each new item bitten or placed in the monkey’s mouth was recorded as a bite. After observing one individual for 3 minutes, I would immediately switch to a different individual and observe it for 3 minutes. One observer watched individuals and counted number of bites/min eaten in 3 minutes, and distance moved in 3 minutes, while the second observer recorded total number of individuals in the tree, and total number of feeding individuals. For each observed individual I recorded age and sex, and the consumed food species and plant part: young leaves (YL), mature leaves (ML), leaves (L; when leaf type could not be identified), unripe fruit (UF), ripe fruit (RF), flowers (F), flower buds (FB), lichen (Li), seeds (S), epiphytes
(EP), and moss (M). In one patch it is possible for multiple food types to be consumed when dietary switching occurs as a preferred food becomes depleted. For each feeding patch period
I recorded the start time (when the first individual started to feed) and end time (when the last individual ceased feeding) of data collection. For each patch, I recorded tree species, plant part
60
(s) consumed, and diameter at breast height (DBH). DBH was used as a patch level estimate of food availability, assuming that DBH is a proxy measure of tree crown volume (Chapman et al. 1992).
Data collection continued until all individuals in the patch ceased to feed. If all individuals left the patch but new individuals immediately moved into the patch, I recorded this as a new feeding event. Thus, a feeding event includes the same set of individuals in a patch until the group leaves the patch or a replacing set of individuals arrives. Multiple feeding events could occur in a single feeding patch if different sets of individuals successively occupied and fed in the patch. The supergroup generally fed during slow directional travel, which ensured that resampling of individuals did not occur. ‘New individuals’ would enter from one side, while others would exit and move the other way. Group displacements were recorded as a sign of contest competition between units/or groups for patches. A displacement event was defined as all individuals leaving a patch (tree) within 1 minute of a new set arriving, suggesting a ‘forced’ or pressured exit, rather than more casual movement between patches. I observed both single and multiple social units occupying patches. Group size in patches ranged from 1-55 individuals, and the mean unit size for Rwenzori colobus is 9.3 individuals (Chapter Two).
Thus, as multiple ‘units’ often occupied patches I refer to these congregations of individuals in patches as ‘groups’.
Data analyses
Patch depletion
I used paired t-tests to assess feeding intake and effort, comparing bite number/min and metres moved/3 min between the first and last quarter of each period of patch occupancy. The data were analysed for all food patches together, and then were separated by food type to look at young leaves, mature leaves and fruit, separately. When calculating intake rate per food type
61 category, I also included patches where dietary switching occurred and multiple food types were consumed within a patch; however, to calculate movement rate I only used those patches where the calculated food type was being eaten exclusively. Data did not deviate markedly from a normal distribution.
Patch level variables
I used linear mixed models (LMM) to investigate the effects of food availability (DBH as a proxy measure), and group size (independent variables) on total patch feeding time in minutes
(dependent variable). Statistical unit of analysis for the patch residence time analyses was a single patch. To control for repeated sampling of the same species across patches, tree species constituting a feeding patch was included as a random factor in the model. Since social unit displacement in a patch resulted in a constrained time in the patch, the feeding events terminated by displacements were removed for this analysis (n=6). Statistical analyses were performed in R version 3.3.1 (R Core Team 2015), and LMMs were conducted using the packages lme4 (Bates et al. 2015) and lmerTest (Kuznetsova et al. 2015).
Results
Patch descriptors, consumption and group sizes
From November 2016 to July 2017, data were collected on individuals feeding in patches (n=38 patches), with a total of 45 feeding events. The total number of patch occupancy hours was
47.3, of which 40.9 hours was spent feeding. Patches included nine tree species (Table 3.1).
Feeding patch data were collected opportunistically, and are not representative of overall feeding time.
62
Table 3.1. Tree species constituting feeding patches, number of patches per tree species and plant parts consumed per tree species by Rwenzori colobus during feeding events.
Species # Mean Plant parts eaten* patches DBH (cm) Ilex mitis (Aquifoliaceae) 14 57.8 UF, RF Alangium chinense (Alangiaceae) 13 51.8 YL, ML, FB, FL, LI Polyscias fulva (Araliaceae) 4 60.7 FB, LI, YL, FL, ML, EPY, FR Tabernaemontana stapfiana 2 43.1 YL, ML (Apocynaceae) Dombeya goetzenii (Sterculiaceae) 1 46.8 ML Macaranga kilimandscharica 1 32.8 LI (Euphorbiaceae) Syzgium guineense (Myrtaceae) 1 62.1 LI Strombosia scheffleri (Olacaceae) 1 65.0 RF Sapium ellipticum (Euphorbiaceae) 1 42.3 UF *YL = young leaves; ML = mature leaves; UF = unripe fruit; RF = ripe fruit; LI = lichen; FL = flower; FB = flower bud; EPY = epiphytic ferns. Mean DBH is the average of species DBH from patches.
In the observed patches, fruit comprised 49% of consumption (bites) (32% ripe fruit, 7% unripe fruit, 10% unspecified fruit, n=13,845 bites), leaves 43% (24% young leaves, 10% mature leaves, 9% unspecified leaves, n=12,046 bites), flowers and flower buds 5% (n=1437 bites) and lichen and epiphytes 3%. The colobus had the fastest intake rates when consuming fruit
(mean=17.9 bites/min, range=0-46 bites/min, SD ±9.4) and slowest when consuming leaves
(mean=9.6 bites/min, range=0-30 bites/min, SD ±5.3) (Figure 3.1). Number of individuals in a single patch (tree) (i.e. group size, some may not be feeding) ranged from 1 to 55 individuals
(x=15.0, SD=10.55, n=38), and feeding group size (i.e. number of feeding individuals in a tree) ranged from 1 to 54 individuals (x=9.7, SD=9.71, n=38). Mean patch occupancy was 78 min
(range 10-245 min, SD=61.79, n=38).
63
Figure 3.1. Box plot for intake rate (bites/min) of different food types consumed by Rwenzori colobus in patches. Number of 1-minute observations per food category: 1) young leaves
(n=668), 2) mature leaves (n=365), 3) fruit (n=738), 4) flower parts (n=119), and 5) lichen
(n=58). The middle line within the box represents the median, the top line represents the 75th percentile, the bottom line represents the 25th percentile, and the unfilled circles represent the outliers.
Testing for within-group scramble competition: patch depletion method
For all food types combined, a decreased intake rate was associated with an increased movement rate in the last quarter of patch occupancy compared to the first quarter (Figure 3.2,
Table 3.2). When separated by food type, I found the same trend for young leaves: intake rate decreased significantly and movement rate increased significantly over patch occupancy
(Figure 3.2, Table 3.2).
For mature leaves, I observed the opposite pattern, with an increased intake rate over patch occupancy (number of bites in first compared to last quarter), paired with an increased
64 movement effort. Finally, for fruit, only intake rate changed significantly, decreasing over patch occupancy, but movement rate did not change significantly (Table 3.2).
Figure 3.2. Changes in intake rate (bites/min) and distance moved (m/3 min) between first
(start) and last quarter (end) of patch occupancy for: all patches combined, young leaves, mature leaves and fruit for Rwenzori black-and-white colobus in Nyungwe National Park,
Rwanda, * indicates p<0.05, and ** indicates p<0.001 level of significance between the start and end (first vs last quarter) of the observation session, S. D lines indicated on bars.
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Table 3.2. Changes in mean (x) intake rate (bites/min) and mean (x) distance moved (m/3 min) between first (start) and last quarter (end) of patch occupancy for: all patches combined, young leaves, mature leaves and fruit for Rwenzori black-and-white colobus in Nyungwe National
Park, Rwanda.
Food type consumed in patch Intake rate (bites/min) n Start End t p Combined food types 45 x=13.44 x=12.06 3.62 <0.001 Young leaves 21 x=8.08 x=6.24 4.38 <0.0001 Mature leaves 24 x=3.80 x=5.79 4.56 <0.0001 Fruit 12 x=18.74 x=15.61 3.88 <0.001 Movement rate (m/3 min) n Start End t p Combined food types 45 x=1.78 x=2.20 3.62 <0.001 Young leaves 9 x=1.53 x=2.43 -2.52 0.013 Mature leaves 5 x=0.97 x=1.82 -2.34 0.025 Fruit 11 x=2.34 x=2.45 -0.38 0.70
Dietary switching
I observed a switch in proportional consumption of food types when comparing the 1st to the
4th quarter: with the percentage of young leaves decreasing and the percentage of mature leaves increasing (Table 3.3).
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Table 3.3. Differences in the composition of food items during the 1st compared to the 4th quarter of the patch occupancy period for different dietary items: young leaves, mature leaves, fruit, lichen, and flower parts.
Contribution to feeding quarter (%) Young leaves Mature leaves Fruit Lichen Flower parts 1st quarter 40.2 24.0 27.6 6.1 2.2 4th quarter 29.7 34.8 24.2 5.5 6.4
Group size and patch occupancy
When controlling for DBH, group size (but not feeding group size) had a significant positive effect on both patch feeding time and patch occupancy time (Tables 3.4-3.7). Bigger groups spent more time feeding in a patch, resulting in longer patch residence time and patch feeding time (Table 3.4 & 3.6).
Table 3.4. LMM investigating the effect of mean group size and food availability (DBH) on patch feeding time (minutes) in Rwenzori colobus in food patches (df=28).
Variables Estimate Std. Error t stat p Intercept 1.62 0.20 8.22 - DBH 0.00 0.00 -1.52 0.14 Group size 0.02 0.01 3.27 0.003
Table 3.5. LMM investigating the effect of mean feeding group size and food availability
(DBH) on patch feeding time (minutes) in Rwenzori colobus in food patches (df=28).
Variables Estimate Std. Error t stat p Intercept 1.72 0.22 7.63 - DBH 0.00 0.00 -1.03 0.31 Feeding group size 0.01 0.01 1.69 0.10
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Table 3.6. LMM investigating the effect of mean group size and food availability (DBH) on patch occupancy time (minutes) in Rwenzori colobus in food patches (df=28).
Variables Estimate Std. Error t stat p Intercept 66.65 32.91 2.02 - DBH -0.82 0.50 -1.62 0.11 Group size 3.47 1.18 2.94 0.006
Table 3.7. LMM investigating the effect of mean feeding group size and food availability
(DBH) on patch occupancy time (minutes) in Rwenzori colobus in food patches (df=28).
Variables Estimate Std. Error t stat p Intercept 86.80 37.44 2.32 - DBH -0.69 0.58 -1.21 0.24 Feeding group size 1.84 1.41 1.41 0.20
Between-group contest
Field observations suggest that contest competition may occur between groups/or units when in feeding patches. I observed six displacement events over the study period. Four of the six displacement events were for ripe fruit of Ilex mitis, and two displacements were for young leaves of Alangium chinense. Displaced and displacing subunits were pursuing the same food types in the contested patches. Displacements were generally accompanied by 1) vigilant individuals observed ‘waiting in the wings’ in nearby trees, 2) aggressive chases either from individuals in/or outside the patch, or 3) displacement events where all individuals left the patch within 1 minute of a new set arriving. Arriving in ones or twos into a patch joining others was normal; but a rapid exit of all individuals in the patch followed by a rapid entry of different individuals was not as common.
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Discussion
I investigated the competition dynamics in food patches of a supergroup of Rwenzori colobus in the mountainous forest of Nyungwe. Based on the patch depletion method previously used to study feeding competition in colobines at Kibale (Snaith and Chapman 2005; Tombak et al.
2012), I found evidence of scramble competition within the supergroup. When individuals fed on young leaves intake declined and effort increased over time, indicating individuals scramble for young leaves as they are consumed in the patch. However, this pattern did not occur when feeding on fruit, suggesting the colobus are not scrambling for this food source. The colobus increased intake rates of mature leaves and increased foraging effort over patch occupancy, which is suggestive of dietary switching; as preferred food items (young leaves) are depleted, the colobus switch to less preferable mature leaves. These results are in line with several other recent studies showing that scramble competition is prevalent among folivorous primates
(Gillespie and Chapman 2001; Grueter et al. 2018; Snaith and Chapman 2008; Steenbeek and van Schaik 2001; Teichroeb and Sicotte 2009).
Scramble competition has not been observed in patch depletion studies on the relatively small groups of guerezas in Uganda or Kenya (Fashing 2001a; Tombak et al. 2012), but has been observed in large groups of red colobus in Uganda (Snaith and Chapman 2005), and in the white-thighed colobus (Colobus vellerosus) in Ghana (Saj and Sicotte 2007). Although feeding competition was not the focus of the study on guerezas in Kakamega Forest, Kenya, Fashing
(2001a) found potential evidence of scramble competition based on longer daily path length for the largest study group, suggesting that beyond a threshold of 15-20 members, some levels of feeding competition may occur. Additionally, Fashing et al. (2007a) recorded increased feeding and moving time, and reduced resting time of Rwenzori colobus in Nyungwe compared to other black-and-white colobus populations, providing additional evidence that scramble competition occurs in this supergroup. Previously it was suggested that it is the differing
69 digestive physiologies of red colobus and guerezas that account for the observed differences in feeding competition (Tombak et al. 2012). However, Rwenzori colobus are certainly more like guerezas in terms of digestive physiology and size, and do experience within-group scramble competition; thus, it is more likely to be group size or localised food availability rather than digestive physiology that dictates the presence of scramble competition in black-and-white colobus and leads to the observed differences between sites and across species of African colobines.
Contrary to expectations, bigger groups spent more time feeding in a patch. This was unexpected as generally larger groups deplete patches more readily (Altmann 1974; Gillespie and Chapman 2001; Snaith and Chapman 2005), resulting in shorter patch residence times
(Isabirye-Basuta 1988). The results of longer patch residency and feeding time in larger groups may accord with a contest-competition based scenario whereby competitively superior groups incur foraging privileges through patch usurpation. However, it is unclear why larger groups monopolise or usurp patches even though average intake rate declines with increasing patch residence time. The finding that group size positively correlates with patch feeding and residency time could be caused by four alternative explanations: 1) perhaps the cost of moving to another patch outweighs the benefits of diminished intake rates while staying put, which would make it beneficial to remain at food patches longer before moving (Charnov 1976).
Alternatively, 2) it could be due to sequential feeding by individuals, resulting in longer time in patches. Wallace (2008) observed that larger subgroups of black spider monkeys (Ateles chamek) spent more time in patches than smaller subgroups, presumably because a finite number of feeding positions existed within the patch necessitating sequential feeding, or taking turns. In the present study, group size but not feeding group size affected overall patch feeding time, which may indicate – similar to Wallace (2008) – that colobus are taking turns to feed while others rest or socialise in the patch, resulting in longer bouts of patch feeding. Or 3)
70 smaller groups may be pressured to prematurely depart patches and re-join the supergroup.
Kazahari (2014) found Japanese macaques (Macaca fuscata) often left patches for social reasons rather than because of diminishing returns and spent longer in patches with more co- feeders (Kazahari and Agetsuma 2008). I suggest that with larger groups occupying a patch, there is less pressure to follow those moving off to new feeding areas. Future studies should measure within-group cohesion, and band spread to assess if social isolation is a factor influencing individual decisions to vacate a patch, which in turn would affect patch residency times. Lastly, 4) an increase in ‘social monitoring’ in larger groups (Gosselin-Ildari and Koenig
2012; Kutsukake 2007; Teichroeb and Sicotte 2012), interspersed with feeding, may prolong overall patch residency and patch feeding time. This may arise in the form of competitively motivated social monitoring (Gosselin-Ildari and Koenig 2012; Hirsch 2002), for example,
Hirsch (2002) found when studying brown capuchin monkeys (Cebus apella) vigilance increased as the number of neighbours increased. I did not measure vigilance behaviour in feeding patches, but suggest this as a potential explanation; as multiple social units are likely simultaneously occupying patches when group size is large, thus social monitoring of neighbours may impede feeding/foraging efficiency.
Another mechanism linking longer patch occupancy to group size may be active supplantation of smaller groups from patches or avoidance of patches by subordinate groups (van Schaik
1989; Wrangham 1980). Larger units, or collections of more closely associated units may occupy patches preventing others from moving into the patch by crowding the patch, or displaying aggressive territorial behaviour. Little is known about dominance associated with group rank in colobines, and the associated foraging privileges and consequences of between- group contest. Harris (2006) reports that higher-ranked guereza groups that win and initiate more encounters, feed in core areas with a higher quantity and quality of food. This is similar to the anecdotal findings of Grueter et al. (2009a), where one-male units of black-and-white
71 snub-nosed monkeys (Rhinopithecus bieti) occupied leafing trees, resulting in other units waiting in trees nearby while feeding on less-preferred food items. I observed six patches which were categorised as being contested. This was based on observations of vigilant individuals
‘waiting in the wings’ in nearby trees, aggressive chases either from individuals in/or outside the patch, or displacement events where all individuals left the patch within one minute of a new set arriving. Arriving in ones or twos into a patch joining others was normal, but a rapid exit of all individuals in the patch followed by a rapid entry of a different set of individuals was not as common (n=6 displacements). Four of the six contested patches were fruiting Ilex mitis trees, which were seasonally covered in small fruits (est. >1000 ripe berries/m3) (A. Miller, pers. obs.). At this density, with an average consumption rate of 18 berries/min, I estimate it would take one individual one hour to deplete a 1m3 portion of the patch. With an extremely high density of food in one patch, and decreasing intake rates over time, forming a coalition with other units may be a beneficial strategy to allow patch monopolisation by a sub-set of the supergroup. I do not have evidence that coalitions are being formed, but suggest this as a possible scenario, as higher-level groupings, such as ‘clans’ consisting of more closely associating units, are known from other multilevel primate societies (Schreier and Swedell
2009).
Notwithstanding the evidence of scramble and possibly contest competition in this group, the lack of competition over high-quality mature foliage together with the utilisation of lichen as a fallback food (Chapter Four) may facilitate the establishment of large multilevel societies. In multilevel primate societies, the natural fissure lines between social units lend themselves to a fluid response to changes in food availability (Schreier and Swedell 2009) and can alleviate the pressures of feeding competition. For example, in the Filoha region of Ethiopia, hamadryas baboons fission and fuse in response to changes in food availability (Schreier and Swedell
2012). Regular fission-fusion events also occur in black-and-white snub-nosed monkeys in
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China, where the band routinely splits into two subgroups at the same site and time of the year to exploit young bamboo shoots which are a high-quality and preferred food source (Ren et al.
2012). In addition, geladas regularly fission and fuse in response to patchily distributed foods
(Hunter 2001), and group sizes exhibit considerable temporal variation (Snyder-Mackler et al.
2012b). Fissuring into subgroups on varying temporal scales may allow Rwenzori colobus to exploit patchily dispersed resources, or high-quality clumped food patches, similar to hamadryas baboons, snub-nosed monkeys and geladas (Hunter 2001; Kummer 1968; Kummer
1971; Ren et al. 2012; Schreier and Swedell 2009).
In conclusion, I provide evidence that Rwenzori colobus do exhibit scramble competition for young leaves. Longer patch feeding times and occupancy periods by larger groups may be indicative of between-group contests, but other interpretations are also possible. In this study, opposing forces may be at play: within-group scramble may limit group size in patches, whereas the benefits of increased feeding time with larger groups may favour larger group size despite the costs of scramble competition. A lack of competition for high-quality mature leaves, the utilisation of fruticose lichen as a fallback food (Chapter Four), and a multilevel structure with fission-fusion dynamics (Chapter Two), allowing the supergroup to cleave and coalesce into bigger or smaller social units, are likely the factors which allow the formation of a supergroup despite apparent feeding competition for resources in Nyungwe.
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CHAPTER FOUR:
DIET AND USE OF FALLBACK FOODS BY
RWENZORI COLOBUS: IMPLICATIONS FOR
SUPERGROUP FORMATION
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Chapter Four: Diet and use of fallback foods by Rwenzori colobus:
Implications for supergroup formation
Abstract
When preferred foods are scarce, one strategy employed by animals is to switch to an alternate food item of lower quality or preferability; this is termed a fallback food. In the montane rainforest of Nyungwe National Park in south-western Rwanda, Rwenzori colobus (Colobus angolensis ruwenzorii) form supergroups comprised of hundreds of individuals. I investigated how a supergroup uses resources in periods of resource abundance vs periods of resource scarcity. When the availability of preferred food species was low, fruticose lichen (Usnea sp.) contributed over >50% of the monthly diet for the Rwenzori colobus. Moreover, their consumption was significantly negatively related to availability of preferred foods. Fruticose lichen can therefore be considered a fallback food for Rwenzori colobus which sustains the supergroups during periods of reduced food availability. This result, in combination with previous findings that mature foliage in Nyungwe is of high quality (Fimbel et al. 2001) and does not elicit feeding competition (Chapter Three), points to the importance of resources in facilitating supergroup formation. However, a number of other montane forests in Eastern
Africa also have fruticose lichen and yet support only small groups of Angolan colobus, suggesting that additional factors such as sufficient forest size and absence of fragmentation and hunting pressure by humans are required for supergroups to form.
Introduction
In tropical forests, resources are often seasonal, for example, flushes of young leaves following rains in Central Africa (Remis 1997), bamboo shoots in the Albertine Rift mountains (Watts
1984), or fruit during the dry season in the rainforest of Sumatra (van Schaik and van
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Noordwijk 1985). This variability of food resources over space and time impacts on primates who respond to the fluctuating abundance of fruit, young leaves, flowers, and seeds (Grueter
2017; Peres 1994; van Schaik et al. 1993). Few primates rely on the same food type year-round, but rather adapt to what is available (Hemingway and Bynum 2005). For example, ripe fruit is a preferred food for a number of primates (Leighton 1993; Tutin et al. 1997), but primates often face seasonal or annual shortages in availability (Jordano 2000). To deal with lean ‘in-between’ times, primates characteristically employ flexible feeding strategies (le Gros Clark 1966), such as relying on fallback foods which are generally abundant year-round, but are relatively poor in nutrition and may also be mechanically challenging (Hanya et al. 2004; Knott 2005; Lambert et al. 2004; Sauther and Cuozzo 2009).
Fallback foods are defined as “foods whose use is negatively correlated with the availability of preferred foods” (Altmann 1998; Marshall and Wrangham 2007, p 1220), and represent a variety of forms depending on primate taxon and environment. Examples of primate fallback foods include herbs (Davenport et al. 2010), seeds (Ma et al. 2017), lianas (Dasilva 1994), figs
(Clink et al. 2017), lichens (Grueter et al. 2009b), fruit (Sauther and Cuozzo 2009), bark (Knott
1998), exudates (Porter et al. 2009), invertebrates (Mosdossy et al. 2015), crops (Chancellor et al. 2012), and aquatic and terrestrial underground storage organs (Fashing et al. 2014; Marlowe and Berbesque 2009; Wrangham et al. 2009). Fallback foods may be less nutritious and/or harder to digest (Stanford and Nkurunungi 2003), require specialised dental or digestive characteristics (Lambert 2007), or are high-quality but mechanically challenging and/or time consuming to extract or manipulate (Mosdossy et al. 2015; Sauther and Cuozzo 2009). For example, tamarind fruit, eaten as a fallback food by ring-tailed lemurs (Lemur catta), is energy- rich but extraction results in tooth wear (Sauther and Cuozzo 2009), and invertebrates eaten by white-faced capuchin monkeys (Cebus capucinus), are a high-quality food source, but require long handling time (Mosdossy et al. 2015). Utilising fallback foods is common as a response
76 to periods of resource scarcity; for example, snub-nosed monkeys (Rhinopithecus bieti) rely on fruticose lichen as a fallback food to buffer groups through winter in a high-altitude forest in
China (Ding and Zhao 2004; Grueter et al. 2009b; Kirkpatrick 1996).
Altering group size via fission-fusion (Aureli et al. 2008), or altering foraging behaviour via daily path length (Yamagiwa and Basabose 2006), are other strategies used to deal with varying food availability (Dolado et al. 2016; Doran 1997). Groups may fission in response to reduced food availability (Asensio et al. 2009; Coles et al. 2012; Schreier and Swedell 2012), or to the presence of a high-quality food resource (Holmes et al. 2016; Ren et al. 2012; Rimbach et al.
2014) presumably to alleviate feeding competition (Asensio et al. 2009; Lehmann et al. 2007).
For example, a band of black-and-white snub-nosed monkeys (Rhinopithecus bieti) fissioned into smaller foraging subgroups to exploit young bamboo shoots which were a high-quality and preferred food source (Ren, Li, Garber, & Li, 2012). Alternatively, hamadryas baboons
(Papio hamadryas) fissioned into smaller foraging parties when there was diminished food availability (Schreier and Swedell 2012).
Certain habitats are characterised by more intense periods of resource scarcity than are others.
In particular, montane ecosystems or high-altitude forests experience scarce or physically/chemically altered resources, because in general species richness, diversity and productivity generally decline as elevation increases (Luo et al. 2004; Rahbek 1995). Thus, primates in montane ecosystems may need to alter their diets by employing dietary switching to survive (Grueter et al. 2009b; Owens et al. 2015). On Bioko Island, Equatorial Guinea, lowland drills (Mandrillus leucophaeus poensis) (0-300 m above sea level) had a more frugivorous diet than their higher altitude dwelling neighbours (500-1000 m a.s.l) who predominantly fed on herbaceous pith, leaves and fungi (Owens et al. 2015). In addition, high- altitude dwelling primates may be acutely impacted by winter conditions, which present challenges of food shortages for a number of months, forcing some to switch to a diet of lichen,
77 buds and bark (Grueter et al. 2009b; Nakagawa 1989, 1997). Subtropical and tropical montane forests, which are predominantly broadleaf, receive consistent moisture via high-humidity conditions resulting in a thick cover of mosses and lichen on ground and vegetation (Frahm
1990; Seifriz 1924). In tropical high-altitude forests, similar to their temperate counterparts, lichen is also an important resource for some primates (Porter 2001; Vedder and Fashing 2002).
However, consuming lichen or fungi as a predominant part of the diet, annually or seasonally is more unusual, and has been observed in geographically and taxonomically divergent species
(Kirkpatrick 1996; Ménard et al. 1985; Porter 2001; Vedder and Fashing 2002). Lichens are also important resources to human inhabitants of mountainous settlements in Nepal, and the significance of this resource increases with altitude (Devkota et al. 2017). Similarly, black-and- white snub-nosed monkeys have been recorded seasonally spending up to a staggering 95% of feeding time eating lichens (Kirkpatrick 1996; Xiang et al. 2007), and for Rwenzori colobus in
Nyungwe, Vedder and Fashing (2002) found lichen to be an important dietary item seasonally making up a large proportion of their diet, but this result was not recorded by Fimbel et al.
(2001).
In Nyungwe National Park, Rwanda, (1600-2950 m a.s.l), Rwenzori black-and-white colobus
(Colobus angolensis ruwenzorii) form a supergroup comprising over 500 individuals (Chapter
Two). Rwenzori colobus in Nyungwe consume substantial amounts of lichen (Vedder and
Fashing 2002), and this dietary trait, combined with large group size, is uncommon amongst black-and-white colobus (Fashing et al. 2007a; Vedder and Fashing 2002). Fimbel et al. (2001) found that Nyungwe has an abundance of high-quality mature leaves, which were higher in nutritional quality than other African sites. It has been proposed that it is this high-quality foliage which are thought to support supergroups (Fashing et al. 2007a; Fimbel et al. 2001). If so, do these monkeys utilise a fallback food to sustain supergroups through periods of diminished resources? I present new data on Rwenzori colobus feeding ecology based on a 13-
78 month study conducted in Nyungwe. I first examine the diet of the Rwenzori colobus and identify preferred foods, and then test the hypothesis that Rwenzori colobus utilise a fallback food when preferred foods are at reduced availability, specifically lichen and/or mature leaves.
The objective of this study is to better understand the feeding ecology and utilisation of fallback foods of Rwenzori colobus. In particular, investigating the relationship of feeding ecology to the formation of a supergroup in this high-altitude forest in Rwanda.
Methods
Study site and species
This study took place in Nyungwe National Park, south-western Rwanda (1013 km²; 2°15’-
2°55’ S, 29°00’-29°30’E, elevation 1600-2950 m). Data collection spanned 13 months, from
19th July 2016 to 22nd August 2017 for a total of 1180 hours. Nyungwe National Park is a large and diverse montane rainforest, comprising primary and secondary forest (Plumptre et al.
2002). For this study the research team was based at Uwinka outpost in the north of the Park
(Figure 4.1), with surrounding forest predominated by Syzygium guineense, Beilshmiedia rwandensis, Macaranga kilimandscharica and Neoboutonia macrocalyx, and extensive herbaceous valleys covered with Sericostachys scandens vines (Fischer and Killmann 2008).
The annual climate is separated into rainy (September to November, and January to March; monthly rainfall >100 mm) and dry periods (April to August, and December, monthly rainfall
<100 mm). The mean temperature for the study period was 14.9°C, mean daily minima and maxima were 12.6°C and 18.8°C, and total rainfall was 1671 mm (Nyirambangutse et al. 2017)
(Figure 4.2).
My research assistant and I followed a habituated supergroup of Rwenzori black-and-white colobus monkeys for 1180 hours over 12 months, collecting data in all months. This supergroup is likely the same as followed by Fimbel et al. (2001) and Fashing et al. (2007b) as there is only
79 one habituated supergroup in the National Park. Colobus follows began at ~08:00 and lasted until ~17:00 across all months (mean number of observation days per month: 11.1, range: 7-
14; mean number of consecutive day follows per month: 7.1, range: 2-14). The colobus tolerate human presence comfortably at an average distance of ~15 m. This habituated supergroup is tracked regularly by the Rwanda Development Board (RDB) trackers. The supergroup (or band) typically consisted of at least 250-300 individuals, and peaked at 512 individuals in
February 2017, but band size fluctuated throughout the study period. On a few occasions, predation by chimpanzees (Pan troglodytes schweinfurthii) triggered short-term fission of the supergroup (19th July 2016, 26th November 2016, 20th February 2017, 21st May 2017, 19th June
2017), causing it to splinter into small groups of ~50 individuals. Only on the 19th July 2016 was a successful hunt witnessed by observers. When fission occurred, we stayed with the larger group, and only followed one group at a time. Each group had at least one individual we could identify, and ranged in separate regions of the national park, ≥2 km apart. In addition, non- habituated groups of Rwenzori colobus with approximately 50 individuals were observed to share partial range overlap with the main study group.
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Figure 4.1. Map of Rwanda (right) and Nyungwe National Park (left) by K. Meisterhans and
C. C. Grueter; adapted from Nyungwe National Park Management Plan 2012-21.
Figure 4.2. Monthly variation of temperature at rainfall at Nyungwe National Park, Rwanda, between July 2016 and August 2017.
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Observational data collection
From July 2016 to August 2017, together with one trained research assistant, I collected systematic data on activity patterns via instantaneous scan-sampling (Altmann 1974). During scans, I randomly selected a focal individual (all age-sex classes, excluding infants, Table S2.1) and recorded its activity (feed, rest, feed, forage, move, vigilant, groom, play, mate, aggress) as well as the activities of all individuals within 30 m proximity of the focal animal. I collected a total of 1257 scans and 5,603 feeding records. If the focal individual was feeding, I recorded the food species and plant part consumed. Food plant parts recorded included leaves (young or mature), fruits (unripe or ripe), flower parts (flowers or buds), herbaceous vegetation (including terrestrial herbaceous vegetation and herbaceous vines), lichen (fruticose or foliose), seeds (i.e. pods, capsules or seed), tree bark, epiphytes, moss, clay, dead wood and milk (nursing young).
If fleshy pericarp of fruit/drupe was consumed but seed was discarded, this was considered fruit-eating. All food trees and herbaceous vines/plants were identified to species if possible by the field team, or by using the “Illustrated Field Guide to the Plants of Nyungwe National Park
Rwanda” (Fischer and Killmann 2008). If the species could not be identified at the time, photos were taken of the leaves and any flowers/fruit present, and samples were collected for identification by a RDB or Wildlife Conservation Society (WCS) staff member with botanical knowledge at Uwinka reception. In general, chemical/nutritional studies find differences between the leaves of trees and herbs/lianas; nutrient storage (N, P, Ca, K, Na) is lower in the leaves of herbs than in tree foliage (Marks et al. 1988; Rothman et al. 2006; Singh and Singh
1993), so I have separated these into different dietary categories.
Phenological monitoring and vegetation sampling
To assess spatial and temporal variation in food availability, I established phenology trails with experienced field assistants, and for 12 months (September 2016-August 2017), monitored
82 phenological changes in 832 individual plants of DBH >10 cm from 57 species (45 tree, 4 shrub, 3 liana, and 5 epiphytic strangler species) known or presumed to be eaten by Rwenzori colobus. Thirteen species were excluded from the analysis because the colobus did not feed on them (10 tree, and three epiphytic species). During the first 5 days of each month, along a series of trails dispersed across the home range, the research team observed each tree crown and trunk using binoculars (Leica© 8x50 BA Binoculars) to monitor the abundance of ripe fruit, unripe fruit, young leaves, mature leaves, flowers, flower buds, lichen, and seeds (i.e. pods, capsules or seed). Abundance on the tree crown of the different food items were scored on a scale from
0 to 4 based on coverage; 0: absence, 1: 1-25%, 2: 26-50%, 3: 51-75% and 4: 76-100%. For each tree we recorded diameter at breast height (DBH) and height (m, visually estimated). We also created tagged observation points on the trail in order to re-locate each tree every month.
We monitored a minimum of 15 individual trees per species where possible (range=3-34).
Limited published information was available on species eaten by Rwenzori colobus, see species lists in Fimbel et al. (2001) and Fashing et al. (2007a), so I relied on local researchers, guides and trackers to assist in compiling a species list to monitor. The same team of field personnel collected the phenology data throughout the 12-month field period, and inter‐observer reliability was assessed regularly throughout the study period and deemed satisfactory.
Food availability index
Together with two field assistants, I established 60 randomly located plots (10 m2) that were distributed throughout the home range of the study group. Plot locations within the colobus home range were randomly generated as points in a geographic information system model
(Quantum GIS Development Team 2012). In each plot we recorded the following variables for each tree (DBH >10 cm): species, circumference at breast height (CBH), and height (estimate, m). To estimate herbaceous vegetation cover in each plot, we recorded total herbaceous vegetation cover (% of area), and also individual cover (% of area) estimates of species
83 consumed by the colobus (Impatiens sp., Ipomea sp., Sericostachys scandens, Mikaniopsis usambarensis, Triumfetta cordifolia, Momordica foestida). I used the following formula to calculate a monthly food availability index (FAI) for each tree species and liana species
(Basabose 2002):
FAI= ∑ Pkm x Bk
Where Pkm is the proportion of trees presenting the specified food item for species k in month
2 m, and Bk is the total basal area of species k in the forest (m per ha; determined from plot survey, calculated using basal area (BA) data from DBH measurements). A separate Pkm was calculated for all monitored species and food items (i.e. ripe fruit, unripe fruit, young leaves, mature leaves, flowers, flower buds, lichen, and seeds. Incorporated into our measure of Pkm was the phenological score for each food item per tree (Wittiger and Boesch 2013).
To obtain a monthly food availability index (FAI) I used the phenology data (incorporated into our measure of Pkm was the phenological score for each food item per tree) (Wittiger and
Boesch 2013) using the following equation:
Pkm = 0.25 x Nkm (score 1) + 0.5 x Nkm (score 2) + 0.75 x Nkm (score 3) + 1 x Nkm (score 4)
Where N is the number of individual trees for species k in month m, and scores and proportions relate to the phenological score for species k that month (0: absence, 1: 1-25%, 2: 26-50%, 3:
51-75% and 4: 76-100%). So, Pkm is the sum of the proportion of species k in month m with food items present weighted according to item yield. The calculated Bk, combined with Pkm, were used to obtain the final food availability index (FAI) for each species per month.
Abundance indices were calculated for each species and were summed for all species within food categories: total fruit=FAITF, unripe fruit=FAIUF, ripe fruit=FAIRF, young leaves=FAINL, mature leaves=FAIML, flower parts=FAIFL, herbaceous vegetation=FAITHV, lichen=FAILI, and
84 preferred foods=FAIPREF (FAIPREF: summed preferred species parts; see Data analysis:
Preferred and Fallback foods). For 15 species for which density could not be estimated from plots (not encountered) I set the density as 0.01 (sq. m per ha), so that availability calculations reflected their presence.
Data analysis
Diet description
Monthly diet was determined using the proportion of each plant part ingested per scan averaged over the number of scans per month. I calculated the mean annual diet using the mean percent of feeding records for each diet category across the 12 study months. I defined “important species” as those plant species occurring in more than 10% of sampled days to represent species eaten regularly even if not intensively (McLennan 2013; Moscovice et al. 2007).
Diet seasonality
To test if the consumption of the important fruit species followed a seasonal pattern, I performed for each plant species a generalised linear model with binomial error structure and logit link function where the presence/absence of each species consumed on a sample day is the response. The predictor was a seasonality term derived from the sine and cosine of the date, transformed to a circular variable (2 x pi x day/365; Grueter et al. 2014). I checked the overall effect of seasonality on species plant part consumption using a likelihood ratio test. I used the
R2 coefficient of determination (Nagelkerke 1991) to compute a comparable value among species.
Preferred and fallback foods
To determine the preferred food items, I ranked (1 to n; 1 being least preferred) each consumed food item per month, a) based on diet frequency and b) availability in the habitat. I then used
85 these rankings for each food item (i.e. species; part eaten), to calculate the preference scores
(EI) using Ivlev’s electivity index (Ganas et al. 2008; Watts 1984):
EI= (rd - na) / (rd + na)
Where rd is the monthly rank of the food item in the diet, and na is the monthly rank of availability of each food item. Scores between -1 and 0 indicated that a food was not preferred, a score of 0 signified neutrality, and a score between 0 and 1 indicated that it was preferred.
I categorised fallback foods as those food categories or species whose consumption increases when preferred foods/or preferred food categories are less available (Altmann 1998; Doran‐
Sheehy et al. 2009; Grueter et al. 2009b). Pearson’s correlations were used to examine how feeding time on potential fallback foods (lichen, terrestrial vegetation, and mature leaves) changed in accordance with availability of total fruit (FAITF), ripe fruit (FAIRF), young leaves
(FAIYL) and preferred foods (FAIPREF). Bonferroni corrections were used when making multiple comparisons. All data analyses were carried out in RStudio v1.1.383 software (R Core
Team 2017).
Results
Phenological patterns
Availability of fruit, flowers and young leaves peaked from October to November, whereas other plant parts were less seasonal. Both ripe and unripe fruit peaked in October 2016, young leaves peaked in October/November 2016, mature leaves were consistently available throughout the year, and more flowers were available in October/November 2016 (Figure 4.3).
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Figure 4.3. Availability of mature leaves, lichen, young leaves, fruit, and flower parts, for tree species eaten by Rwenzori black-and-white colobus in Nyungwe National Park.
Diet description
Over the 12-month study period, I identified 67 plant species consumed by the colobus as well as clay (Table 4.1). The data collection period was sufficient to identify the majority of diet species based on the observed asymptote when the cumulative number of species was plotted against sampling time, but is unlikely to capture every consumed species. The annual diet of the colobus was composed of 36.5% leaves (9.8% young leaves, 26.7% mature leaves; n=55 species), 15.6% fruits (n=16 species), 20.6% lichen (n=≥2 species), 12.8% herbaceous vegetation (n=18 species), flower parts (4.5% flowers, 1.2% flower buds; n=10 species), bark
(6.7%), clay (0.9%), and other (epiphytes, moss, dead wood; 0.9%) (Table 4.1, Table S4.1,
Figure 4.4).
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Table 4.1. Annual consumption (% of feeding scans) of all species consumed during scans, ranked most to least consumed, plant parts are indicated (including % annual consumption):
LE (leaf), FR (fruit), FL (flower), FB (flower bud), LI (lichen), OF (old fruit on ground), EPY
(epiphyte), BK (bark), YL (young leaf), italicized= not observed during scan, +exotic species.
Plant part Species Rank Species Family annual annual # consumption consumption (%) (%) 1 Ilex mitis Aquifoliaceae LE (12.22), FR 17.20 (4.64), FL (0.34), LI 2 Usnea sp. lichen Parmeliaceae LI (13.79) 13.79 3 Strombosia scheffleri Olacaceae FR (11.42), LE 12.02 (0.60), OF, LI 4 Polyscias fulva Araliaceae FL (2.39), FB 9.85 (0.50), FR (4.22), LE (2.73), LI, Leaf stem 5 Alangium chinense Alangiaceae FB (0.45), YL 8.90 (5.23), ML (3.21), FL 6 Foliose lichen Parmeliaceae LI (6.48) 6.48 7 Zanthoxylum gilletti Rutaceae LE (4.30), LI 4.30 8 Lianas * - LE (3.96), FL 3.96 9 Ipomea sp. Convolvulaceae LE (3.81) 3.81 10 Sericostachys scandens Amaranthaceae LE (3.81) 3.81 11 Tabernaemontana stapfiana Apocynaceae LE (3.12) 3.12 12 Dombeya goetzenii Sterculiaceae LE (1.77), LI 1.77 13 Sapium ellipticum Euphorbiaceae FR (1.18), LE, EPY 1.18 14 Albizia gummifera Fabaceae LE (1.03), SE 1.03 15 Mikaniopsis usambarensis Asteraceae LE (0.90) 0.90 16 Triumfetta cordifolia Tiliaceae LE (0.82) 0.82 17 Olea hochstetteri Oleaceae LE (0.71), LI 0.71 18 Chrysophyllum rwandensis Sapotaceae FR (0.09), LE 0.65 (0.56), LI 19 Eucalyptus sp. + Myrtaceae FR (0.24), LE 0.63 (0.56), FL, BK 20 Salacia erecta Hippocrateaceae FR (0.48), LE 0.62 (0.13) 21 Ficus oreodryadum Moraceae FR (0.02), LE 0.58 (0.56) 22 Neoboutonia macrocalyx Euphorbiaceae LE (0.54), LI 0.54 23 Apodytes dimidiata Metteniusaceae LE (0.41) 0.41 24 Cassipourea ruwensorensis Rhizophoraceae LE (0.39), LI 0.39
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25 Ocotea usambarensis Lauraceae FB (0.22), LE 0.39 (0.17), LI 26 Syzygium guineense Myrtaceae FR (0.06), LE 0.35 (0.29), LI, EPY 27 Schefflera goetzenii Araliaceae FL (0.02), FB 0.34 (0.02), FR (0.02), LE (0.28) 28 Momordica foestida Cucurbitaceae LE (0.32) 0.32 29 Cleistanthus polystachyus Phyllanthaceae LE (0.19), BK 0.19 30 Schefflera myriantha Araliaceae LE (0.17), FL, FR 0.17 31 Macaranga kilimanjarica Euphorbiaceae LE (0.11), FR, LI 0.11 32 Bridelia brideliifolia Euphorbiaceae FB (0.06), LE 0.11 (0.05) 33 Prunus africana Rosaceae FR (0.11), LE, LI 0.11 34 Balthasarea schliebenii Theaceae FR (0.09) 0.09 35 Hagenia abyssinica Rosaceae LE (0.09) 0.09 36 Xymalos monospora Monimiaceae LE (0.07) 0.07 37 Ficalhoa laurifolia Theaceae LE (0.06), LI 0.06 38 Symphonia globulifera Clusiaceae LE (0.04) 0.04 39 Ekibergia capensis Meliaceae LE (0.02), LI 0.02 40 Galienera saxifraga Rubiaceae LE (0.02) 0.02 41 Impatiens sp. Balsaminaceae LE (0.02) 0.02 Species consumed outside of scan periods Alchornea hirtella Euphorbiaceae LE - Beilschmiedia rwandensis Lauraceae LI, FR, LE, FL - Bersama abyssinica Francoaceae LE - Carapa grandiflora Meliaceae LI, FR skin - Elaphoglossum sp. Lomariopsidaceae LE - Ficus othorinipholia Moraceae LE - Harungana montana Hypericaceae LE - Lepidotrichilia volkensii Meliaceae LE - Magnistipulata butayei Chrysobalanaceae FR - Moss Bryophyta Moss - Myrianthus holistii Urticaceae FR - Newtonia buccanii Fabaceae LE - Noxia congestens - LE - Ocotea kenyensis Lauraceae FR - Olinia roscheliana - YL - Parinari exelsa Chrysobalanaceae LE, LI - Pavetta rwandensis Rubiaceae LE - Vimprise bautonizii - LE - Unknown ficus Moraceae YL, FB - *6 species of lianas (Gouania longispicata, Urera sp. Cleradenron sp., Monanthotaxis orophila, Mikania chenopodifolia, Unknown vine 1).
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Seasonal variation in dietary composition
The diet of Rwenzori colobus in Nyungwe National Park changed seasonally (Figure 4.4). The colobus consumed the most fruit in May-August 2017 (mainly Strombosia scheffleri, Ilex mitis,
Polyscias fulva, and Chrysophyllum rwandensis). Tree leaf consumption peaked in October
(young and mature; mainly Alangium chinense, Tabernaemontana stapfiana, and Albizia gummifera), herbaceous vegetation consumption was more consistent throughout the study period but peaked in October (mainly Ipomea sp., Sericostachys scandens, and Triumfetta sp.).
Lichen consumption (Usnea sp.) was highest in March and April (>50% of the monthly diet), flower part consumption was highest in December-February (mainly Polyscias fulva, Ocotea usumbarensis and Ilex mitis), and consumption of ‘other’ food items was highest in December
(Eucalyptus sp. tree bark and clay). In the diet of scanned individuals, the families
Euphorbiaceae, Moraceae and Lauraceae were represented by the most species (Table 4.1).
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Figure 4.4. The percentage of monthly diet feeding on lichen, fruit, young leaves, mature leaves, young leaves and other (flower parts, herbaceous vegetation, bark, clay, dead wood, epiphytes); data based on scans.
Preferred and fallback foods
Out of 67 plant parts (and lichen) from 41 species (tree species, herbaceous vegetation species, lichen and lianas), there were 19 preferred plant items (average preference score: >0) (Table
S4.2), which comprised flower buds, fruits, and leaves. Three of the eight important tree species
(Ilex mitis, Zanthoxylum gilletti, Alangium chinense) were identified as preferred species
(Table 4.2). Flower buds of Ocotea usambarensis ranked as the most preferred food part (0.80)
(Table S4.2). Of the preferred plant items, eight had a narrow consumption window of one month. Lichen (n=2) and all terrestrial herbs (n=6) (Impatiens sp., Ipomea sp., Sericostachys scandens, Mikaniopsis usambarensis, Triumfetta cordifolia, Momordica foestida) ranked among the non-preferred food items. Rwenzori colobus consumed two of the 19 preferred food
91 parts in accordance with their availability (Table S4.3): Tabernaemontana stapfiana young leaves (n=12, r=0.54, p<0.001), and Alangium chinense mature leaves (n=12, r=0.36, p=0.04).
The consumption of plant parts of six of the eight important species followed a seasonal pattern
(likelihood ratio test, Table 4.2) and the effect of seasonality was strongest for consumption of fruticose lichen (Usnea sp.), and was also generally stronger for fruit (Strombosia scheffleri,
Polyscias fulva, Ilex mitis) [R2 in Table 4.2 & Figure 4.5]. The two herbs among the important species were consumed throughout the year as indicated by low seasonal variation in amplitude
(small R2).
Turning to the question of fallback foods for Rwenzori colobus, only the consumption of fruticose lichen was negatively correlated with the availability of preferred foods (FAIPREF)
(n=12, r=-0.69, p=0.01) (Table 4.3 & Figure 4.6). There was a positive correlation between consumption of mature leaves and availability of preferred foods (n=12, r=0.67, p=0.02), indicating it is unlikely to be a fallback food. There was no significant correlation between preferred food availability and consumption of terrestrial vegetation/flower parts, indicating these food categories are unlikely to be fallback foods for Rwenzori colobus during the study period.
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Table 4.2. Important species in Rwenzori colobus diet.
Plant species No. days (%) Plant part Mean monthly Avg. pref. Seasonality Preferred Fallback consumed diet (%) (SD) score (EI) X2 p R2 Lichen 93 (62.0) Fruticose 11.2 (21.8) -0.15 71.53 ** 0.76 No Yes Foliose 7.2 (6.4) -0.23 7.30 * 0.07 No No Strombosia scheffleri 61 (40.7) Fruit 10.6 (9.4) -0.10 15.99 *** 0.14 No No Leaves 0.9 (1.75) -0.51 18.19 *** 0.30 No No Polyscias fulva 55 (36.7) Flower bud 0.4 (0.8) -0.15 4.94 N.S 0.10 No No Fruit 3.8 (7.8) -0.15 36.82 *** 0.45 No No Flower 3.1 (5.2) -0.30 19.07 *** 0.24 No No Mature leaves 1.7 (1.9) -0.47 4.46 N.S 0.05 No No Young leaves 0.8 (1.3) -0.47 5.04 N.S 0.11 No No Ilex mitis 42 (28.0) Ripe fruit 3.1 (7.9) 0.11 36.42 *** 0.56 Yes No Young leaves 7.7 (11.5) -0.03 0.07 N.S 0.0007 No No Unripe fruit 0.5 (1.1) -0.08 13.43 ** 0.65 No No Mature leaves 6.0 (3.7) -0.10 6.80 * 0.07 No No Sericostachys scandens 37 (24.7) Leaves 4.0 (3.1) -0.41 0.30 N.S 0.003 No No Ipomea spp. 26 (17.3) Leaves 4.2 (6.9) -0.28 7.65 * 0.08 No No Zanthoxylum gilletti 19 (12.7) Young leaves 0.6 (1.9) 0.54 0.78 N.S 0.02 Yes No Mature leaves 2.6 (3.1) 0.39 1.84 N.S 0.02 Yes No Alangium chinense 18 (12.0) Young leaves 5.9 (9.9) 0.24 19.06 *** 0.25 Yes No Mature leaves 3.7 (6.5) 0.06 1.89 N.S 0.02 Yes No Flower bud 0.4 (0.9) -0.12 1.23 N.S 0.18 No No Note: No. days (%) the species was consumed was used to determine important species, mean monthly diet (%) is the average percent that the species plant part was consumed across all months in feeding scan observations, Average preference scores (EI) were calculated using Ivlev’s electivity index, based on each species plant part; monthly rank in the diet, and the monthly rank of availability (Table S2). Seasonality p-values indicate the significance of the chi likelihood ratio test comparing the model with the seasonality term to a model without this predictor (***p<0.0001, **p<0.001, *p<0.05, N.S.: not significant). Seasonality (R2) indicates the coefficient of determination, i.e. the proportion of variance explained by the regression model.
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Figure 4.5. Seasonality in time spent feeding on important species/plant parts from September
2016 to August 2017. Only species/plant parts showing significant seasonality are presented.
Months are indicated by a single letter on the x-axis. Species part consumption (Y) or absence
(N) on feeding days is on the y-axis; circles indicating presence/absence are overlaid so that colour corresponds to the intensity to which feeding points were clustered in time. The fitted models are indicated by the solid/dashed lines.
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Table 4.3. Pearson correlation matrix comparing consumption and availability of plant parts; ripe fruit (FAIRF), total fruit (FAITF), young leaves (FAIYL), preferred foods (FAIPREF) and consumption of potential fallback foods by Rwenzori colobus: lichen, mature leaves, and terrestrial herbaceous vegetation (THV).
Availability (FAI) Ripe fruit Total Fruit Young leaves Pref. Foods Consumption r p r p r p r p % total lichen -0.57 0.05 -0.45 0.13 -0.63 0.03 -0.62 0.03 % foliose lichen -0.15 0.63 -0.11 0.72 -0.17 0.60 0.57 0.05 % fruticose lichen -0.44 0.15 -0.35 0.26 -0.48 0.11 -0.69 0.01 % mature leaves 0.89 <0.001 0.90 <0.001 0.71 <0.001 0.67 0.02 % THV in diet -0.30 0.35 -0.21 0.50 -0.45 0.14 -0.15 0.64 In bold are p<0.01 (threshold for Bonferroni correction with 5 multiple comparisons).
Figure 4.6. a) Consumption of lichens in relation to availability of preferred food for Rwenzori colobus in Nyungwe; Pearson correlation between FAIPREF and the percentage of monthly consumption of fruticose lichen, and b) Rwenzori colobus feeding on bunches of the hair-like fruticose lichen (Usnea sp.).
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Discussion
I present data on seasonal variation in the diet of Rwenzori colobus in Nyungwe and the use of a fallback food. Lichen, specifically fruticose lichen, constitutes a fallback food for the
Rwenzori colobus supergroup, as it was continuously available, non-preferred, and consumption was negatively correlated with the availability of preferred foods, meeting the definition of a fallback food. During the lean period, when preferred foods were least available, the colobus switched from intermittently picking foliose lichen off tree trunks to gathering bunches of the hair-like fruticose Usnea sp. lichen. Staple fallback items are available year- round and may seasonally make up 100% of the diet whereas filler fallback items are also consistently available but may be ignored for weeks at a time and never make up 100% of the diet (Marshall and Wrangham 2007). The fruticose lichen was ignored by the colobus for most of the year and consumed in large amounts only during the lean season, so it does not quite fit the definition of either category, but is more in line with a filler fallback food. However, lichens
(fruticose and foliose combined) were eaten in every month by Rwenzori colobus and seasonally comprise a large proportion of the diet when preferred foods were unavailable, and hence can be considered a staple fallback food.
Lichens inhabit most temperate, marginal or extreme environments, such as high-elevation mountains, and polar regions (Iversen et al. 2013), and the majority of mammals who consume them do so seasonally, e.g. snub-nosed monkeys and macaques (Grueter et al. 2009b; Hanya et al. 2011; Tsuji et al. 2013), humans (Devkota et al. 2017), polar bears (Iversen et al. 2013), voles (Ure and Maser 1982), squirrels (McKeever 1960), reindeer (Pegau 1968) and deer (Ward and Marcum 2005). Lichens are pandemic, inhabit most terrestrial ecosystems, and can tolerate a spectrum of harsh environmental conditions (Nash 2008). Lichens are low in fibrous components, high in nonstructural carbohydrates, and are highly digestible (Kirkpatrick 1996;
Nash 2008). Specifically, fruticose lichens are low in calories, condensed tannins and crude
96 proteins, and are high in nonstructural carbohydrates (Bissell 2014a, 2014b; Liu 2012).
Fruticose lichens (Usnea longissima and Bryoria spp.) were also recorded as a staple fallback for the black-and-white snub-nosed monkeys in the mountains of China, constituting up to
100% of the diet in winter (Grueter et al. 2009b). Vedder and Fashing (2002) found a similar seasonal contribution of lichen to the diet of Rwenzori colobus in Nyungwe; in contrast, Fimbel et al. (2001) reported a minimal contribution of lichen to the diet of Rwenzori colobus in
Nyungwe. However, Fimbel et al. (2001) reported different seasonal phenology patterns to the present study (in particular the timing of fruit availability), and these studies were widely separated in time from one-another, which suggests the conflicting findings may be the result of inter-annual variability in food availability, or a greater availability of preferred foods (e.g. young leaves). When Rwenzori colobus fed on fruticose lichen during the resource-scarce months (March and April) they also fed on a number of other non-preferred species such as leaves of the trees Macaranga kilimanjarica and Syzygium guineense, the terrestrial herbs
Sericostachys scandens, Triumfetta sp., Ipomea sp., and species not observed in the diet prior to the food scarcity period (lianas: Monanthotaxis oreophila and Mikania chenopodifolia). In contrast, during a period of resource scarcity in the Samage Forest when there were virtually no fruits and digestible leaves, snub-nosed monkeys fed almost entirely on fruticose lichen
(Grueter et al. 2009b). Temperate forests are characterised by having a higher density of fewer tree species compared to a tropical forest (Janzen 1970; Richards 1952), and a lean season for fruit coincides with a lean season for leaves, enhancing the effect of resource-scarcity bottlenecks. Like other high-altitude forests (Luo et al. 2004; Rahbek 1995), phenology results show that Nyungwe experiences limitations in food, especially those of preferred species, from
March through May, however, Nyungwe has ample non-seasonal food resources (lichen, mature leaves, terrestrial herbs, and herbaceous lianas) which can be exploited when preferred foods are not available.
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I argue that fruticose lichen in addition to high-quality mature leaves allow supergroup formation in Nyungwe. However, similarly large groups of Angolan colobus are not known to occur in any other montane tropical areas with similar characteristics. Angolan colobus occur in several other high-altitude forests in Eastern Africa, including Kibira National Park in
Burundi, and Mahale, Usambara and Udzungwa mountains in Tanzania. However, despite similar altitude, tree species and abundances of fruticose lichen, Angolan colobus do not form supergroups at those sites (Marshall 2007; Nishida et al. 1981; Preston 2011). Kibira National
Park (1,600-2,666 m a.s.l), is a contiguous forest to Nyungwe, contains the same tree species, and yet Rwenzori colobus there form relatively small groups (mean=25 individuals;
Hakizimana, pers. comm.). This pattern may be due to historical factors. Kibira NP has fragmented into four districts due to forest clearing; Rwenzori colobus are now restricted to the northernmost district (Hakizimana 2014), and are hunted for skins (Hakizimana, pers. comm.).
Differences in group sizes can be attributed to the different hunting histories: armed groups permanently occupied Kibira during the 1993–2007 conflict resulting in significant decreases in interventions relating to protection and extensive hunting of large mammals (Hakizimana et al. 2015; Hakizimana and Huynen 2013; OBPE 2014). In contrast, Nyungwe has experienced relatively brief lapses in protection over time (Crawford 2012; Rutagarama and Martin 2006;
Weber 1989), and poachers in Nyungwe more often uses snares (Moore et al. 2018), which are less effective than guns at capturing arboreal primates (Kümpel et al. 2009; Remis and Kpanou
2011). Similarly, in the Udzungwa Mountains, where Angolan colobus form small groups, there is considerable anthropogenic pressure with widespread hunting past and present (Hegerl et al. 2017; Jones et al. 2019; Marshall 2007; Nielsen 2006; Topp-Jørgensen et al. 2009). Local tribes surrounding the forests hunt colobus for meat and skins (Marshall 2007). In the DRC the majority of the human population live in rural forested regions and rely on bushmeat for food including primates (Nasi et al. 2011; Switzer et al. 2012). Although Rwenzori colobus may
98 once have been abundant in Kahuzi-Biega National Park, there has been considerable hunting of Angolan colobus at this site (Inogwabini et al. 2000; Kasereka et al. 2006). In addition, forty years ago, the dry coral-rag forest bordering the Indian ocean in Kenya, used to support groups of Angolan colobus twice as large as we see today (Dunham 2017; Moreno-Black 1974), but today groups are restricted to remnant habitat patches (Clarke 2000; Hawthorne 1993), and many other coastal populations have been extirpated by human hunting (Anderson et al. 2007).
Hunting pressure by humans can have a more negative impact on animal populations than habitat disturbance, and few primate populations are safe from hunting with relatively modern firearms (Oates 1996). Hunting is documented to reduce group size and also alter social organisation for other primates (e.g. simakobu Simias concolor; Erb et al. 2012; Watanabe
1981). I suggest that it is differences in land-use history (including fragmentation), forest contraction, and hunting that restricts Angolan colobus group sizes at other sites, despite apparent resource availability sufficient to facilitate supergroup formation.
In the lower altitude forest of Manwa Forest Reserve (1,136 m a.s.l) at Lake Nabugabo, central
Uganda, Rwenzori colobus form temporary supergroups of over 100 individuals, despite persisting in relatively small forest fragments surrounded by an anthropogenically modified landscape (Arseneau-Robar et al. 2018; Chapman et al. 2016). Local people practise small- scale agriculture and fishing, and appear to have a relatively low impact on primates in terms of hunting (Chapman et al. 2016). A brief bout of logging in the area resulted in Rwenzori colobus temporarily moving away from the disturbed area temporarily but did not appear to impact group size (Teichroeb et al. 2019). Nyungwe and Manwa Forest seem very different, yet they both support supergroups of Rwenzori colobus. Nyungwe is a large forest tract of 1013 km2, Manwa is a pocket of forest 2.8 km2 in size. The two sites differ in elevation and species composition and lie at different elevations (Arseneau-Robar et al. 2018; Plumptre et al. 2002), and lichen is consumed in small amounts at Manwa (S. Stead, pers. comm.), but both
99 populations experience low levels of hunting pressure (Chapman et al. 2016). Supergroups may thus have remained largely intact. Or alternatively, at Manwa, the extremely small forest size has squeezed groups into proximity, creating artificially elevated colobus densities. Angolan colobus (C. a. cottoni) have also been reported to form large multimale assemblages (n=36 individuals) in Ituri Forest, DRC (Bocian 1997b), with groups mixing to feed and travel together for several hours to more than one day. However, the group sizes are not comparable to those observed in Rwanda and Uganda, forming large groups rather than supergroups. The
Rwenzori colobus subspecies may be unique amongst the Angolan colobus in forming supergroups as we see in Rwanda and Uganda. Alternatively, it is possible that Angolan colobus historically formed large groups throughout the Albertine Rift Valley and Eastern Arc
Mountains and subsequent habitat degradation and hunting resulted in smaller group sizes.
The Angolan colobus have a wide geographical range across Africa, inhabiting small pockets of forest in human-modified landscapes (Anderson et al. 2007; Dunham 2017; Teichroeb et al.
2019), as well as large tracts of montane forest (Fashing et al. 2007a), with different levels of hunting pressure across those populations. The Rwenzori colobus in Nyungwe utilise fruticose lichen as a fallback food when preferred foods are diminished, which combined with a lack of competition (Chapter 3) for high-quality mature leaves (Fimbel et al. 2001), presumably allow these primates to form such large groups. However, in a number of other montane forests in
Burundi and Tanzania with similar tree species as well as fruticose lichen, the colobus form small groups, which suggests that lichen and high-quality leaves may create a resource base necessary to support colobus supergroups, but factors such as forest size, fragmentation, degradation and hunting may impact group sizes.
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Supplementary material
Table S4.1. Diet of C. angolensis at Nyungwe and other sites. The % composition of diet is presented for each site including young leaves (YL), mature leaves (ML), total leaves (TL), flowers (FL), fruit (FR), seeds (SE), and lichen (LI).
% composition of diet Study site* YL ML TL FL FR SE LI References Nyungwe, Rwanda 10 27 37 6 16 0a 21 This study Nyungwe, Rwanda 30 7 38 1 23 20b 32 Vedder and Fashing (2002) Nyungwe, Rwanda 25 40 72 5 17 <1c 5 Fimbel et al. (2001) Ituri, D.R.C 26 2 50 7 28 22d 0 Bocian (1997a) Salonga, D.R.C 21 6 27 6 17 50e 0 Maisels et al. (1994) Diani, Kenya 61 13 74 12 14 12f 0 Dunham (2017) *Only studies of ≥8 months included, aseed-eating (i.e. pods, capsules or seed) observed infrequently outside of focal period (all consumption of fruit/drupe pericarp regarded as fruit- eating if seed was dropped), binformation on seeds not available, cseed-eating not specified, dseed-eating included fruit of undetermined age; unripe seed, ripe seed or seed of undetermined age, unclear if pericarp and/or seed was eaten, eseed-eating included unripe fleshy fruit or unripe fruit with arillate seeds or immature and mature seeds from dry fruit (e.g. pods or capsules), unclear if pericarp and/or seed was eaten, f fruit-eating if both the outer flesh and internal elements (i.e., whole fruit) consumed or seed-eating if just the inner seeds (i.e., seed) consumed.
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Table S4.2. The food item preference ranks for all plant parts consumed by Rwenzori colobus; monthly percentage in the diet, average diet and availability rank, number of months in which they were consumed and average preference rank (most preferred to least preferred).
Plant species Part eaten Mean Avg. diet. Avg. # Avg. monthly diet rank (SD) avail. mo. pref. (%) (SD) rank (SD) score when consumed Ocotea usambarensis Flower buds 2.2 (0.0) 9.0 (0.0) 1.0 (0.0) 1 0.80 Tabernaemontana stapfiana Young leaves 3.5 (0.9) 9.0 (1.0) 1.5 (0.5) 2 0.71 Balthasarea schliebenii Fruit 0.8 (0.0) 5.0 (0.0) 1.0 (0.0) 1 0.67 Prunus africana Fruit 2.4 (0.0) 4.0 (0.0) 1.0 (0.0) 1 0.60 Zanthoxylum gilletti Young leaves 5.7 (1.1) 13.5 (1.5) 4.0 (1.0) 2 0.54 Chrysophyllum rwandensis Fruit 0.8 (0.0) 3.0 (0.0) 1.0 (0.0) 1 0.50 Tabernaemontana stapfiana Mature leaves 11.0 (5.0) 12.0 (2.5) 4.5 (2.4) 4 0.47 Schefflera myriantha Leaves 1.6 (0.0) 8.0 (0.0) 3.0 (0.0) 1 0.45 Zanthoxylum gilletti Mature leaves 5.2 (2.2) 11.2 (3.3) 4.8 (1.2) 6 0.39 Bridelia brideliifolia Flower bud 0.8 (0.0) 2.0 (0.0) 1.0 (0.0) 1 0.33 Sapium ellipticum Fruits 11.6 (0.0) 21.0 (0.0) 11.0 (0.0) 1 0.31 Alangium chinense Young leaves 10.2 (11.5) 8.8 (4.8) 5.3 (2.9) 7 0.24 Dombeya goetzenii Mature leaves 3.4 (3.1) 8.6 (4.3) 4.8 (2.2) 5 0.23 Eucalyptus sp. Fruit 0.87 (0.3) 4.0 (1.7) 4.0 (4.3) 3 0.17 Salacia erecta Fruit 0.89 (1.1) 3.0 (2.7) 1.5 (0.5) 6 0.16 Ilex mitis Ripe fruit 18.9 (6.6) 17.5 (0.5) 14.0 (2.0) 2 0.11 Cassipourea ruwensorensis Young leaves 4.1 (0.0) 7.0 (0.0) 6.0 (0.0) 1 0.08 Alangium chinense Mature leaves 7.4 (7.8) 8.3 (4.3) 7.2 (3.1) 6 0.06 Ficus oreodryadum Leaves 1.7 (1.3) 5.0 (2.6) 4.5 (1.3) 4 0.01 Schefflera goetzenii Leaves 0.9 (0.5) 3.2 (1.2) 3.7 (1.9) 4 -0.02 Ilex mitis Young leaves 11.5 (12.6) 10.7 (5.9) 10.5 (3.8) 8 -0.03 Cassipourea ruwensorensis Mature leaves 4.5 (0.0) 8.0 (0.0) 9.0 (0.0) 1 -0.06 Ilex mitis Unripe fruit 2.8 (0.6) 9.0 (1.0) 10.5 (0.5) 2 -0.08 Eucalyptus sp. Mature leaves 1.0 (0.8) 4.2 (3.3) 4.2 (2.1) 4 -0.09 Strombosia scheffleri Fruit 12.7 (8.8) 12.1 (5.4) 14.1 (7.1) 10 -0.10 Ilex mitis Mature leaves 6.0 (3.7) 9.8 (3.8) 11.8 (4.2) 12 -0.10 Alangium chinense Flower bud 2.2 (0.7) 8.5 (1.5) 10.5 (1.5) 2 -0.12 Ilex mitis Flower 4.9 (0.0) 9.0 (0.0) 12.0 (0.0) 1 -0.14 Polyscias fulva Flower bud 1.8 (0.4) 7.0 (0.0) 11.3 (7.7) 3 -0.15 Polyscias fulva Fruit 9.2 (10.2) 9.4 (4.7) 12.0 (4.1) 5 -0.15 Lichen 2 Usnea sp. Lichen 45.0 (18.3) 14 (1.7) 19.0 (3.6) 3 -0.15 Hagenia abyssinica Young leaves 0.5 (0.3) 2.5 (1.5) 3.0 (0.0) 2 -0.18 Bridelia brideliifolia Young leaves 0.8 (0.0) 2.0 (0.0) 3.0 (0.0) 1 -0.20 Lichen (Remototrachyna sp.) Lichen 9.6 (5.5) 11.8 (4.9) 18.3 (6.0) 9 -0.23 Apodytes dimidiata Mature leaves 1.3 (0.7) 4.3 (2.1) 7.0 (1.0) 3 -0.26 Salacia erecta Mature leaves 0.5 (0.4) 1.7 (1.1) 3.0 (1.7) 3 -0.27
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Ipomea sp. Leaves 6.3 (7.7) 8.5 (3.3) 15.4 (4.7) 8 -0.28 Polyscias fulva Flower 4.7 (5.8) 6.2 (4.9) 10.1 (4.1) 8 -0.30 Albizia gummifera Mature leaves 5.4 (8.2) 5.0 (3.6) 8.7 (4.7) 3 -0.31 Schefflera goetzenii Flower 0.2 (0.0) 1.0 (0.0) 2.0 (0.0) 1 -0.33 Ficus oreodryadum Fruit 0.1 (0.0) 1.0 (0.0) 2.0 (0.0) 1 -0.33 Apodytes dimidiata Young leaves 0.5 (0.0) 2.0 (0.0) 4.0 (0.0) 1 -0.33 Albisia gummifera Young Leaves 0.9 (0.4) 3.0 (1.0) 7.0 (2.0) 2 -0.41 Sericostachys scandens Leaves 4.3 (3.0) 8.4 (4.5) 18.7 (4.8) 11 -0.41 Lianas Leaves 3.9 (2.1) 8.8 (4.4) 20.5 (5.4) 11 -0.43 Ocotea usambarensis Young leaves 1.4 (0.0) 5.0 (0.0) 13.0 (0.0) 1 -0.44 Polyscias fulva Mature Leaves 2.0 (1.9) 4.9 (3.1) 10.1 (6.7) 10 -0.47 Polyscias fulva Young leaves 1.6 (1.4) 4.7 (2.3) 13.2 (3.9) 6 -0.47 Neoboutonia macrocalyx Leaves 2.0 (2.2) 4.0 (4.2) 10.0 (3.8) 4 -0.47 Schefflera goetzenii Fruit 0.2 (0.0) 1.0 (0.0) 3.0 (0.0) 1 -0.50 Strombosia scheffleri Leaves 2.6 (2.2) 5.2 (2.6) 17 (6.0) 4 -0.51 Xymalos monospora Leaves 0.4 (0.1) 2.0 (0.0) 6.5 (0.5) 2 -0.53 Olea hochstetteri Leaves 1.6 (0.9) 4.7 (2.8) 15.5 (6.0) 6 -0.53 Chrysophyllum rwandensis Young leaves 2.2 (2.8) 4.7 (2.1) 17.0 (4.3) 3 -0.55 Mikaniopsis usambarensis Leaves 1.6 (1.1) 5.8 (4.0) 18.0 (4.8) 6 -0.56 Cleistanthus polystachyus Leaves 0.7 (0.2) 3.0 (2.0) 10.0 (2.0) 3 -0.56 Triumfetta cordifolia Leaves 1.3 (1.1) 4.6 (3.3) 16.3 (4.8) 7 -0.59 Schefflera goetzenii Flower bud 0.2 (0.0) 1.0 (0.0) 4.0 (0.0) 1 -0.60 Macaranga kilimanjarica Young leaves 0.6 (0.4) 2.5 (1.5) 11.0 (3.0) 2 -0.60 Momordica foestida Leaves 1.8 (2.0) 4.7 (3.2) 18.7 (6.0) 3 -0.60 Galiniera saxifraga Leaves 0.4 (0.0) 1.0 (0.0) 5.0 (0.0) 1 -0.67 Ficalhoa laurifolia Leaves 0.5 (0.0) 3.0 (0.0) 16.0 (0.0) 1 -0.68 Syzygium guineense Leaves 0.8 (0.7) 3.5 (3.3) 19.0 (5.7) 4 -0.74 Ekebergia capensis Leaves 0.2 (0.0) 1.0 (0.0) 8.0 (0.0) 1 -0.78 Symphonia globulifera Leaves 0.4 (0.0) 2.0 (0.0) 19.0 (0.0) 1 -0.81 Syzygium guineense Fruit 0.4 (0.3) 1.5 (0.5) 14.0 (1.0) 2 -0.81 Impatiens sp. Leaves 0.4 (0.0) 1.0 (0.0) 10.0 (0.0) 1 -0.82
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Table S4.3. Phenological availability and consumption of preferred food parts.
Plant species Part eaten Avg. # mo. # mo. Consumption pref. consumed available and avail (R2) score Ocotea usambarensis Flower buds 0.80 1 5 0.05 Tabernaemontana staphfiana Young leaves 0.71 2 12 0.54*** Balthasarea schliebenii Fruit 0.67 1 6 0.02 Prunus africana Fruit 0.60 1 6 0.02 Zanthoxylum gilletti Young leaves 0.54 2 12 0.13 Chrysophyllum rwandensis Fruit 0.50 1 2 0.01 Tabernaemontana staphfiana Mature leaves 0.47 4 12 0.01 Schefflera myriantha Leaves 0.45 1 7 0.03 Zanthoxylum gilletti Mature leaves 0.39 6 12 0.15 Bridelia brideliifolia Flower bud 0.33 1 4 0.03 Sapium ellipticum Fruits 0.31 1 7 0.13 Alangium chinense Young leaves 0.24 7 11 0.19 Dombeya goetzenii Mature leaves 0.23 5 12 0.05 Eucalyptus sp. Fruit 0.17 3 8 0.10 Salacia erecta Fruit 0.16 6 4 0.01 Ilex mitis Ripe fruit 0.11 2 4 0.11 Cassipourea ruwensorensis Young leaves 0.08 1 12 0.14 Alangium chinense Mature leaves 0.06 6 12 0.36* Ficus oreodryadum Leaves 0.01 4 12 0.17 * P<0.05, ** P<0.01, *** P<0.001
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CHAPTER FIVE:
GENERAL DISCUSSION AND CONCLUSIONS
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Chapter Five: General Discussion and Conclusions
Summary of thesis aims and findings from each chapter
Primates exhibit high diversity in their social systems, ranging from solitary individuals to large groups of varying size, composition, cohesion, interaction pattern, dispersal pattern, and mating systems (Kappeler 2019; Kappeler and van Schaik 2002). These components can vary across species, within species and populations (Crook and Gartlan 1966; Kappeler and van Schaik
2002). The size and structure of these groups are constrained by ecological and social selective factors such as competition for food and mates, infanticide, and disease, but group living can provide benefits such as enhanced predator defence, alloparental care, and resource defence
(Alexander 1974; Dunbar 1988a; Janson and Goldsmith 1995; Rubenstein and Wrangham
1986; van Schaik 1983). Some primate species form “supergroups” which are socially organised into multilevel societies with central one-male units (OMUs) composed of a core male and multiple female/s (Grueter et al. 2012a; Snyder-Mackler et al. 2012b). Amongst primates, multilevel supergroups have been observed in only a few taxa. In the high-altitude, mountainous forest of Nyungwe National Park, Rwanda, Rwenzori colobus form large supergroups (Fimbel et al. 2001). Previous studies have investigated the diet (Fimbel et al.
2001; Vedder and Fashing 2002) and activity and ranging patterns of the Rwenzori colobus
(Fashing et al. 2007a). The shared similarities with Chinese snub-nosed monkeys in terms of large group size, montane habitat and seasonal consumption of lichen (Grueter et al. 2009b), led to predictions that the Rwenzori colobus form multilevel societies similar to those of
Rhinopithecus sp. (Fashing et al. 2007a). This lead to the following aims of this thesis: 1) identify the internal social organisation of the Rwenzori colobus supergroup (multilevel vs multimale-multifemale), 2) determine the extent to which members of this group experience
106 direct and indirect feeding competition, and 3) investigate the ecological basis of Rwenzori colobus supergroup formation at this site.
In this chapter, I summarise the main findings of this research and discuss the wider implications of the results, integrate this with recent findings and discrepancies in the realm of research on multilevel societies and discuss future directions.
Chapter Two: Social structure
In Chapter Two I investigated the social structure of a supergroup based on a previously generated hypotheses (Grueter and Zinner 2004) that this supergroup may display multilevel social organisation. I extracted the social network structure from the timestamped, spatio- temporal distribution of passing individuals in travel progressions identified to age-sex class and described the ‘anatomy’ of a supergroup numbering 500+ individuals. I detailed the existence of core units – multi-male units (MMUs) with a mean of 1.73 adult males and 3.11 adult females, as well as one-male units (OMUs), all-female units and bachelor units composed of adult and sub-adult males. More than two-thirds of units were MMUs, containing multiple males. Separately, I obtained proximity scans during feeding/resting, which revealed that adult males were in proximity to adult and sub-adult males more often than expected by chance.
Close-proximity resting clusters included a mean of two adult-males. The culmination of the results from the 1) longitudinal network analysis, 2) proximity analysis and 3) close-proximity resting patterns of multiple males within mixed-sex groups, indicate that the Rwenzori colobus supergroup exhibits a multilevel structure, with mainly MMU core units, and some OMUs.
This pattern is different from that observed in other non-human primates forming multilevel societies with predominantly OMUs, such as snub-nosed monkeys, geladas and hamadryas baboons (Grueter et al. 2017b).
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Variable levels of male-male tolerance do exist across the spectrum of primate multilevel societies (Goffe et al. 2016; Grueter et al. 2012a). For example, leader hamadryas males often tolerate follower males which may assist with unit defence and/or infant protection
(Chowdhury et al. 2015), geladas dominant males share reproductive benefits with subordinate males co-existing within their unit (Snyder-Mackler et al. 2012a), and Guinea baboon males occasionally engage in male-male grooming (Fischer et al. 2017; Goffe et al. 2016). The occurrence of multi-male groups may arise due to the benefits provided by male-male cooperation, or the inability of dominant males to exclude rival males and monopolise a large number of females (Ostner and Schülke 2014; Port et al. 2018). The presence of supernumerary males can reduce the risk of takeovers (Port et al. 2010; Snyder-Mackler et al. 2012a), improve access to resources (Pope 2000), or provide more efficient predator deterrence (van Schaik and
Hörstermann 1994). I propose that the formation of the multilevel society of Rwenzori colobus may have resulted from the fusion of overlapping multi-male units, when resources permit, or due to the associated socioecological benefits. Despite male-male tolerance existing in multiple primate multilevel societies, the Rwenzori colobus multilevel society differs from most others described so far in having primarily multi-male, multi-female units instead of one-male, multi- female units at its core, a unique form of social organisation observed in this population in
Rwanda, and the population of Rwenzori colobus in Uganda (Stead and Teichroeb 2019).
Chapter Three: Supergroup formation in the absence of feeding competition
Competition for food is often exacerbated by living in a group, and varying socioecological pressures can dictate whether a group is affected by indirect or direct feeding competition.
Rwenzori colobus in Nyungwe National Park form supergroups of over 500 individuals and present an opportunity to investigate feeding competition in such a large primate group. In
Chapter Three I examined whether freedom from scramble competition allows Rwenzori colobus to form supergroups. The colobus exhibited within-band scramble competition over
108 young leaves, but not over mature leaves or fruit. Larger groups occupied food patches for longer than smaller groups, suggesting between-group contest for food patches. Tombak et al.
(2012) suggested that the different digestive physiologies of red colobus and guerezas may contribute to the observed differences in feeding competition (Tombak et al. 2012). However,
Rwenzori colobus and guerezas are similar in digestive physiology and size, and, unlike guerezas, I found that they do experience scramble competition. This suggests group size and/or localised food availability more than digestive physiology determines the presence of scramble competition in black-and-white colobus. The factors allowing the formation of supergroups, despite evident feeding competition, therefore may be a lack of competition for high-quality mature leaves.
Chapter Four: Ecological basis for supergroup formation
In Chapter Four I investigated changes in the Rwenzori colobus supergroup during periods of resource scarcity by examining whether the supergroup utilises a fallback food when preferred foods are scarce. Fruticose lichens (Usnea sp.) contributed >50% of the monthly diet when preferred foods were less available, suggesting that they constitute a fallback food for Rwenzori colobus supergroups. However, in a number of other montane forests in East Africa with similar tree species as well as fruticose lichen, the colobus form small groups, which suggests that lichen and high-quality leaves may create a resource base necessary to support colobus supergroups, but factors such as forest size, fragmentation, degradation and hunting may impact group sizes.
Supergroups: Habitat or taxon specific?
The pronounced variation in social organisation observed amongst the subspecies of Colobus angolensis may be due to the extreme differences in habitat. Angolan colobus inhabit dry coastal rag forest (Dunham 2017), degraded forest (Marshall 2007), forest fragments
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(McDonald and Hamilton 2010), lowland rainforest (Arseneau-Robar et al. 2018) and montane rainforest (Vedder and Fashing 2002). However, even coastal colobus (Colobus angolensis palliatus) may have once formed multilevel societies (Moreno-Black 1974; Moreno-Black and
Maples 1977). Historically, multi-male units temporarily coalesced into larger groupings
(Moreno-Black 1974; Moreno-Black and Maples 1977); however, today they only exist in small one-male units existing in a human-impacted matrix of forest and non-forest habitat
(Dunham 2017). Anthropogenic impacts on primates are diverse and widespread (Estrada et al. 2017; McKinney 2015), and large bands or supergroups have been more geographically widespread or present among more primate species/subspecies in the absence of certain anthropogenic pressures (Zhao et al. 2018). For example, human expansion in China has resulted in the extirpation of many low-elevation snub-nosed monkey populations (Wen and
Wen 2006; Zhao et al. 2018), leaving remaining populations marooned in forested mountainous regions.
In Chapter Two, I provide evidence that Rwenzori colobus form a multilevel society in the high-altitude forest of Nyungwe. However, Rwenzori colobus also form a multilevel society at
Manwa Forest, Lake Nabugabo, Uganda, a low-altitude forest, with different forest composition (Stead and Teichroeb 2019). The forests of Nyungwe and Manwa (Lake
Nabugabo) differ fundamentally in size and elevation which has repercussions for the diet of the colobus. Nyungwe is a large forest tract (1013 km2), Manwa is a pocket of forest 2.8 km2 in size. Nyungwe is high-altitude and Manwa is a lowland forest (Arseneau-Robar et al. 2018;
Plumptre et al. 2002). Rwenzori colobus at Nyungwe rely on lichen as a fallback food (Chapter
Four), whereas at Manwa Forest, young leaves and fruit make up most of the diet (Stead and
Teichroeb 2019). However, as discussed in Chapter Four, both experience low levels of human hunting pressure on primates (Chapman et al. 2016; Stead and Teichroeb 2019), and in both forests colobus form supergroups.
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If supergroup formation and multilevel social organisation was phylogenetically inert in the subspecies Rwenzori colobus one would expect to see supergroups in the contiguous Kibira
National Park in Burundi; rather, they form relatively small groups averaging 25 individuals
(Hakizimana, pers. comm.), despite the colobus occupying the same big forest which has been divided into two National Parks. In Africa specifically, hunting by humans for bushmeat represents a bigger threat to primates than habitat degradation (Brugiere 1998; Chapman et al.
2000; Johns and Skorupa 1987; Linder and Oates 2011; Milner-Gulland and Bennett 2003;
Oates 1996). Hunting of primates in Nyungwe and Kibira have different histories. The occupation of Kibira by armed groups means it has experienced extensive hunting of large mammals (Hakizimana et al. 2015; Hakizimana and Huynen 2013; OBPE 2014). In contrast, poaching is snare-based in Nyungwe (Moore et al. 2018), which has lower success in arboreal primates compared to gun hunting (Kümpel et al. 2009; Remis and Kpanou 2011).
In this study, the results of Chapter Three & Four demonstrate that fallback foods such as fruticose lichen, or a resource base such as mature leaves that do not elicit feeding competition, are factors that support supergroup formation. I suggest that the prevalence of bushmeat hunting may be responsible for the absence of supergroups in other forests, as Rwenzori colobus are not known to form supergroups at other sites impacted by human hunting of colobus. Nyungwe is the largest remaining montane forest in Africa, is not impacted by bushmeat hunting for primates (Moore et al. 2018), and represents a key site for primate conservation in East Africa (De Jong and Butynski 2012). Therefore the primate population in
Nyungwe is one of the very few that are not exposed to firearm hunting (Moore et al. 2018;
Oates 1996). As pointed out by Grueter et al. (2012b), the pristine conditions required for multilevel systems to unfold are becoming rare, as we see more habitat fragmentation and forest loss. The displayed tolerance of Angolan colobus to disturbed habitats (Dunham 2017) is
111 encouraging, but the persistence of Angolan supergroups in Africa may be uncertain due to reductions in forest size, forest fragmentation and hunting of primates by humans.
Future directions: Multilevel societies
In this section, I discuss topics pertaining to multilevel societies which require clarification or warrant further research: 1) what constitutes a multilevel society, 2) fission-fusion dynamics, and 3) superficial complexity. I provide evidence to support each point and discuss future research directions.
Defining multilevel societies
Multilevel, modular, hierarchically nested, nested, social modules, community clustering – all terms relating to the same thing – structural properties within a system at multiple organisational levels, nested within one-another (Fisher and Pruitt 2019). I believe this varied use of terminologies across disciplines has contributed to assumptions that multilevel societies are rare. Rarity may also be due to previously strict definitions of what constitutes a multilevel society. This point has also been discussed by De Silva and Wittemyer (2012), who posit that biological scientists need a more relaxed definition of multilevel societies, incorporating those societies that display more fluid modularity and are less clearly delineated.
Recent advances in the application and accessibility of social network analysis has led to a plethora of investigations into different species’ social organisation (Krause et al. 2014), inevitably describing more multilevel societies in the animal world (Tavares et al. 2017;
VanderWaal et al. 2014; Wolf et al. 2007). For example, the fission-fusion structure of giraffe societies appears fluid and random, but when examined using network analysis and community finding methods VanderWaal et al. (2014) find a multi-tiered social structure.
‘Traditional’ multilevel networks such as the societies of hamadryas baboons, geladas and snub-nosed monkeys display ‘disjoint’ modules (Fortunato 2010), where each individual (or
112 node) within the network has a low membership number [which is the number of communities the node belongs to], with nodes typically belonging to one community (module or unit) (Palla et al. 2005). This form of social network can be distinguished from one that contains communities that overlap, or contains overlapping individuals (or nodes or vertices), a more common scenario in real-world networks (Goldberg et al. 2010; Lancichinetti et al. 2011; Sun et al. 2011). Thus a ‘traditional’ multilevel society is 1) hierarchically partitioned, and 2) forms disjoint [or distinct] groups that display collective movement/behaviour (Goldberg et al. 2010).
The social organisation of Rwenzori colobus described in Chapter Two fits the description of a traditional multilevel society, as units travelled in spatiotemporal isolation from other units.
In addition, observations of resting clusters in separate trees suggest that units maintain spatial separation when resting. Our observations of spatially distinct units are also corroborated by
Stead and Teichroeb (2019) who observed “socially and spatially distinct core units” at the lowland site of Lake Nabugabo in Uganda.
Multilevel and fission-fusion
The tendency to pair the terms ‘multilevel’ with ‘cohesive’, and ‘fission-fusion’ with ‘fluid’, has possibly led to some confusions; for example, the fluid variable group composition [daily and seasonal] of Guinea baboons (Papio papio) implied a social system differing from savanna and hamadryas baboons (Patzelt et al. 2011), but later this species was confirmed to form a multilevel society (Patzelt et al. 2014). All primate multilevel societies display fission-fusion dynamics (Aureli et al. 2008; Kirkpatrick et al. 1999; Majolo et al. 2018; Nie et al. 2009; Qi et al. 2014; Schreier and Swedell 2012; Snyder-Mackler et al. 2012b). The frequency of such events varies in scale, and is more frequent in some taxa, or species, than others (Kirkpatrick and Grueter 2010). In this study, Rwenzori colobus displayed frequent fission-fusion dynamics that varied from less than an hour to several months. The group was often spread over a large area and divided into subgroups that were separated by many kilometres; these subgroups
113 would travel and feed simultaneously and take different travel paths to arrive at a similar location where they would coalesce after several days. How cohesive a multilevel society is may not be a unique feature of a species’ social system, but rather a reflection of the environment. In this study, within-band cohesion may be influenced by increased food availability reducing fissioning (Anderson and McGrew 1984; Galat-Luong and Galat 2003;
Galat-Luong et al. 2006), or the presence of a fallback food, such as lichen available to supergroups, similar to the instance of snub-nosed monkeys in China (Grueter et al. 2009b).
Investigating how the cohesion of the Rwenzori colobus supergroup varies with food availability and the frequency of short-and-long-term fission-fusion dynamics would be interesting avenues for future research.
Are multilevel societies socially complex environments?
Multilevel societies may be viewed as being socially complex, possibly due to the well-known correlation between group size and neocortex size [a proxy for cognitive capacity] (Dunbar
1995). However, this gives little insight into how the individuals are interacting within these groups (Shultz and Dunbar 2007). Multilevel societies are likely superficially complex environments, where numbers of individuals or layers do not necessarily equate to complexity from an individual’s perspective. Aureli and Schino (2019) note that, a scientist viewing a primate group, a human crowd, an ungulate herd, or school of fish may observe emergent complexity, but is that also what the individual monkey, person, zebra, or fish experiences?
For example, in ant colonies, Anderson and McShea (2001) note that the complexity of lower- level individuals is reduced as social complexity increases. Barrett et al. (2007) proposed that it may be the human observer that imposes a narrative structure of complexity but may allude to more complexity than is present when discussing non-human primate social interactions.
Thus, multilevel societies may be outwardly complex to the observer, but relatively simple to the individual within the network. With increasingly large and dispersed communities (as seen
114 in primates, such as geladas, hamadryas baboons and Rwenzori colobus) (Snyder-Mackler et al. 2012b), keeping track of all individuals becomes increasingly difficult (Cohen et al. 2012;
Dunbar 2014; Layton and O’Hara 2010). Thus, relying on long-distance visual and/or auditory signals (as opposed to social knowledge) may be essential in large groups as a strategy to assess the quality or dominance of unknown individuals (Bergman and Sheehan 2013; Grueter et al.
2015). As highlighted by Maciej et al. (2013) “complex social organisation does not necessarily translate into the need for more elaborate social knowledge” (p. 66), and with multilevel societies that may be the exact advantage. The apparent anonymity observed in some non- human primate multilevel societies appears to be consistent with the ‘tag-based cooperation’
(Cohen et al. 2012, p 588), or ‘social categorisation’ (Kramer et al. 2017, p 115), which is useful in situations where individuals are unable to observe or remember the actions of others
(Boyd and Richerson 1987; Cohen et al. 2012; Kramer et al. 2017; Moffett 2013; Riolo et al.
2001; Spector and Klein 2006).
Moffett (2013) points out that it is a mystery why so few vertebrates have adopted the insect route of “using the low-cost cognitive trick of employing group-identity labels to create larger social groups, an option potentially available to many species by social learning”. Perhaps they do, as highlighted by the following research on geladas. Bergman (2010) highlighted the first evidence of ‘missing’ social knowledge in a wild primate, demonstrating that OMU males could not identify any other males in their band. Moreover, Benítez et al. (2017) provided the first evidence for a mutual assessment strategy in a non-human primate; geladas use signals to interact with unknown individuals rather than a self- or opponent-based approach using social knowledge. Dimorphism is associated with social organisation, and Grueter et al. (2015) found that males from species with multilevel social organisations have the highest ratings for ornamentation, specifically males have more developed visually conspicuous secondary sexual traits. For example, Koda et al. (2018) found that noses of proboscis monkey bachelor males
115 were considerably smaller than those of harem males, suggesting the male nose size may function as a badge of status for the core males in harem groups. As highlighted by Dunbar
(1993) in the context of humans, adding to the size of one’s social group is cognitively costly; however labels can be applied to an indefinite number of individuals, thus reducing the cognitive load of social surveillance (Clark and Chalmers 1998; Wilson 2005).
Although social knowledge was not investigated in the current study it represents a future avenue of research on Rwenzori colobus. Future research could investigate within-unit dynamics and the extent to which social affiliation is extended outside of the multi-male or one-male unit, explicitly investigating the boundaries of social knowledge within the band.
Rwenzori colobus are slightly ornamented, with a tufted tail and somewhat longer white-and- black coat hair in males, and dimorphism in body mass between the sexes is quite pronounced, with adult males heavier than adult females (Smith and Jungers 1997). Fully grown, unit- holding adult males generally appear to have longer wavy black hair on their back, longer white mantle hair, and more prominent white cheek tufts (pers. obs. A. Miller). Investigating if
Rwenzori colobus differentiate between mixed-sex unit males and bachelor males based on appearance characteristics, and if any of the described physical attributes function as a badge of status for the unit-holding males, would be an interesting avenue for future research.
Conclusions
Primates display a wide variety of social systems, and few primate species form “supergroups” which are shaped by a range of social and ecological selective pressures. Rwenzori colobus form a supergroup numbering 500+ individuals in Nyungwe National Park in Rwanda and are socially organised into a multilevel society with core multi-male units as well as one-male units. This pattern of organisation differs from the mainly one-male unit structure observed in other non-human primates forming multilevel societies such as snub-nosed monkeys, geladas
116 and hamadryas baboons. While investigating the ecological preconditions underlying supergrouping, I showed that the Rwenzori colobus individuals experience within-band scramble competition over young leaves, but not over mature leaves or fruit. In addition, occupancy of food patches by larger groups suggests potential between-group contest for food patches. Comparing preferred food availability with consumption of potential fallback foods, I found fruticose lichen to constitute a fallback food for the supergroup. However, in a number of other montane forests in Burundi and Tanzania with similar tree species as well as fruticose lichen, Angolan colobus form small groups suggesting that lichen and high-quality leaves may create a resource base necessary to support colobus supergroups, but factors such as forest size, fragmentation, degradation and hunting by humans may impact group sizes.
Summary
The main contributions of this thesis are as follows:
1. Rwenzori colobus in Nyungwe National Park form a supergroup of over 500
individuals that is sub-structured into a multilevel society.
2. The multilevel society is composed of core units – multi-male units with a mean of 1.73
adult males and 3.11 adult females, as well as one-male units, all-female units and
bachelor units composed of adult and sub-adult males.
3. Multi-male units were the most common unit type, with more than two-thirds of units
containing multiple males, a different pattern than the one-male unit core observed in
other primate multilevel societies.
4. The Rwenzori colobus supergroup exhibited within-band scramble competition over
young leaves, but not over mature leaves or fruit.
5. Larger groups were able to occupy food patches for longer than smaller groups, which
hints at the existence of between-group contest for food patches.
117
6. Fruticose lichen (Usnea sp.) contributed >50% of the monthly diet when preferred
foods were less available. Lichen, specifically fruticose lichen, appears to be a fallback
food for Rwenzori colobus supergroups.
7. The presence of other potentially suitable montane sites for supergroup formation in
Eastern Africa where Angolan colobus form smaller groups suggests that lichen and
high-quality mature leaves may provide appropriate conditions for supergroup to form.
However, these factors alone are likely not sufficient; supergroup formation is likely
permitted by sufficient forest size, and an absence of fragmentation and hunting
pressure by humans.
118
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