Fission-Fusion Dynamics in Spider Monkeys in Belize

University of Calgary PRISM: University of Calgary's Digital Repository

Graduate Studies The Vault: Electronic Theses and Dissertations

2016 Fission-Fusion Dynamics in Spider Monkeys in Belize

Hartwell, Kayla Song

Hartwell, K. S. (2016). Fission-Fusion Dynamics in Spider Monkeys in Belize (Unpublished doctoral thesis). University of Calgary, Calgary, AB. doi:10.11575/PRISM/26183 http://hdl.handle.net/11023/3497 doctoral thesis

University of Calgary graduate students retain copyright ownership and moral rights for their thesis. You may use this material in any way that is permitted by the Copyright Act or through licensing that has been assigned to the document. For uses that are not allowable under copyright legislation or licensing, you are required to seek permission. Downloaded from PRISM: https://prism.ucalgary.ca UNIVERSITY OF CALGARY

Fission-Fusion Dynamics in Spider Monkeys in Belize

Kayla Song Hartwell

A THESIS

SUBMITTED TO THE FACULTY OF GRADUATE STUDIES

IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE

DEGREE OF DOCTOR OF PHILOSOPHY

GRADUATE PROGRAM IN ANTHROPOLOGY

CALGARY, ALBERTA

DECEMBER, 2016

Abstract

Most diurnal primates live in cohesive social groups in which all or most members range in close proximity, but spider monkeys (Ateles) and chimpanzees (Pan) are known for their more fluid association patterns. These species have been traditionally described as living in fission-fusion societies, because they range in subgroups of frequently changing size and composition, in contrast with the more typical cohesive societies. In recent years the concept of fission-fusion dynamics has replaced the dichotomous fluid versus cohesive categorization, as it is now recognized that there is considerable variation in cohesiveness both within and between species. This thesis is a study of the fission-fusion dynamics in spider monkeys to quantify and explain temporal variation in subgroup size, spatial cohesion, and stability. I collected behavioural, ecological, and genetic data from a group of spider monkeys at Runaway Creek Nature Reserve in Belize from January 2008 until

September 2013. I found that most subgroups were small (1-3 individuals), contained only adult females, and changed membership every 30-40 minutes. Habitat-wide fruit availability showed a weak relationship with subgroup size, contrary to what I expected, but it did explain some of the variation in subgroup stability. Likewise, degree of relatedness between individuals was not correlated with an association index that measured the likelihood that any two individuals would be in the same subgroup together. This thesis also describes the feeding ecology of the study group, and explores their genetic structure.

The latter revealed some unexpected patterns: although traditionally believed to be a male philopatric, female dispersal species, male spider monkeys at Runaway Creek were no more closely related to one another than were females, and both males and females were ii

residents and immigrants. As expected, given the common characterization of spider monkey males as experiencing low levels of within-group competition for females, paternity analysis revealed no reproductive skew, with all males siring offspring. Further analysis is needed to identify and understand the variables that are affecting the temporal changes in subgroup size, spatial cohesion, and stability of this group. However, this study makes an important contribution to this much larger question.

iii

Acknowledgements

I am sincerely grateful to my supervisors, Dr. Mary Pavelka and Dr. Hugh Notman, whose constant support, encouragement, and guidance helped me to accomplish my graduate work and research. I would also like to thank the other members of my advisory committee,

Dr. Linda Fedigan and Dr. Pascale Sicotte for valuable feedback and support over the years, as well as to Dr. Kathreen Ruckstuhl who has served on my defenses for Masters, candidacy exam, and PhD. And many many thanks to my external examiner, Dr. Colin

Chapman. Dr. Peter Dawson, Graduate Program Director, served as the neutral chair for the oral defense, and his calm and supportive presence was much appreciated.

I would also like to thank everyone (graduate students, faculty, and staff) in the

Anthropology Department at the U of C, and Tracy Wyman for help with ranging data and mapping. To Jane Champion (this is for the fallen soldiers, never forget), Colin Dubrool (I purposely spelled your name wrong), Meredith Brown (sleeps like Teenager), Kayley

Evans, and Brittany Dean: thank you for your friendship, dedication to the field, and for your contribution toward data which helped make this research possible. And thanks to my dear friend and mentor, Dr. Sarah Hewitt, for always being there for me during the best and worst of times.

I am very grateful to Sharon Matola, Founder and Director of the Belize Zoo and

Tropical Education Center for her support in helping Mary Pavelka to launch the spider monkey study at Runaway Creek Nature Reserve, along with Dr. Gil and Lillian Boese. I also thank Lillian and Gil for permission to work in the Reserve and for their ongoing iv

support of the project. Local NGO Birds without Borders (Reynold Cal, Wilber Martinez,

David Tzul, and Stevan Reneau) was also critical to the success of this study for their assistance with field work and for the countless times they came to the rescue when I bogged the truck in knee-deep mud or broke down along the Coastal Road. I am especially grateful to Stevan Reneau and David Tzul for sharing their knowledge of the bush and for helping me chase monkeys up and over karst hills for months on end during the long habituation process. I also want to thank Gilroy (Nico) Welsh for his assistance with chopping trails, collecting data, and for always keeping everyone in good spirits with his cool vibes. Many thanks to David Tzul and Dr. Steven Brewer for vegetation sampling and plant identification, and Gerson Garcia and Richard Usher for their assistance in the field.

I would also like to thank Sharon Matola and everyone at the Tropical Education Center for providing accommodation over the years, and to Sue Hufford at Amigos for keeping me well fed and hydrated.

I am grateful to Dr. Anthony Di Fiore for inviting me to work in his genetics lab at the University of Texas at Austin, and to Amely Martins for her training and guidance. A big thank you to Marie Tosa for contributing additional genotype data on the spider monkeys at Runaway Creek.

I would like to thank the following agencies for the funding that made this research possible: Natural Sciences and Engineering Research Council of Canada; National

Geographic; Athabasca University Academic Research Fund; Andover (New Hampshire)

Service Club Scholarship; the Shelley R. Saunders Thesis Research Grant (Canadian

Association for Physical Anthropology); and the University of Calgary (URGC

Dissertation Research Grant, Graduate Faculty Council Scholarship, Chancellor’s

Challenge Graduate Scholarship, J.B. Hyne Graduate Scholarship, the Department of

Anthropology and Archaeology, the Faculty of Graduate Studies, and the Faculty of Arts).

A very special thank you to my family in New Hampshire for all their support, love, and encouragement. I couldn’t have done this without you.

Dedication

This thesis is dedicated to those with learning disabilities in academia who have to work

so much harder to be where they are.

vii

Table of Contents

Abstract ...... ii Acknowledgements ...... iv Dedication ...... vii List of Tables ...... ix List of Figures ...... x

CHAPTER 1. GENERAL INTRODUCTION ...... 1 Introduction ...... 1 Background in Spider Monkey Behaviour and Social Organization ...... 8 Thesis Objectives ...... 11

CHAPTER 2. QUANTIFYING FISSION-FUSION DYNAMICS IN SPIDER MONKEYS IN BELIZE: TEMPORAL VARIATION IN SUBGROUP SIZE, SPATIAL COHESION, AND STABILITY...... 17 Introduction ...... 17 Methods ...... 20 Results ...... 24 Discussion ...... 36

CHAPTER 3. THE EFFECTS OF FEEDING ECOLOGY ON FISSION-FUSION DYNAMICS IN SPIDER MONKEYS ...... 41 Introduction ...... 41 Methods ...... 44 Results ...... 51 Discussion ...... 57

CHAPTER 4. PATTERNS OF GENETIC RELATEDNESS IN A POPULATION OF SPIDER MONKEYS IN BELIZE ...... 64 Introduction ...... 64 Methods ...... 71 Results ...... 79 Discussion ...... 85

CHAPTER 5. GENERAL DISCUSSION ...... 94

REFERENCES ...... 104

APPENDIX A: LIST OF PLANT SPECIES CONSUMED BY THE SPIDER MONKEYS AT RUNAWAY CREEK ...... 136

APPENDIX B: DYADIC ESTIMATES OF RELATEDNESS AND ASSOCIATION INDEX VALUES ...... 141

viii

List of Tables

Table 1. Study group size and composition over the study years 2008-2013. Subadults are included with adults...... 21

Table 2. Temporal variation in mean subgroup size: month, season, year, and overall ... 26

Table 3. Temporal variation in subgroup spatial cohesion (subgroup spread/subgroup size): Amount of space available in meters per subgroup member...... 31

Table 4. Temporal variation in mean subgroup stability (duration of time= h:mm) across months, seasons, years, and overall...... 35

Table 5. Summary of descriptive trends ...... 37

Table 6. List of phenology tree species and their percentage in the spider monkey diet at Runaway Creek...... 49

Table 7. Panel of microsatellite markers used for genotyping the Runaway Creek spider monkeys ...... 75

Table 8. Corrected population assignment indices (AIc) of the 7 adult males and 15 adult females in the spider monkey study group at Runaway Creek...... 81

Table 9. Assigned paternities and associated significance measures for 19 immatures in the study group over the years 2008-2013 ...... 83

Table 10. Number of offspring sired per adult male and the number of study years as a breeding male ...... 84

List of Figures

Figure 1. Satellite image of Runaway Creek Nature Reserve and its general location within Belize ...... 13

Figure 2. An adult female spider monkey with her infant foraging on the leaves of Brosimum alicastrum (Moraceae) ...... 14

Figure 3. Overall distribution of the size of spider monkey subgroups at Runaway Creek ...... 25

Figure 4. Yearly variation in mean monthly subgroup size of spider monkeys at Runaway Creek from 2008 to 2013...... 25

Figure 5. Percentage of subgroups of different sizes for all-female, all-male, and mixed-sex subgroups...... 27

Figure 6. Yearly variation in mean subgroup size for all-female, all-male, and mixed- sex subgroups of spider monkeys at Runaway Creek (2008-2013)...... 28

Figure 7. Percentage of subgroups of different spatial cohesion (subgroup spread/subgroup size)...... 30

Figure 8. Percentage of all-female, all-male, and mixed-sex subgroups of different spatial cohesion (subgroup spread/subgroup size) ...... 32

Figure 9. Yearly variation in mean spatial cohesion (subgroup spread/subgroup size) in all-female, all-male, and mixed-sex subgroups...... 34

Figure 10. Mean monthly subgroup stability (duration of time before a change in subgroup membership) for all-female, all-male, and mixed-sex subgroups in 2009-2013 ...... 36

Figure 11. Monthly rainfall in the Belize’s capital city of Belmopan (Cayo District), which is located approximately 35km west of Runaway Creek Nature Reserve ..... 44

Figure 12. Yearly variation in dietary composition of spider monkeys at Runaway Creek from 2008-2013 ...... 51

Figure 13. Mean monthly fruit availability scores across 2009-2013. Grey shaded area denotes months of the wet season ...... 52

Figure 14. Diet composition of spider monkeys at Runaway Creek during the wet and dry seasons of 2008-2013 ...... 53

Figure 15. Scatter plot showing the positive relationship between fruit availability and the proportion of fruit in the spider monkey diet...... 54

Figure 16. Temporal variation in monthly fruit availability scores and the proportion of ripe fruit in the spider monkeys’ diet from 2009-2013...... 55

Figure 17. Scatter plot showing subgroup stability decreases as fruit availability increases...... 56

Figure 18. Distribution of relatedness values among male-male and female-female dyads of spider monkeys at Runaway Creek...... 80

Figure 19. Frequency distributions of corrected assignment index (AIc) values of adult males and adult females at Runaway Creek...... 82

CHAPTER 1. GENERAL INTRODUCTION

Introduction

Hans Kummer (1971) introduced the term ‘fusion-fission’ to describe primate societies that changed the size of their groups by fusion (merge) and fission (split) according to the activity of group members and the distribution of food resources. Fusion- fission societies (later termed ‘fission-fusion’) were considered uncommon in primates except for chimpanzees (Pan troglodytes), hamadryas baboons (Papio hamadryas hamadryas), and geladas (Theropithecus gelada). The fluid grouping patterns of fission- fusion societies were contrasted with socially cohesive groups, which were considered the norm of most primate species. Since then, several other mammalian species have been identified as having fission-fusion social organization, such as spider monkeys (Ateles spp.:

Fedigan & Baxter 1984), bonobos (Pan paniscus: Kuroda 1979), bottlenose dolphins

(Tursiops spp.: Connor et al. 2000), elephants (Loxodonta africana: Wittemyer et al. 2005), and spotted hyenas (Crocuta crocuta: Holekamp et al. 1997).

Flexible spatiotemporal grouping patterns are not limited to species with classic fission-fusion social organization. For example, frequent changes in group size and composition are common in many temperate bat species, and males typically roost separate from female maternity groups, either alone or in small all-male groups (reviewed in

Altringham & Senior 2005; Patriquin & Ratcliffe 2016). Colonies of Bechstein’s bats

(Myotis bechsteinii) and big brown bats (Eptesicus fuscus) move between multiple tree roosts, and the size and composition of groups change daily (Kerth & König 1999; Willis 1

& Brigham 2004). Some individuals associate randomly, while others preferentially roost with certain individuals (Kerth & König 1999).

Grevy’s zebra (Equus grevyi) and the Asiatic onager (Equus hemionus) are two closely related species that differ in the size, cohesiveness, and stability of social groups

(Sundaresan et al. 2007; Rubenstein et al. 2015). Grevy’s zebras aggregate in subgroups that are larger and more stable in membership, whereas onagers move more frequently between smaller subgroups. Lactating female Grevy’s zebras are also more socially fluid than males and non-lactating females, and switch between larger ‘communities’ more often

(Rubenstein et al. 2015).

Bottlenose dolphins form temporary parties of unstable size and composition, but they most often consist of same-sex partners (Connor et al. 2000). Although mixed sex parties are encountered, most long term associations are between members of the same sex, and adult male subgroups are the most consistent over time (Smolker et al. 1992). These all-male subgroups consist of individuals who associate preferentially with each other, and usually consist of two to three males. Female-female associations tend to be less strong than male associations and are described as a loose network rather than preferred associations (Smolker et al. 1992). Male-female associations are not consistent and are strongly influenced by the reproductive state of the female (Connor et al. 2000).

African elephants live in complex, multi-tiered, fission-fusion societies (Wittemyer et al. 2005; Archie et al. 2006). Within closed communities, matriarchal family units

(which consist of two to three closely related females and their young) frequently join and 2

separate from other family units and will sometimes form large aggregations of multiple families. Wittemyer et al. (2005) suggest that females form these large aggregations when food availability is high to benefit from increased predator protection and territoriality, knowledge sharing, and alloparental care. Male elephants live separate from female family units and are usually solitary or in small all-male groups (Stokke & du Toit 2002).

Among primates, there is considerable inter- and intra-species variation in the size and cohesiveness of social groups (reviewed in: Strier 1994; Kinzey & Cunningham 1994;

Bearder 1999), as well as in how groups respond to temporal changes in the social and ecological environments (Strier 2009). For example, in a growing population of muriqui monkeys (Brachyteles arachnoids hypoxanthus) studied over 25-years, social groups shifted from cohesive to more fluid (Dias & Strier 2003), while muriqui populations studied in less disturbed habitats exhibit subgrouping behaviour characteristic of classic fission-fusion societies (Coles et al. 2012).

Several studies have noted fission-fusion subgrouping behaviour in Cercocebus mangabeys. For example, Jones & Sabater Pi (1968) observed a group of C. torquatus in

Equatorial Guinea fission into small groups and then later merge back together, and similar subgroup formation has been observed in other populations (Mitani 1989; Range 2006).

More recently, Dolado et al. (2016) reported seasonal fission-fusion dynamics in a group of C. torquatus in Gabon. During peak fruiting months, the study group of 90 individuals split into three ‘parties’ (Dolado et al. 2016).

Female mouse lemurs (Microcebus spp.) forage alone and sleep in communal sleeping sites with fixed composition (Radespiel et al. 2001). Males are solitary and range over an area containing the smaller ranges of multiple females (Eberle & Kappeler

2002), and in some species of mouse lemurs, males will join females temporarily at sleeping sites (Radespiel et al. 2001). Black-and-white ruffed lemurs (Varecia variegata) also exhibit variation in group size, composition, and spatial cohesion over time. A recent study by Holmes et al. (2016) revealed that fission-fusion dynamics in black-and-white ruffed lemurs are closely tied to spatiotemporal variation of food availability, as well as for the communal care of infants. The lemurs formed larger subgroups during the wet season when fruit availability was low, as well as when infants were present in the group

(Holmes et al. 2016).

The variation in primate and other animal grouping patterns has led to greater interest in documenting the range of flexibility that exists within and between species and populations (Strier 1994; Kinzey & Cunningham 1994; Bearder 1999; Lynch-Alfaro

2007; Aureli et al. 2008). Strier (1989) argued that variation in spatiotemporal cohesion of animal groups may play an important role in helping animals adapt to changes in the social and ecological environments. Instead of classifying primate species as either cohesive or fluid, Strier (1989) argued that social groups vary along a continuum from highly cohesive to highly fluid. This framework was later adapted by Aureli et al. (2008), who proposed the use of the term fission-fusion dynamics to reflect the extent of variation in group size, composition, and spatial cohesion over time. In this perspective, animal social groups vary from high cohesion with stable group membership (i.e. low 4

fission-fusion dynamics) such as black howler monkeys (Alouatta pigra: Pavelka 2011) to low cohesion and high sociospatial fluidity (i.e. high fission-fusion dynamics) such as chimpanzees and spider monkeys (Symington 1990; Chapman et al. 1995). Aureli et al.

(2008) argue the importance of quantifying fission-fusion dynamics, and of conducting both within- and between-species comparisons to better our understanding of the social, ecological, genetic, and demographic factors that might influence the maintenance and variation in social relationships.

Year-round association of males and females in social groups, even in sexually dimorphic and seasonally breeding species, has long been noted to be a distinctive feature of primate sociality (Fedigan 1992; Watts 2005), however in species characterized by high fission-fusion dynamics such as chimpanzees and spider monkeys, males and females have been described as ranging separately at least some of the time. Sexual segregation is recognized as an important part of the socioecology of many vertebrate taxa (reviewed in:

Ruckstuhl & Neuhaus 2005; Ruckstuhl 2007), and was recently examined systematically in primates, using the spider monkey population at Runaway Creek in Belize. Hartwell et al. (2014a) provided the first quantitative test of sexual segregation in a primate species using an analytical technique designed to distinguish active patterns of aggregation and segregation from those that would be predicted by models in which animals associate randomly on the basis of group size and sex ratio. This study found that the regularly changing spider monkey subgroups were segregated by sex most of the time, probably as a result of different sex-specific energetic requirements and reproductive strategies, and

proposed that sexual segregation may represent an important and previously unrecognized constraint on fission-fusion dynamics.

Chimpanzees and spider monkeys are among the least cohesive primate species and all members of a community are rarely seen together as a cohesive group. Both species are large-bodied frugivores that live in large, territorial, multi-male/multi-female communities characterized by male philopatry and female dispersal (Wrangham 1979; Symington 1987,

1990; Di Fiore et al. 2009). Males exhibit stronger social bonds than females, and adult females and their dependent young often travel and forage separately from adult males

(Wrangham & Smuts 1980; Goodall 1986; Fedigan & Baxter 1984; Chapman 1990a;

Shimooka 2003). The degree of sexual segregation varies seasonally in spider monkeys

(Hartwell et al. 2014a), and descriptive accounts show inter-site variation in male-female associations in chimpanzees (Sugiyama & Koman 1979; Stumpf 2007; Lehmann & Boesch

2008). This variation suggests that some ecological factors may be at play when shaping the sociality of these populations.

Food availability explains some of the variation in chimpanzee and spider monkey subgroup size (Chapman et al. 1995; Newton-Fisher 1999). High fission-fusion dynamics in these species are thought to mitigate the costs of group living when high-quality food such as fruit is distributed patchily in time and space (Klein & Klein 1977; Wrangham

1980; Symington 1990; Chapman et al. 1995). By foraging in smaller subgroups, researchers argue that individuals can reduce feeding competition and time spent traveling between food patches. Several studies have found that individuals will forage in larger

subgroups when food availability is high (Chapman 1990a; Chapman et al. 1995; Mitani et al. 2002; Hashimoto et al. 2001, 2003; Shimooka 2003; Itoh & Nishida 2007).

In chimpanzees, several factors are thought to influence subgroup size and composition. These include the presence of estrous females (Wrangham et al. 1992;

Matsumoto-Oda et al. 1998; Mitani et al. 2002), the activity of the subgroup (Wrangham

& Smuts 1980; Newton-Fischer 1999), spatial fluctuations in predation risk (Boesch 1991;

Boesch & Boesch-Achermann 2000), demographic variables like community size and sex- ratio (Goodall 1986; Newton-Fisher 1999; Boesch & Boesch-Achermann 2000; Lehmann

& Boesch 2004), preferred social partners (Pepper et al. 1999; Newton-Fisher 1999;

Wakefield 2008; Gilby & Wrangham 2008), female dominance and range use (Pusey et al.

1997; Thompson et al. 2007; Gilby & Wrangham 2008), and genetic relatedness (Goodall

1986; Morin et al. 1994; Langergraber et al. 2007). For example, the number of males and anestrous females increase in subgroups containing estrous females (Wrangham et al.

1992; Matsumoto-Oda et al. 1998; Mitani et al. 2002) and are even larger when older, more dominant females are in estrous (Muller et al. 2006). Subgroups also tend to be larger when individuals are foraging, resting, or grooming (Newton-Fisher 1999; Wrangham & Smuts

1980), or when the risk of predation from leopards is greater (Boesch 1991; Boesch &

Boesch-Achermann 2000). In a Taï chimpanzee community that decreased in size over a

10-year period, male-female association rates increased and individuals traveled and foraged in larger, more cohesive subgroups than previously when the community was larger (Lehmann & Boesch 2004).

Male chimpanzees show specific association preferences (Pepper et al. 1999;

Newton-Fisher 1999; Gilby & Wrangham 2008). For example, at Budongo, males with stronger alliances tend to associate in smaller subgroups (Newton-Fisher 1999). Although male-male association indices are stronger than females, evidence suggests that females, particularly older, more dominant females, benefit from stable long-term social bonds

(Pepper et al. 1999; Stumpf 2007; Gilby & Wrangham 2008; Wakefield 2008). Higher ranking females often travel together, range in areas of better quality food, and support each other during conflict, while low-ranking females rarely associate with high-ranking females (Goodall 1986; Boesch & Boesch-Achermann 2000; Williams et al. 2002).

Females are also more likely to associate with other females with whom they share overlapping core areas (Thompson et al. 2007; Gilby & Wrangham 2008).

Since male chimpanzees are philopatric, Hamilton’s (1963; 1964) inclusive fitness and kin selection theory are proposed to explain the high rates of affiliation and cooperation among male chimpanzees (Wrangham & Smuts 1980; Goodall 1986; Mitani et al. 2000).

Genetic analyses find some support for this (Morin et al.1994; Langergraber et al. 2007), while others find no significant correlation between male cooperation and genetic relatedness, suggesting that male alliance partners have more to do with close age and rank cohorts (Goldberg & Wrangham 1997; Mitani et al. 2000; Stumpf 2007).

Background in Spider Monkey Behaviour and Social Organization

Spider monkeys typically inhabit tall evergreen and semi-deciduous tropical forests in Mexico, Central and South America and are classified as endangered or critically 8

endangered throughout their geographic range (IUCN 2015). Across all long-term studies over 12 months, spider monkeys are reported to live in groups of 15-56 individuals which contain more females than males on average (Shimooka et al. 2008). Groups range within areas of 150-350 ha (Wallace 2008a) and their diet largely consists of ripe fruit (55% to

>90% of annual feeding time) supplemented with new leaves, flowers, and seeds (Di Fiore et al. 2008).

As described above, spider monkeys live primarily sexually segregated, but the degree of segregation varies seasonally and between years (Hartwell et al. 2014a). Like chimpanzees, male spider monkeys are closely bonded, interact affiliatively and cooperatively with one another more so than females (Fedigan & Baxter 1984; Chapman

1990a; Shimooka 2003; Slater et al. 2009). They form all male subgroups which are typically larger on average and show less temporal variation in size than female subgroups

(Shimooka 2005; Wallace 2008b). They travel faster than females and cover a greater area of their home range daily (Chapman 1990a; Shimooka 2005; Wallace 2008b).

Within groups, male-male aggression is rare (van Roosmalen & Klein 1988;

Fedigan & Baxter 1984; Slater et al. 2009). However, males routinely (and often cooperatively) direct aggression toward adult females (Campbell 2003; Aureli & Schaffner

2007; Slater et al. 2009). The function of female-directed aggression by male spider monkeys is not fully understood, but is likely a form of indirect sexual coercion (Link et al. 2009) and may be a mechanism for segregation between males and females (Hartwell et al. 2014a).

Female spider monkeys are described as less social than males and often travel alone with their dependent young or in small subgroups with other females and young

(Fedigan & Baxter 1984; Chapman 1990a; Slater et al. 2009). They also range within smaller, overlapping core areas (Chapman 1990a; Shimooka 2003). Using a social network analysis, Ramos-Fernández et al. (2009) found that female-female dyads had high association rates, but these associations could not be distinguished from random aggregation. The authors suggested that female spider monkeys passively aggregate at large feeding sites and show no preferences for social partners. However, Chapman

(1990a) and Shimooka (2003) report that some adult females show clear association preferences for particular females.

The association patterns of nursing and cycling females also vary across populations. At Santa Rosa National Park in Costa Rica, nursing females were more solitary and less social toward other females and males than cycling females (Chapman

1990a), while at Tikal National Park in Guatemala and La Macarena in Colombia, nursing females were more social than cycling females (Fedigan & Baxter 1984; Shimooka 2003).

At Punta Laguna in Mexico, females with infants received significantly more approaches and embraces from other females than females without infants (Slater et al. 2007) and at

Runaway Creek Nature Reserve in Belize, males were attracted to infants and preferentially handled male infants (Evans et al. 2012).

There are no clear female dominance hierarchies and aggression between females is generally low (Asensio et al. 2008; Slater et al. 2009); however, older, more long-term

resident females occasionally direct aggression toward natal subadult or newly immigrated females (Symington 1987; Asensio et al. 2008; Slater et al. 2009). Immigrant females show little association with other group members (Ramos-Fernández et al. 2009) and males are more likely to tolerate their presence than resident females (Aureli & Schaffner 2008;

Asensio et al. 2008).

Female spider monkey (and chimpanzee) social relationships appear to fit Sterck et al.’s (1997) dispersal-egalitarian category and support Wrangham’s (2000) scramble competition hypothesis. It is hypothesized that weakly bonded female spider monkeys spread out over a large area and forage alone or in small subgroups to reduce feeding competition (van Schaik & Aureli 2000; Aureli & Schaffner 2008). Since females are widely dispersed, male spider monkeys benefit reproductively by forming strong bonds and cooperating with male relatives in defending a large territory containing the ranges of multiple females (Fedigan & Baxter 1984; Symington 1988; Chapman 1990a).

Thesis Objectives

Two of the important issues identified in Aureli et al.’s (2008) re-conceptualization of fission-fusion societies are the need to quantify specific group ‘dynamics’ (i.e., variation in subgroup size, composition and spatial cohesion) and to identify the mechanisms, or factors, underlying these dynamics. Using data collected by myself and other members of the Pavelka-Notman research team from the spider monkey (Ateles geoffroyi yucatanensis) population at the Runaway Creek Nature Reserve in Belize over a six-year period from

2008 – 2013 (Figures 1 and 2), I provide a descriptive quantification of the subgrouping 11

patterns and attempt to relate variation in subgrouping patterns to changes in fruit availability and to the relatedness of individuals in the study group. The data for this study comprise 4,770 subgroup scans collected over 67 months (1,033 days) from January 2008 to September 2013. I was present for 40 out of the 67 months of data collection at Runaway

Creek, while the remaining months were collected by other graduate students and field assistants trained in the same data collection protocol. A total of 6,428 hours were spent in the forest searching, while 2,686 hours were spent in visual contact with monkeys. The lower proportion of contact time compared to time in the forest is due to the difficulty in following fast-travelling spider monkeys over the steep karst hills and cliffs that characterize the terrain at Runaway Creek. Additionally, on October 25th of 2010, in the middle of the study, a category 2 hurricane (Hurricane Richard) passed over the study site, causing habitat damage which was further exacerbated six months later by forest fires.

Figure 1. Satellite image of Runaway Creek Nature Reserve and its general location within Belize. Dotted white line= property boundary of the reserve. Red solid line= estimated home range of the spider monkey study group. Map prepared by Tracy Wyman.

Figure 2. An adult female spider monkey with her infant foraging on the leaves of

Brosimum alicastrum (Moraceae). Photo by Kayla S. Hartwell

Chapter Two provides a descriptive quantification of the fission-fusion dynamics of the study group by measuring subgroup size, subgroup spatial cohesion and subgroup stability. I also describe how these characteristics of the subgrouping patterns, or fission- fusion dynamics of spider monkeys vary by year, season, and subgroup composition

(subgroup type). Quantifying temporal variation in subgroup size, spatial cohesion, and stability is a necessary first step in the investigation of fission-fusion dynamics and the social, ecological, and genetic factors that might influence them, and this chapter is

intended to provide the reader with a good sense of the characteristics of the subgroups that the study population formed which will be useful to read the subsequent chapters.

Because spider monkey fluid ranging is generally interpreted as a response to female feeding competition, in Chapter Three, I test for a relationship between fruit availability and subgroup size, subgroup spatial cohesion, and subgroup stability using behavioural and ecological data. A number of studies have looked at the relationship between food availability and subgroup size in spider monkeys, but this is the first investigation of the effect of fruit availability on other aspects (specifically, subgroup spatial cohesion and stability) of their fission-fusion dynamics. This chapter also includes a description of the diet of spider monkeys at Runaway Creek and an evaluation of the effect of fruit availability and season on diet by comparing seasonal differences in dietary composition and the amount of ripe fruit available.

In Chapter Four I present the results of a genetic analysis of the study group to assess the role of relatedness in shaping patterns of association. Male spider monkeys exhibit strong social bonds, while females appear to be relatively indifferent to one another.

This has been suggested to be due to the fact that males remain in their natal groups while females disperse at sexual maturity to new breeding groups (Wrangham & Smuts 1980;

Goodall 1986). As a consequence, the males within a social group should be more closely related to one another than are the females. However, at most study sites, the relatedness among individuals is not known. Using genetic and behavioural data, I test the more specific hypotheses that: males within the study group are more closely related to each

other than are the females; there is greater genetic variability among females; and that relatedness among females predicts association in the same subgroups. I also measure the extent of reproductive skew among the males in order to test the hypothesis that males experience low levels of within group competition.

In Chapter Five I summarize the results of the study and reflect upon what it has contributed to our knowledge of spider monkey sociality and fission-fusion dynamics. I also acknowledge some of the limitations of this project and directions for future research.

CHAPTER 2. QUANTIFYING FISSION-FUSION DYNAMICS IN SPIDER

MONKEYS IN BELIZE: TEMPORAL VARIATION IN SUBGROUP SIZE,

SPATIAL COHESION, AND STABILITY

Introduction

Fission-fusion social organization traditionally described the fluid grouping patterns of a few mammalian species (e.g. elephants [Loxodonta africana: Wittemyer &

Getz 2005], dolphins [Tursiops spp.: Connor et al. 2000], chimpanzees and bonobos [Pan spp.: Nishida & Hiraiwa-Hasegawa 1987], and spider monkeys [Ateles spp.: Symington

1990]), in which group members regularly fission (split) and fuse (join) into subgroups of varying size and composition. However, subgrouping patterns vary greatly within and between species with ‘classic’ fission-fusion social organization. For example, chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) are considered to live in classic fission-fusion societies, yet they differ in the size, composition, and cohesiveness of subgroups. Bonobo subgroups are larger, more cohesive, less sexually segregated, and contain a higher ratio of females to males than the subgroups typically observed in chimpanzees (Kano 1992; Furuichi 2009; Wrangham 1986; Nishida & Hiraiwa-Hasegawa

1987; Furuichi 2009). Both species also vary greatly in social behaviour and subgrouping patterns across populations (White 1992; Hohmann & Fruth 2003; Boesch et al. 2002).

The traditional classification of primate social systems contrasted socially cohesive groups (which were considered the norm for most primate species) with the fluid grouping

patterns of fission-fusion societies (which were considered uncommon). However, flexible grouping patterns are not limited to species with classic fission-fusion social organization.

Among primates, there is considerable inter- and intra-species variation in the size and cohesiveness of social groups (reviewed in: Bearder 1999; Kinzey & Cunningham 1994;

Aureli et al. 2008). For example, Hamadryas baboons (Papio hamadryas) exhibit another kind of fission-fusion social organization in which males defend small groups of females within a multi-level society consisting of one-male units nested within clans, bands, and troops (Kummer 1968; Schreier & Swedell 2009). At the highest level is the troop: a large group of up to several hundred baboons that aggregate at night on sleeping cliffs. Within each troop are several bands: stable social units that travel together during the day, coordinate their movements and activities, and sleep on the same cliff each night. Within each band are a number of one-male units: a leader male, several females, and their offspring. Another level within the band are clans: several one-male units that maintain close spatial proximity throughout the day and night. Clans occasionally travel as a subgroup separate from the band (Schreier & Swedell 2009).

Spider monkeys and chimpanzees are among the least cohesive of primate species and all members of a group are rarely (if ever) together as a cohesive group. Both are large- bodied frugivores that live in large, territorial, multi-male/multi-female communities characterized by male philopatry and female dispersal (Wrangham 1979; Symington 1987,

1990; Di Fiore et al. 2009). In both species, males exhibit stronger social bonds than females, and adult females and their dependent young often travel and forage separately from adult males (Wrangham & Smuts 1980; Goodall 1986; Fedigan & Baxter 1984; 18

Chapman 1990; Shimooka 2003). Spider monkeys live primarily sexually segregated, but the degree of segregation varies seasonally and between years (Hartwell et al. 2014a).

Descriptive accounts show inter-site variation in male-female associations in chimpanzees as well (Sugiyama & Koman 1979; Stumpf 2007; Lehmann & Boesch 2008). For example, male and female chimpanzees at Taï National Park in Côte d’Iviore are more cohesive and spend more time in mixed-sex subgroups than chimpanzees studied in Western Africa at

Gombe National Park, Tanzania and Ngogo, Kibale National Park in Uganda (Boesch

1996; Pepper et al. 1999; Wrangham & Smuts 1980; Lehmann & Boesch 2004).

The variation and flexibility in primate social groups and populations led to greater interest in the flexibility that exists within and between species and populations (Strier

1994; Kinzey & Cunningham 1994; Bearder 1999; Lynch-Alfaro 2007; Aureli et al. 2008).

Following Strier (1989), Aureli et al. (2008) proposed the use of the term ‘fission-fusion dynamics’ to reflect the extent to which a social group varies in size, composition, and spatial cohesion over time. In this perspective, animal groups are characterized by their degree of fission-fusion dynamics, which can vary from high cohesion with stable group membership (i.e. low fission-fusion dynamics) to low cohesion and high sociospatial fluidity (i.e. high fission-fusion dynamics). Quantifying the variation in fission-fusion dynamics within and between species will better our understanding of the social, ecological, genetic, and demographic factors that might influence social relationships, as well as the underlying behavioural and cognitive demands imposed by them.

In this chapter, I quantify the fission-fusion dynamics of a group of spider monkeys

(Ateles geoffroyi yucatanensis) in Belize by measuring subgroup size, spatial cohesion and stability over six years. I also describe how these characteristics of the social subgrouping of spider monkeys vary by year, season, and subgroup type. Quantifying temporal variation in subgroup size, spatial cohesion, and stability is a necessary first step in the investigation of fission-fusion dynamics and the social, ecological, and genetic factors that might influence them.

Methods

Study Site and Study Group

Runaway Creek Nature Reserve is a 2,469 ha private reserve in central Belize, located approximately 30 miles west of the Caribbean Sea coast. The reserve encompasses two main vegetative zones: pine savannah and semi-deciduous, broadleaf tropical forest, and is part of a larger area of approximately 58 km2 of continuous forest. At 20 - 120 meters above sea level, the terrain at Runaway Creek encompasses steep limestone karst hills, low valleys, and seasonal swamps. This area of Belize has a dry season from December - May and a wet season from June – November, in which it receives an estimated 2,000 - 2,200 mm of rain annually (Meerman 1999).

recognizable by differences in size, pelage color, and facial markings. During the study years of 2008-2013, group size ranged from 31 to 37 individuals (5-7 adult males, 12-14 adult females, and 12-18 immatures; Table 1) due to births, immigrations, disappearances, and immatures maturing to adulthood.

Table 1. Study group size and composition over the study years 2008-2013. Subadults are included with adults.

Year Adult males Adult females Immatures Total 2008 5 13 13 31 2009 5 12 17 34 2010 7 14 14 35 2011 7 12 12 31 2012 7 12 18 37 2013 7 14 12 33

Behavioural Data Collection

With the help of field assistants, I conducted full or part day follows on spider monkey subgroups. I defined a subgroup using a “chain-rule” (Ramos-Fernández 2005) of

50 meters and considered any individual seen within 50 meters of another individual as part of the same subgroup. “Fissions” occurred when an individual moved more than 50 meters from any other subgroup member, and “fusions” occurred when an individual moved within 50 meters of another subgroup member.

During a subgroup follow, I recorded the time of first contact and conducted an instantaneous scan sample every 30 minutes to record the subgroup size and composition, subgroup spread (distance estimated in meters between the two furthest individuals in a subgroup), as well as the identity and behaviour of each monkey present. I also recorded all observations of fission and fusion events by noting the time, type of event (fission or fusion), and the identity of individuals leaving (fission) or joining (fusion) the subgroup. I stayed with the subgroup for as long as possible. In the event of a subgroup fission, I stayed with the subgroup containing individuals on which I had less data, or sometimes with the subgroup traveling in an area where I was more likely to be able to follow. A subgroup follow ended when I lost the monkeys or I left them to hike out of the forest, in which case

I noted the time and whether I lost or left the monkeys. The data for this study include

4,770 subgroup scans collected over 67 months (1,033 days) from January 2008 to

September 2013.

Measures of Fission-Fusion Dynamics

For all measures in this study, I used data on independently traveling individuals.

Thus, I treated adults and subadults (≥5 years of age) as independent individuals and excluded immatures (<5 years of age) who are dependent upon and always accompanying their mothers. I excluded consecutive scans in which there were no changes in subgroup membership and I treated subgroup scans as independent from the previous subgroup scan when there was a change in subgroup membership.

From the independent subgroup scans, I calculated mean subgroup size, which was simply the total number of individuals in a subgroup (including single individuals, i.e. subgroup size of one). Subgroup spatial cohesion is sometimes measured using subgroup spread; however, spread may not be independent of subgroup size. Larger subgroups might well occupy more area. To correct for different subgroup sizes, I divided the subgroup spread by subgroup size, which generates an estimate of the space available to each individual (as if they were spaced evenly within a subgroup). A low value for meters per individual represents high spatial cohesion and a higher value for meters per individual represents lower spatial cohesion. For this measure, I included subgroups containing at least two individuals and used data from 2009-2013 since subgroup spread was not consistently recorded in 2008.

Using all observed occurrences of an individual joining (fusion) or leaving (fission) a subgroup, I calculated subgroup stability: the duration of time during a subgroup follow in which there were no changes in subgroup membership. In other words, how long a subgroup stays together before there is a change in membership via a fission or fusion event. Because fission and fusion events were not systematically recorded in 2008, I only included data from 2009-2013 for this measure.

In this chapter, I present the variation in the above measures across months, seasons

(wet and dry season) and years (2008-2013) to explore temporal variation in these different aspects of the fission-fusion dynamics in spider monkeys. Additionally, I categorized subgroups by type as either all-male, all-female, or mixed-sex. Because spider monkeys

are sexually segregated for most of the year (Hartwell et al. 2014a) and because male and female spider monkeys differ in many aspects of their socioecology (Fedigan & Baxter

1984; Chapman 1990a; Slater et al. 2009), I investigated whether subgroup types differ in fission-fusion dynamics by comparing the above measures across the three subgroup types.

Results

Subgroup Size

Over the six years of study at Runaway Creek, I never observed the entire spider monkey group together. Subgroups ranged in size from 1-14 individuals (mean= 2.8, ±SE

0.03, median: 2.0, mode: 1.0), but rarely exceeded more than four to five individuals, and subgroups of one to two individuals were the most common (Figure 3). Mean subgroup size varied only slightly over the six years of the study (Figure 4) and was smallest in 2008

(mean= 2.3 ±SE 0.06) and largest in the year 2009 (mean= 3.4 ±SE 0.08). The overall mean subgroup size was slightly larger in the wet season compared to the dry season (3.1 vs. 2.6 individuals) and the biggest seasonal change occurred in 2009 when overall subgroup size increased by almost two individuals on average from the dry to wet season (2.7 vs. 4.3 individuals; Table 2).

30 Overall Subgroup Size (840) (827) Mean= 2.8 25 Median= 2 (643) N= 3,171 20

15 (378) 10 % Subgroups % (207) (135) 5 (65) (35) (17) (12) (4) (6) (1) (1) 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 Subgroup Size Figure 3. Overall distribution of the size of spider monkey subgroups at Runaway

Creek with the corresponding number of subgroups in parentheses above each bar.

4 2008 2009 2010 3 2011

2012 Subgroup SizeSubgroup 2 2013

1 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Figure 4. Yearly variation in mean monthly subgroup size of spider monkeys at

Runaway Creek from 2008 to 2013. Grey shaded area denotes months of the wet season.

Table 2. Temporal variation in mean subgroup size: month, season, year, and overall

2008 2009 2010 2011 2012 2013 Overall Mean Dry 2.2 2.7 2.7 2.3 2.7 2.9 2.6 Dec 2.0 2.0 1.9 3.3 2.1 Jan 2.0 1.4 2.3 1.8 2.8 3.2 2.2 Feb 2.6 1.9 2.3 2.3 2.4 2.9 2.3 Mar 1.9 2.1 2.2 2.3 2.4 3.2 2.3 Apr 2.0 3.0 2.4 2.5 2.7 2.8 2.7 May 2.3 4.0 4.8 2.5 3.0 2.2 3.2 Wet 2.5 4.3 2.7 2.6 2.6 3.5 3.1 Jun 2.4 4.1 3.3 2.4 2.4 4.0 3.0 Jul 2.4 5.0 2.7 2.8 2.9 3.3 3.6 Aug 4.8 2.8 2.7 2.2 3.4 Sep 2.7 3.9 2.4 2.5 2.5 1.7 2.8 Oct 2.4 2.8 3.1 3.8 3.2 3.0 Nov 2.7 2.7 2.5 2.0 3.1 2.6 Overall Mean 2.3 3.4 2.7 2.4 2.6 3.0 2.8

Overall subgroup size was smallest for all-female subgroups with a mean of 2.2 individuals S.E. ±0.0 (median= 2; mode= 1; range= 1-12), followed by all-male subgroups at a mean of 2.4 individuals S.E. ±0.1 (median= 2; mode= 1; range= 1-7). Mixed-sex subgroups were the largest overall with a mean of 4.1 individuals S.E. ±0.1 (median= 4; mode= 3; range= 1-14; Figure 5). I observed a subgroup containing all 12 female members of the group once in the six years of study at Runaway Creek, which occurred during the wet season of 2009. This was the only time during the study when all-female subgroups contained more than seven females at a time. Surprisingly, it was rare to see more than four males together, and only once were all seven males observed together in a subgroup.

Figure 5. Percentage of subgroups of different sizes for all-female, all-male, and mixed-sex subgroups. In parentheses above each bar is the corresponding number of subgroups.

Mean subgroup size varied across the years for all three subgroup types (Figure 6), but variation was greatest for all-female subgroups, which ranged in size from 1.6-2.8 individuals on average. Yearly means in the size of mixed-sex subgroups varied from 3.2 individuals in 2008 to 5.1 individuals in 2009, but mixed-sex subgroup size was relatively stable from 2010-2013 and averaged around 4 individuals. All-male subgroup size varied the least out of the three subgroup types with yearly means ranging between 2.1-2.8 individuals.

4 All-Female 3 All-Male

2 Mixed-Sex Mean Mean SizeSubgroup 1

0 2008 2009 2010 2011 2012 2013

Figure 6. Yearly variation in mean subgroup size for all-female, all-male, and mixed- sex subgroups of spider monkeys at Runaway Creek (2008-2013).

Across seasons, mean subgroup size for all three subgroup types tended to increase in the wet season compared to the dry season, with the exception of mixed-sex subgroups in 2010 and 2012, when subgroup size decreased by almost one individual on average. The overall mean size of all-female subgroups varied the most across seasons and in some years 28

more than other years. For example, in 2009, the subgroup size increased from 2.5 females on average in the dry season to 4 females in the wet season, and in 2012, there was almost no seasonal change in the mean size of female subgroups (dry season: 2.4 females versus wet season: 2.5 females). Seasonal variation in the size of all-male subgroups was subtler, with an overall change in mean size from 2.3 males in the dry season to 2.6 males in the wet season.

Subgroup Spatial Cohesion

Subgroup spatial cohesion, an estimate of the amount of space around each subgroup member (if they were spaced evenly within the subgroup), ranged from 0-40 meters/individual with an overall mean of 8.1 ±S.E. 0.1 meters/individuals (median:

7.5m/ind; mode: 10m/ind; Figure 7). Mean subgroup spatial cohesion varied slightly between years with a difference of less than three meters/individual. Mean subgroup spatial cohesion was lowest in 2009 (i.e. high scores indicating that subgroup members were more spatially dispersed) and highest in 2013 (i.e. low mean scores indicating that subgroup members were less spread out and more clustered together; Table 3). Overall mean subgroup spatial cohesion increased slightly in the wet season compared to the dry season.

In other words, the subgroup members were closer together on average during the wet season compared to the dry season. However, in 2009, mean spatial cohesion did the opposite trend with a mean of 8.6m/individual in the dry season and 9.1m/individual in the wet season (Table 3).

Overall Subgroup Spatial Cohesion 50 Mean= 8.1m/indv (849) Median= 7.5m/indv 40 N= 2,090

30 (505) (462)

20 % Subgroups % (182) 10 (58) (34) 0 0-4 5-9 10-14 15-19 20-24 25+ Meters Per Individual

Figure 7. Percentage of subgroups of different spatial cohesion (subgroup spread/subgroup size). In parentheses above each bar is the corresponding number of subgroups.

Table 3. Temporal variation in subgroup spatial cohesion (subgroup spread/subgroup size): Amount of space available in meters per subgroup member.

2009 2010 2011 2012 2013 Overall Mean Dry 8.6 7.6 6.4 9.7 6.6 8.2 Dec 11.0 4.8 8.5 7.5 Jan 8.6 9.3 5.0 13.5 8.5 9.3 Feb 9.6 9.1 6.4 11.1 5.0 8.7 Mar 8.9 8.7 7.4 9.8 6.5 8.6 Apr 8.3 7.3 5.4 8.5 6.8 7.7 May 7.7 6.3 6.8 8.0 7.3 7.4 Wet 9.7 6.0 8.1 7.8 6.2 8.1 Jun 8.5 4.6 7.3 8.1 5.7 7.6 Jul 10.2 6.6 8.4 6.9 4.6 8.4 Aug 9.6 7.3 7.3 8.3 8.6 Sep 10.2 3.8 11.0 10.0 16.7 9.4 Oct 8.8 6.8 8.3 7.0 7.2 Nov 11.5 5.9 16.7 6.5 7.9 Overall Mean 9.1 6.8 7.1 8.9 6.5 8.1

Overall spatial cohesion was lowest in all-female subgroups with a mean distribution per individual of 9.1 ±SE 0.17 meters (median: 8 m/ind; mode: 10 m/ind; range: 0-40 m/ind), followed by mixed-sex subgroups at 7.5 ±SE 0.16 meters per individual

(median: 6.7 m/ind; mode: 10 m/ind; range: 0-25 m/ind), and highest in all-male subgroups with a mean of 5.7 ±SE 0.34 meters per individual (median: 5 m/ind; mode: 5 m/ind; range:

0-20 m/ind; Figure 8). In other words, males are more spatially cohesive with one another, staying closer together when in a subgroup, whereas females are less cohesive and more spread out from one another.

Figure 8. Percentage of all-female, all-male, and mixed-sex subgroups of different spatial cohesion (subgroup spread/subgroup size). In parentheses above each bar is the corresponding number of subgroups. 32

There was no variation in mean subgroup spatial cohesion from dry to wet season for all-female subgroups (mean dry: 9.1 m/ind vs. wet: 9.2 m/ind) and mixed-sex subgroups

(mean dry: 7.6 m/ind vs. wet: 7.4 m/ind). Cohesiveness increased slightly in all-male subgroups from a mean of 6.1 meters per male in the dry season to 5 meters per male in the wet season. Mean spatial cohesion varied across the years 2009-2013 for all three subgroup types (Figure 9). All subgroup types were less spatially cohesive in 2009 and

2012 (i.e. subgroup members were spread further apart on average), and the greatest fluctuations in mean cohesiveness were observed in all-male subgroups. For example, male subgroup members were more spread out in 2009 at levels similar to all-female and mixed- sex subgroups (mean: 8.1 m/male), then they increased in cohesiveness by over two-fold in 2010 and 2011 (means: 3.6 - 3.8 m/male), and then dropped again in 2012 (mean: 7 m/male). In 2013, the final year of this study, all-male subgroups were at their most cohesive with a mean subgroup distribution of three meters per male.

Low All-Female All-Male Mixed-Sex 12 10 8 6 4

2 (meters/individual)

Subgroup Cohesion Spatial Subgroup 0 High 2009 2010 2011 2012 2013

Figure 9. Yearly variation in mean spatial cohesion (subgroup spread/subgroup size) in all-female, all-male, and mixed-sex subgroups.

Subgroup Stability

Overall, subgroups maintained membership for a mean duration of 34 minutes

±S.E.0.0 (median= 21mins; mode= 6mins; range= 4mins - 6hrs 45mins) before a change via an individual(s) leaving or joining the subgroup. Mean subgroup stability varied across

2009-2013 by nine minutes or less with the greatest difference in yearly means between

2009 (mean= 30mins) and 2010 (mean= 39mins). Overall mean subgroup stability decreased from dry to wet season (mean dry= 38mins versus mean wet= 30mins), meaning that subgroup membership remained unchanged for longer periods in the dry season compared to the wet season. A decrease in mean subgroup stability in the wet season occurred in every year except 2013, in which case subgroup stability increased in the wet season by four minutes. In 2010, the year with the greatest seasonal change in subgroup stability, subgroups maintained membership for a mean duration of 55 minutes in the dry

season to 29 minutes in the wet season—a difference of 26 minutes, or almost half the amount of time. In all other years, mean subgroup stability changed from dry to wet season by four to six minutes (Table 4).

Table 4. Temporal variation in mean subgroup stability (duration of time= h:mm) across months, seasons, years, and overall.

2009 2010 2011 2012 2013 Overall Mean Dry Season 0:33 0:55 0:37 0:36 0:35 0:38 Jan 0:53 1:03 0:42 0:34 0:45 0:46 Feb 0:41 0:47 0:45 0:44 0:32 0:42 Mar 0:39 0:57 0:40 0:40 0:32 0:41 Apr 0:33 0:43 0:38 0:35 0:36 0:35 May 0:24 1:04 0:26 0:30 0:33 0:28 Dec 0:38 0:51 0:34 0:44 Wet Season 0:27 0:29 0:31 0:31 0:39 0:30 Jun 0:28 1:19 0:33 0:27 0:46 0:30 Jul 0:24 0:54 0:24 0:27 0:40 0:26 Aug 0:23 0:21 0:28 0:34 0:26 Sep 0:26 0:21 0:37 0:51 0:35 0:31 Oct 0:39 0:23 0:38 0:32 0:28 Nov 0:36 0:36 1:14 1:09 0:40 Overall Mean 0:30 0:39 0:34 0:34 0:36 0:34

Overall mean subgroup stability was highest in all-female subgroups at 38 minutes

±SE 0.0 (median= 24mins; mode= 5mins; range= 4mins - 6hrs 45mins), followed by mixed-sex subgroups at 29 minutes ±SE 0.0 (median= 19mins; mode= 10mins; range=

4mins - 5hrs 31mins), and lowest in all-male subgroups at 26 minutes ±SE 0.0 (median=

16mins; mode= 5mins; range= 4mins - 3hrs 4mins). Mean subgroup stability decreased in the wet season for all three subgroup types overall (Figure 10), but seasonal variation in

subgroup stability across years revealed that all-male subgroups increased in stability during the wet seasons of 2009 and 2012.

All-Female All-Male Mixed-Sex 1:04 0:57 0:50 0:43 0:36 0:28 0:21

Membership (h:mm) Membership 0:14 Duration of of Subgroup Duration 0:07 0:00 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Figure 10. Mean monthly subgroup stability (duration of time before a change in subgroup membership) for all-female, all-male, and mixed-sex subgroups in 2009-

2013. Grey shaded area denotes the months of the wet season.

Discussion

In this chapter, I describe the fission-fusion dynamics of a group of wild spider monkeys in Belize by quantifying temporal variation in subgroup size, spatial cohesion, and stability using data on subgrouping patterns that span almost six consecutive years. I separate these descriptive data into three subgroup types (all-female, all-male, and mixed- sex), showing monthly, seasonal, and yearly values. While these data have not undergone quantitative comparative analyses here, they are illustrative of the overall subgrouping 36

patterns of the monkeys as well as of the potential range of variation in fission-fusion dynamics over a 6-year temporal scale (Table 5).

Table 5. Summary of descriptive trends

Subgroup Overall Measure Seasonal Trend Yearly SD Type Mean Overall 2.8 ind ↑ wet season +/- 0.5 ind Subgroup size Female 2.2 ind ↑ wet season +/- 0.6 ind Male 2.4 ind ↑ wet season +/- 0.4 ind Mixed-Sex 4.1 ind ↑ wet season +/- 1 ind Overall 8.1 m/ind no difference +/- 1.6 m/ind Subgroup spatial cohesion Female 9.1 m/ind no difference +/- 1.8 m/ind Male 5.7 m/ind ↑ wet season +/- 2.7 m/ind Mixed-Sex 7.5 m/ind no difference +/- 2 m/ind Overall 34 mins ↓ wet season +/- 5 mins Subgroup stability Female 38 mins ↓ wet season +/- 4 mins mostly ↓ wet Male 26 mins +/- 6 mins season Mixed-Sex 29 mins ↓ wet season +/- 4 mins

My data clearly show that the most common type of subgroup encountered were those comprised of one to two adult females (40% of 3171 subgroup observations). The next most common subgroup type were mixed-sex subgroups that contained at least three individuals (14%), followed by all-male subgroups of up to three individuals (8.5%). Thus, average subgroup size was slightly larger in males than in females, although mixed-sex subgroups were largest (mean = 4.1 individuals). These data are generally consistent with

those reported from other sites where spider monkeys have been studied. For example, at

Corcovado National Park in Costa Rica, Weghorst (2007) reports that 53% of subgroup sightings were all-female subgroups, and of those the most common subgroup consisted of two females. Similarly, the least common sightings at Corcovado were all-male subgroups

(13%), and the average mixed-sex subgroup size was 7.1 individuals (mode = 5). At

Runaway Creek, there was a mode of three individuals. In general, then, the overall size and frequency of the three subgroup types at Runaway Creek are roughly analogous to other spider monkey populations, and they likely reflect the species-characteristic demographic pattern and social organization (i.e. high adult female-to-male ratios and male philopatry) that have been recorded previously (Klein & Klein 1977; Fedigan & Baxter

1984; Symington 1988; Chapman 1990a; Shimooka 2003).

Seasonal subgroup size averages were generally consistent from year to year, both within and between years. There was, however, a trend toward larger subgroups during the wet seasons, especially in 2009 and 2013. This observation is consistent with those reported in a range of studies of species with high levels of fission-fusion dynamics; subgroups are generally larger in the wet season during periods of food abundance and smaller during the dry season in periods of relative food scarcity (Klein & Klein 1977;

Ghiglieri 1984; Symington 1988; Chapman 1988; Chapman et al. 1995; Ahumada et al.

1998; Te Boekhorst et al. 1990; Anderson et al. 2002; Heithaus & Dill 2002; Mitani et al.

2002; Muller 2002; Williams et al. 2002; Basabose 2004; Itoh & Nishida 2007; Smith et al. 2008). I will explore further the relationship between fruit availability and fission-fusion dynamics in Chapter 3. 38

As with subgroup size, subgroup spatial cohesion (i.e., the estimated distance between individuals as a function of the number of animals in a subgroup) tended to be higher (i.e., more ‘cohesive’) during the wet season, except during two years out of the six- year study. Males were generally more spatially cohesive than females; the mean estimated inter-individual distance for males was 5.7 meters, versus 9.1 for females. A number of factors may influence variation in subgroup cohesion, such as activity (Wrangham & Smuts

1980; Newton-Fisher 1999; Lusseau 2007), food patch size (Symington 1988; Chapman

1990b; Castellanos & Chanin 1996), relationship strength (Pepper et al. 1999; Ramos-

Fernández et al. 2009; Wiszniewski et al. 2009), the presence of estrous females

(Matsumoto-Oda et al. 1998; Shimooka 2003; Connor et al. 2006) and infanticide risk or predation (Boesch 1991; Boesch & Boesch-Achermann 2000; Pearson 2009). In sexually segregated species such as spider monkeys, different factors may exert pressure on subgroup cohesion in one sex disproportionately over the other (Hartwell et al. 2014a). For instance, kinship bonds may result in tighter cohesion in the philopatric sex (e.g., males in spider monkeys), while unrelated females maintain larger individual distances in order to reduce feeding competition and to avoid the risk of female-directed aggression (Asensio et al. 2008). Although in this chapter I do not systematically explore the influence of these possible independent variables on subgroup spatial cohesion, my six-year data exhibit trends that are consistent with prior work suggesting male spider monkeys are more cohesive than are females, which may be due to the relative strength of their social bonds vis-à-vis those observed between females. My data also suggest that seasonal variation

might affect spatial cohesion in male subgroups, which tend to be more cohesive in the wet season. Interestingly, female subgroup cohesion did not appear to change between seasons.

Subgroup stability is an additional dimension of fission-fusion dynamics that reflects the degree to which individuals move (or fission and fuse) in-and-out of subgroups.

I observed a tendency for subgroup stability to decrease in the wet season. The underlying factors that might affect variation in subgroup stability are less clear than those hypothesized to affect size and cohesion, but some published accounts suggest that subgroup stability might reflect relative fruit availability (see chapter 3).

Summary

My objective in this chapter was twofold: first, I wanted to describe, and operationally define three important dimensions of fission-fusion dynamics (subgroup size, spatial cohesion, and stability) that serve as my dependent variables in subsequent analyses in my study. Second, I described, using seasonal and yearly values over a six-year timeframe, the range of variation intrinsic to these three measures of fission-fusion dynamics displayed by this population of spider monkeys. In essence, my goal was to portray the social fluidity of this population using broad descriptive strokes, while at the same time providing some quantitative context that will be a starting point for analyses in later chapters of my thesis. My descriptive data suggest some seasonal variation in these three subgroup measures, and, as fruit availability is likely tied to season, this further suggests that at least part of the spider monkey subgrouping behaviour is determined by changes in food resources. I will explore this specific relationship in the next chapter. 40

CHAPTER 3. THE EFFECTS OF FEEDING ECOLOGY ON FISSION-FUSION

DYNAMICS IN SPIDER MONKEYS

Introduction

Animal social groups vary along a continuum from highly cohesive (low fission- fusion dynamics), to highly fluid (high fission-fusion dynamics; Strier 1989; Aureli et al.

2008). Group-living animals tend toward cohesiveness, forming social groups in which group members synchronize their daily movements, and species living in social groups with a high degree of fission-fusion dynamics are less common. In these latter species (e.g. bottlenose dolphins [Tursiops spp.]: Connor et al. 2000; several species of bats: Altringham

& Senior 2005; chimpanzees [Pan troglodytes] and spider monkeys [Ateles spp.]:

Symington 1990; Chapman et al. 1995), members live within a closed social group, but travel and forage independent from one another. Group members leave (fission) and join

(fusion) others in subgroups, and as a result, subgroups frequently change in size, composition, and spatial cohesion. High fission-fusion dynamics are thought to mitigate the costs of group living by adjusting subgroup size to changes in the spatial and temporal availability of food resources (Klein & Klein 1977; Wrangham & Smuts 1980; Symington

1990; Chapman 1990a). By foraging in smaller subgroups, researchers argue that individuals can reduce feeding competition and time spent traveling between food resources (Chapman & Chapman 2000; Korstjens et al. 2006; Lehmann et al. 2007). By implication, larger food patches should be able to support larger subgroups, and vice versa.

The actual relationship between food availability and subgroup size, however, is not clear and research in this area has yielded conflicting results. In chimpanzees and spider monkeys, for example, some studies have found a positive correlation between habitat-wide fruit availability and the size of subgroups (Symington 1990; Chapman et al.

1995; Mitani et al. 2002; Shimooka 2003; Asensio et al. 2009), while others found little to no correlation between fruit availability and subgroup size in these same species (Pan:

Newton-Fisher et al. 2000; Hohmann & Fruth 2002; Hashimoto et al. 2003; Wakefield

2008). A recent study on spider monkeys (A. hybridus) living in a small forest fragment in Colombia also revealed that subgroups were smaller when fruit availability was high compared to when it was low (Rimbach et al. 2014). While the authors of this study concede that the fragmented habitat may have affected normal subgrouping patterns in this particular population, the conflicting results of studies on both genera suggest that factors other than fruit availability may affect subgroup size, or that there may be other aspects to fruit availability affecting subgroup size that have yet to be detected.

Spider monkeys are considered ripe fruit specialists and typically consume >75% ripe fruit in their diet, supplemented with young leaves, flowers, seeds, and sometimes decayed wood, insects, other small prey items during periods of fruit scarcity (reviewed in:

Di Fiore et al. 2008; González-Zamora et al. 2009). Spider monkeys living in highly seasonal forests (Stevenson et al. 2000; Wallace 2005), small forest fragments (Chávez et al. 2012; Rimbach et al. 2014), or areas damaged from hurricanes (Schaffner et al. 2012;

Champion 2013) cope with periods of fruit scarcity by increasing their consumption of leaves, as well as a greater variety of food items (González-Zamora et al. 2009). Spider 42

monkeys and other species with high fission-fusion dynamics may also adjust to reduced levels of fruit availability by modifying the size, stability, and spatial cohesion of subgroups to avoid feeding competition (Schaffner et al. 2012; Champion 2013; Rimbach et al. 2014).

In this chapter, I examine the feeding ecology of a group of spider monkeys in

Belize and investigate the relationship between fruit availability and subgrouping patterns using behavioural and vegetation data collected over five and a half consecutive years. My objectives in this chapter are first, to describe the diet of spider monkeys at Runaway

Creek; second, to evaluate the effect of fruit availability and season on diet by comparing seasonal differences in dietary composition and the amount of ripe fruit available; and third, to examine the relationship between fruit availability and three important aspects of fission-fusion dynamics: subgroup size, subgroup spatial cohesion, and subgroup stability.

I predict that the monkeys will eat more fruit during periods of relatively higher fruit availability (i.e., the wet season). Although previous research (reviewed above) has been conflicting with respect to the effects of fruit availability on subgroup size, in the main, current socio-ecological theory predicts greater fruit availability will lead to larger group size. Accordingly, I predict here that the spider monkeys will range in smaller subgroups during periods of low fruit availability, and range in larger subgroups during periods of high fruit availability (Chapman 1990a; Shimooka 2003; Asensio et al. 2009). I anticipate that periods of high habitat-wide fruit availability may lead to more cohesive but less stable subgroups, as individual monkeys move more frequently between resources while at the same time tolerating closer inter-individual proximity when contest competition is reduced. 43

Methods

Study Site and Study Group

Runaway Creek Nature Reserve is a small 2,469 ha private reserve in central Belize, located approximately 30 miles inland from the Caribbean Sea coast. The reserve has two main vegetation zones: pine savannah and low broadleaf, semi-deciduous tropical forest.

The forest is comprised of steep karst hills with caves, low valleys, and seasonal swamps, and is connected to approximately 58 km2 of similar habitat to the west, but is otherwise surrounded by pine savannah and citrus plantations. This area of Belize has a dry season from December to May and a wet season from June to November in which it receives an estimated 2,000-2,200mm of rain annually (Meerman 1998; Figure 11).

Figure 11. Monthly rainfall in the Belize’s capital city of Belmopan (Cayo District), which is located approximately 35km west of Runaway Creek Nature Reserve. Data include monthly rainfall records from 1979-2014 (source: http://hydromet.gov.bz).

Since 2008, I have been part of a research team studying the behaviour and ecology of a group of wild spider monkeys (Ateles geoffroyi yucatanensis) at Runaway Creek. All individuals in the study group are habituated to researchers’ presence and are individually recognizable by differences in size, pelage color, and facial markings. Over the course of this study, the group ranged in size from 31 to 37 individuals (5-7 adult males, 12-14 adult females, and 12-18 immatures) due to births, immigrations, disappearances, and immatures maturing to adulthood.

Behavioural Data Collection

With the help of field assistants, I conducted full or part day follows on spider monkey subgroups. I defined a subgroup using a “chain-rule” (Ramos-Fernández 2005) of

vegetation expert. I also recorded all observations of the monkeys consuming a new species and plant part, and kept an on-going food species list throughout the study.

During a subgroup follow, I also recorded all observations of fission and fusion events by noting the time, type of event (fission or fusion), and the identity and age/sex class of individuals leaving (fission) or joining (fusion) the subgroup. I stayed with the subgroup for as long as possible. In the event of a subgroup fission, I stayed with the subgroup containing individuals on which I had fewer data, or sometimes with the subgroup traveling in an area where I was more likely to be able to follow. A subgroup follow ended when I lost the monkeys or I left them to hike out of the forest, in which case

I noted the time and whether I lost or left the monkeys.

Measures of Fission-Fusion Dynamics

For the following measures of fission-fusion dynamics (below), I used data on independently traveling individuals. Thus, I treated adults and subadults (≥5 years of age) as independent individuals and excluded immatures (<5 years of age) who are dependent upon, and always accompanying their mothers. To increase the independence of samples,

I excluded consecutive scans in which there were no changes in subgroup membership and

I treated subgroup scans as independent from the previous subgroup scan when there was a change in subgroup membership.

From the independent subgroup scans, I calculated mean subgroup size, which was simply the total number of individuals in a subgroup (including single individuals, i.e.

subgroup size of one). Subgroup spatial cohesion is sometimes measured using subgroup spread; however, spread may not be independent of subgroup size. Larger subgroups might well occupy more area. To correct for different subgroup sizes, I divided the subgroup spread by subgroup size, which generates an estimate of the space available to each individual (as if they were spaced evenly within a subgroup). A low value for meters per individual represents high spatial cohesion and a high value for meters per individual represents low spatial cohesion. For this measure, I included subgroups containing at least two individuals.

Using all observed occurrences of an individual joining (fusion) or leaving (fission) a subgroup, I calculated subgroup stability: the duration of time (minutes) during a subgroup follow in which there were no changes in subgroup membership. In other words, how long a subgroup stays together before there is a change in membership via a fission or fusion event.

Vegetation Data Collection

With the help of field assistants, I sampled twenty-one 40 m x 40 m (1600 m2) vegetation plots in the range of the study group and in all habitat types used by the monkeys, which include swamp, low valley, karst hill top, ridge side, and transitional forest

(to savannah). Within the vegetation plots, I identified and measured the diameter at breast height (DBH) of all trees over 10cm DBH. If a tree species was unknown, I flagged the tree for later identification with the assistance of a botanist or local vegetation expert. A tree’s DBH is an indicator of the size of the tree and has been shown to reflect the trees 47

fruit production (Leighton & Leighton 1982; Peters et al. 1988; Chapman 1990b; Chapman et al. 1992). These data provided a measure of the area of a cross section of a tree trunk

(DBH/2 = R [radius], πR2= area), which I then used to calculate species basal area (sum of the area for each tree of species A) and species dominance (total basal area of species

A/total area sampled).

To track temporal variation in ripe fruit availability, I monitored a phenology trail on a biweekly basis (twice a month) from January 2009 – July 2013. The trail included 225 trees from 15 food tree species, each represented by 15 individual trees. I chose species for the phenology trail based on the top fruit species consumed by the spider monkeys at

Runaway Creek (not including vines) that constituted greater than 2% of their diet each

(Table 6). Each phenology tree was scored with an estimate of ripe fruit on the crown as one of: 0, 25%, 50%, 75%, and 100%. I then took the mean proportion fruit coverage score for each tree species and multiplied it by the dominance value for that species. To provide a biweekly fruit availability score, I summed all scores across the 15 species for each biweekly period. This resulted in an index of estimated relative fruit availability over time. (Note: hereafter, “fruit availability scores” refers to ripe fruit availability).

Table 6. List of phenology tree species and their percentage in the spider monkey diet at Runaway Creek.

Family Genus Species Common Name % Moraceae Ficus insipida Fig 14 Sapotaceae Manilkara staminodella Sapodilla 10 Moraceae Ficus pertusa Fig 8 Arecaceae Attalea cohune Cohune Palm 8 Burseraceae Protium copal Copal 8 Anacardiaceae Metopium brownei Black Poisonwood 7 Anacardiaceae Spondias radlkoferi Hog Plum 6 Moraceae Pseudolmedia spuria Wild Cherry 5 Arecaceae Sabal yapa Tiger Bay Leaf Palm 4 Moraceae Brosimum alicastrum Wild Breadnut 4 Ulmaceae Ampelocera hottlei Female Bull Hoof 3 Caesalpiniaceae Dialium guianense Ironwood 3 Fabaceae Caesalpinia gaumeri Warrie Wood 3 Moraceae Trophis racemosa Red Ramon 2 Simaroubaceae Simarouba glauca Negrito 2

Data Analysis

My first objective was to describe the overall diet of the spider monkeys at

Runaway Creek and examine variation in dietary composition over time. I quantified the diet composition throughout the study (2008-2013) as the proportion of scan feeding records in which the monkeys were feeding on the different plant parts (ripe fruit, unripe fruit, leaves, flowers, or ‘other’). I partitioned these data by month and season to evaluate temporal variation in diet composition. For my second objective, to evaluate the effect

of fruit availability and season on diet, I ran a one-tailed Independent Sample Student’s t

Test to determine 1) if the proportion of ripe fruit in the spider monkeys’ diet increased from the dry season to the wet season, and 2) if the proportion of leaves in their diet decreased from the dry to wet season. I ran the same (two-tailed) analysis to determine if the proportion of unripe fruit and flowers differed between seasons. Likewise, I used a one- tailed Independent Sample Student’s t Test to determine if the amount of fruit available

(based on monthly fruit availability scores) increased in the wet season compared to the dry. To evaluate the extent to which the fruit availability scores predicted the proportion of ripe fruit in the spider monkeys’ diet, I performed a linear regression.

Finally, my third objective was to examine the relationship between temporal variation in fruit availability and three measures of fission-fusion dynamics (subgroup size, spatial cohesion, and stability). For analysis of fruit availability, I discarded every other phenology sample to increase the independence of the fruit availability scores. As a result,

I have a fruit availability score once per month (N= 50), which was analysed in relation to the subgrouping variables (size, spatial cohesion, and stability) drawn from one week before and one week after the date of the phenology sample used in the fruit availability score. I tested the extent to which fruit availability predicted variation in subgroup size, spatial cohesion, and stability using linear regression. The fruit availability scores were not normally distributed (violating one of the assumptions of parametric tests) so I log transformed the fruit availability scores and used these normally distributed values for analysis. I performed all analyses in IBM SPSS Statistics version 23.

Results

Diet Composition

Over the five and a half years of study at Runaway Creek, we observed the monkeys feeding from 121 plant species representing 83 genera and 47 families (Appendix A). Of those, three families (Moraceae, Anacardiaceae, and Arecaceae) represented over half of their diet, most notably Moraceae, which constituted 39% of all plant items consumed by the spider monkeys. Their overall diet was composed of 60% fruit (48% ripe and 12% unripe fruit), 30% young leaves, 8 % flowers, and 0.5% ‘other’ items (limestone, soil, and insect eggs). The remaining 1.5% of their diet were items that were unknown and could not be identified. The diet composition varied over the five and a half years of study

(Figure 12).

Ripe Fruit Unripe Fruit Leaves Flowers 100% 90% 80% 70% 60% 50%

40% Overall Diet Overall 30% 20% 10% 0% 2008 2009 2010 2011 2012 2013

Figure 12. Yearly variation in dietary composition of spider monkeys at Runaway

Creek from 2008-2013.

Seasonal Differences in Diet

Based on the mean monthly fruit availability scores for all study years combined, there appears to be two fruiting peaks within an annual cycle: one smaller peak at the very end of the dry season in May, and a larger fruiting peak toward the end of the wet season in October-November (Figure 13). Although mean monthly fruit availability scores were slightly higher in the wet season than in the dry, these differences were not significant (t=

-1.34, df= 49, p= .093).

2.5

1.5

1 Fruit Availability Fruit 0.5

0 Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov Dec

Figure 13. Mean monthly fruit availability scores across 2009-2013. Grey shaded area denotes months of the wet season.

The results of the Student’s t test indicated that there was no statistical difference in the proportion of ripe fruit in the spider monkeys’ diet during the wet season (mean=

.60) compared to the dry season (mean= .46; t= -1.51, df= 56, p= .069), as well as no

seasonal differences in the proportion of leaves consumed (mean wet= .34 versus dry= .29; t= -9.85, df= 56, p= .165). However, there was a significant difference in the proportion of unripe fruit in the diet from wet (mean= .07) to dry (mean= .12) season (t= 2.13, df= 56, p= .037), as well as the proportion of flowers (mean wet= .03 versus dry= .13; t= 3.2, df=

39, p= .003; Figure 14). During the dry season, the spider monkeys increased their consumption of flowers (primarily from Brosimum alicastrum, Pseudobombax ellipticum, and the vine Combretum fruticosum) and preyed on the seeds of unripe fruit from

Brosimum alicastrum, Pseudolmedia spuria, and Caesalpinia gaumeri.

Dry Wet 0.7 0.6 0.5 0.4 0.3

0.2 * * Proportion of Diet of Proportion 0.1 0 Ripe Fruit Unripe Fruit Leaves Flowers

Figure 14. Diet composition of spider monkeys at Runaway Creek during the wet and dry seasons of 2008-2013. The asterisk denotes food items that differ significantly between seasons.

Although fruit availability scores were not significantly different between seasons, they were positively correlated with the proportion of ripe fruit in the spider monkeys’ diet

(Linear regression: F= 29.28, df= 44, R2= .405, p= < .001; Figure 15) and they explained

41% of the variation in ripe fruit consumption. In addition, the consumption of fruit over the study years tracked temporal variation in fruit availability (Figure 16).

Figure 15. Scatter plot showing the positive relationship between fruit availability and the proportion of fruit in the spider monkey diet.

Figure 16. Temporal variation in monthly fruit availability scores (bars) and the proportion of ripe fruit in the spider monkeys’ diet (line) from 2009-2013.

Fruit Availability and Fission-Fusion Dynamics

The results of the linear regression model revealed that there is no relationship between fruit availability and subgroup size in the Runaway Creek spider monkey population (F= 2.97, df= 46, R2= .062, p= .092). Similarly, fruit availability did not predict subgroup spatial cohesion (F= .233, df= 46, R2= .005, p= .632). However, fruit availability is a significant predictor of subgroup stability (F= 14.25, df= 45, R2= .245, p= < .000;

Figure 17) and explained 25% of the variance. As fruit availability increases, subgroup stability decreases (the duration of time before a change in subgroup membership becomes shorter). In other words, spider monkey subgroups are more fluid when there is more fruit available, and subgroup membership is more stable when fruit availability is low.

Figure 17. Scatter plot showing subgroup stability decreases as fruit availability increases.

To assess how fruit availability might affect female subgrouping patterns when males were not present, I ran the analysis a second time on all-female subgroups, omitting all-male and mixed-sex subgroups. The results of the linear regression model revealed that fruit availability is positively related to the size of all-female subgroups (F= 5.08, df= 45,

R2= .101, p= .029). Female spider monkeys tend to range in larger subgroups when fruit availability is higher. However, this only explains 10% of the variance in size. Fruit availability is also a significant predictor of female subgroup stability (F= 7.35, df= 45,

R2= .14, p= .009), explaining 14% of the variance. As fruit availability increases, all-female subgroups become less stable and more fluid. The linear regression also indicated that fruit availability does not predict spatial cohesion in females (F= .672, df= 45, R2= .015, p=

.209). 56

Because the damage to the forest from Hurricane Richard and subsequent forest fires may have affected fruit availability and its influence on spider monkey subgrouping patterns, I ran the analyses once more using only subgrouping data (including subgroups with males) from before the hurricane (i.e. January 2009 to October 25, 2010). Indeed, fruit availability significantly decreased following the hurricane (t= 3.03, df= 68, p= .002). The results of the linear regression revealed that fruit availability pre-hurricane was significantly related to subgroup size (F= 5.46, df= 15, R2= .281, p= .035), as well as subgroup stability (F= 11.96, df= 16, R2= .44, p= .004). Once again, fruit availability was not a predictor of subgroup spatial cohesion (F= .183, df= 15, R2= .012, p= .338).

Discussion

My objectives for this chapter were to describe the feeding ecology of spider monkeys and to explore the relationship between feeding ecology and fission-fusion dynamics; namely, how fruit availability might influence variation in subgroup size, spatial cohesion, and stability. I show that spider monkey diets are variable from year to year, but that they consistently contain a large proportion of ripe fruit, and that ripe fruit availability positively predicts the amount of fruit in their diet. Spider monkeys are typically characterized as ripe fruit specialists, because between roughly 75% and 90% of their diet is based on fruit (Wallace 2005; Di Fiore et al. 2008). In my study, ripe fruit consumption never exceeded 75%, but when unripe fruit is included, the category of ‘fruit’ accounts for

48-82% of their annual diet. An important factor to consider here is the effect of Hurricane

Richard in 2010 on fruit consumption. Ripe fruit consumption was highest in the pre- 57

hurricane years (2008-09), but dropped precipitously after 2010, as fruiting trees ceased fruit production in many parts of the forest that sustained wind damage (Champion 2013).

Given this situation, my results are generally consistent with those across study sites, which demonstrate that spider monkeys show an overwhelming preference for fruit over nutritionally poorer yet more abundant food resources (Dew 2005; Stevenson et al. 2000).

My results also show that spider monkeys can substitute leaves and flowers for fruit when fruit availability is relatively low. In the post-hurricane years, both leaf and flower consumption increased, and flower consumption increased during the dry season more generally. Leaves can be a seasonally important food item to spider monkeys, particularly during periods of fruit scarcity. For example, Ateles belzebuth chamek in northeastern

Bolivia is highly frugivorous except for one or two months during the dry season when leaves constitute up to 36% of their diet (Wallace 2005). Similarly, leaves represent over half the diet of A. b. belzebuth in La Macarena, Colombia, during the end of the rainy season when fruit is scarce (Di Fiore et al. 2008). At Runaway Creek, leaf consumption approached 50% in 2012, and was generally higher in post-hurricane years than in pre- hurricane years. The proportion of leaves in their diet after the hurricane is comparable to that observed in spider monkeys confined to small forest fragments (Chávez et al. 2012;

Rimbach et al. 2014), and this may speak to the effects that even non-anthropogenic habitat disturbances have on the diet of this species. Interestingly, and contrary to my expectation, fruit availability did not significantly increase during the wet season, although mean availability scores did trend toward higher values during the wet season. However, spider monkeys did consume more fruit when fruit was relatively more abundant, and their 58

consumption of fruit seems to be at least in part determined by its availability across different months.

High fission-fusion dynamics are hypothesized to result from contest competition over patchily-distributed and temporally unpredictable fruit resources. Accordingly, I predicted that fruit availability would have an effect on subgroup size (larger subgroups would be observed during periods of higher fruit availability, and vice versa), and I expected that subgroup stability would decrease, and spatial cohesion increase, during relative fruit abundance. Contrary to my prediction, when males and females were analyzed together across all study years, I found no correlation between fruit availability and subgroup size. However, when females were analyzed separately, fruit availability did affect subgroup size in the predicted direction, as it also did in pre-hurricane years, even when males were included in the analysis. There are a number of ways to interpret these results. One possibility is that males and females associate at random with respect to fruit availability, so larger, mixed-sex subgroups (see Chapter 2) were not affected by fruit availability. Interestingly, prior research has shown that spider monkeys are sexually segregated, and that males and females are more often segregated when fruit availability is high (Hartwell et al. 2014a). This fact might explain why, when males were included in this analysis, subgroup size did not significantly increase with fruit availability because it was during periods of relatively lower fruit availability that larger, mixed-sex subgroups were formed. That female subgroup size was larger during periods of higher fruit availability may have obscured a clear, linear relationship between these two variables when males and females were analyzed together, and it also confirms my initial prediction 59

in light of what is understood about female socio-ecology vis-à-vis that of males. As female reproductive fitness is limited by access to food, females are predicted to distribute themselves to best take advantage of food resources and minimize contest competition, thus rendering their behavioural patterns more sensitive to ecological pressures such as food availability (Dunbar 1988; Clutton-Brock 1989). In other words, variation in female subgrouping patterns might more accurately reflect changes in fruit availability than does variation in all-male or mixed-sex subgroups, which could be caused by some other factors, such as the availability of estrous females (for mixed-sex groups) or more consistent rates of association among philopatric males (see Chapter 4).

The fact that fruit availability did affect overall subgroup size before the hurricane in 2010, however, does somewhat challenge this interpretation. It is possible that the variable effects of fruit availability on the respective subgrouping patterns of males and females is too subtle to be apparent from the smaller sample used in the pre-hurricane analysis. Alternatively (or in addition), the habitat changes caused by the hurricane may have created conditions in which the respective fitness interests and optimal ecological requirements of male and female spider monkeys were forced into starker contrast, which was reflected in my results when females were analyzed separately from the overall dataset.

The effect of fruit availability on the two other dimensions of fission-fusion dynamics analyzed here (subgroup spatial cohesion and stability) was more clear; in all analyses, higher fruit availability was correlated with lower subgroup stability, and fruit availability never had an effect on subgroup spatial cohesion. The first result is consistent

with my hypothesis that, when more fruit is available, individual monkeys have more patch options to choose from and therefore they may move between these patches more often.

My observation here that spider monkey subgroups are less stable when fruit availability is high is consistent with results from two recent studies that showed subgroups were more stable in times of fruit scarcity following a hurricane at a site in Mexico (Schaffner et al.

2012; Champion 2013). The fact that fruit availability had no effect on spatial cohesion is a bit more surprising, as I expected higher fruit availability to lead to higher spatial cohesion as closer inter-individual proximity between subgroup members might be tolerated when contest competition was potentially reduced. However, it is possible that my measure of spatial cohesion was too crude to capture the effects of fruit availability on this aspect of subgrouping behaviour. In addition, it might be that food patch size exerts a more powerful influence on spatial cohesion than does overall fruit availability. Future research in this area would benefit from a more detailed analysis of the differential effects of food patch size and overall availability on a more accurate measure of spatial cohesion, such as inter-individual distances between each subgroup member (Wallace 2008c).

In this chapter I have shown that temporal variation in some features of fission- fusion dynamics does correlate with resource availability, and this corroborates research on other spider monkey populations and on other taxa (Smith et al. 2008; Shimooka 2003;

Wallace 2005). However, it is also clear from my own and others’ research that variation in food availability alone is insufficient to explain variation in subgroup size, spatial cohesion, and stability in species characterized by high fission-fusion dynamics (Lehmann

& Boesch 2003; Chapman & Rothman 2009). A growing body of evidence suggests that 61

demographic and social factors interact with ecological drivers in determining the spatial arrangement of group members (Murray et al. 2007; Fury et al. 2013), and, within this potentially complex synergy of influences, individual decisions to join, leave, or remain in a certain subgroup are thrown into the mix. Therefore, the co-occurrence of individuals in subgroups (spatiotemporal association) must encompass these individual decisions and their underlying influences (Aureli et al. 2012; Smith-Aguilar et al. 2016).

Directions for Future Research

To test more accurately how, and the extent to which ecological factors may affect fission-fusion dynamics, future studies would benefit by incorporating other, and more refined measures of fruit availability, such as patch size and fruiting tree density, as well as assessments of food distributions throughout the home range, and how variability in these measures interacts with subgrouping behaviour. In addition, a more accurate food availability index might include foods less-frequently consumed by the animals, but which nonetheless might constitute an important part of their diet, and which, if highly valued, might also affect levels of contest competition and subsequent subgrouping patterns. Such food species could include vines and epiphytes, as well as other more ephemeral food resources that are rare but nutritionally critical.

In the next chapter (Chapter 4), I investigate an additional potential influence on subgrouping patterns; namely, that of relatedness. I have suggested here, and shown elsewhere (Hartwell et al. 2014a) that ecological and social factors may exert fitness pressures differently on males and females in species that are sexually segregated. In spider 62

monkeys, demographic factors such as male philopatry may have a greater influence on variation in fission-fusion dynamics than on females, who may be more sensitive to changes in habitat food supply, and less constrained by relatedness and the need to associate with allies.

CHAPTER 4. PATTERNS OF GENETIC RELATEDNESS IN A POPULATION

OF SPIDER MONKEYS IN BELIZE

Introduction

Spider monkeys (Ateles spp.) live in a social system characterized by a high degree of fission-fusion dynamics in which group members are rarely, if ever, together as a cohesive group. Instead, individual members of a group split (fission) and merge (fusion) into subgroups of variable size and composition (Fedigan & Baxter 1984; Chapman et al.

1995; Aureli et al. 2008). Among mammals, this type of social system with high fission- fusion dynamics is also characteristic of bottlenose dolphins (Tursiops spp.: Connor et al.

2000), elephants (Loxodonta africana: Wittemyer et al. 2005), spotted hyenas (Crocuta crocuta: Holekamp et al. 1997), chimpanzees and bonobos (Pan spp.: Nishida & Hiraiwa-

Hasegawa 1987), and humans (Rodseth et al. 1991; Marlowe 2005).

Like many mammals with high fission-fusion dynamics, spider monkeys live primarily sex-segregated (Hartwell et al. 2014a) and males and females differ in many aspects of their socio-ecology. Male spider monkeys within a group are closely bonded to one another and interact affiliatively (e.g. embraces, grooming, and body contact) at rates much higher than among females (Fedigan & Baxter 1984; Ramos-Fernández et al. 2009).

They typically travel together as an all-male subgroup over a large area containing the ranges of multiple females, and cooperate in territory boundary patrols and defense against intrusions from males of neighbouring groups (Chapman 1990a; Shimooka 2003; Aureli 64

& Schaffner 2008). All adult males within a group mate and there is little to no evidence of a male hierarchy (Campbell & Gibson 2008). Based on these observations, male spider monkeys are assumed to experience high between-group and low within-group competition for mates.

In contrast to males, female spider monkeys spread out over a large home range to reduce feeding competition over patchily distributed ripe fruit, and travel and forage alone or in small subgroups with other females and their young (Fedigan & Baxter 1984;

Chapman 1990a; Shimooka 2003). Female social relationships appear undifferentiated, and they are described as weakly bonded, associating in subgroups in which membership is random (Chapman 1990a; Shimooka 2003; Aureli & Schaffner 2008; Ramos-Fernández et al. 2009).

Like chimpanzees and bonobos, spider monkeys are characterized by male philopatry and female dispersal (Symington 1988; Shimooka et al. 2008; Di Fiore et al.

2009). Most female spider monkeys leave their natal group once sexually mature (reviewed in: Shimooka et al. 2008). These findings, coupled with the fact that male spider monkeys are closely bonded and engage more frequently in affiliative and cooperative behaviours than do females (Fedigan & Baxter 1984; Symington 1990; Aureli & Schaffner 2008), suggest that male philopatry and female dispersal is the norm in spider monkeys. This characterization is largely based on behavioural and demographic observations.

Recent advances in molecular methods have made it easier and more cost-effective to analyze genetic data (Di Fiore 2003), which can then be used to test previously held 65

assumptions about dispersal and philopatry (reviewed above), as well as to explore the way in which genetic relatedness might explain variation in association patterns in societies with high fission-fusion dynamics. For example, one such assumption that has received empirical support in a number of primate studies is that group-level relatedness is higher in the philopatric sex than in the dispersing sex (Inoue et al. 2008; Wikberg et al. 2012;

Wikberg et al. 2014a). By extension, kin selection theory predicts, and observation generally confirms that, higher levels of within-sex genetic relatedness underlie sex-biased affiliation patterns and cooperation among philopatric individuals, including association and grooming patterns as well as agonistic support (Wrangham & Smuts 1980; Sterck et al. 1997; Silk 2006; Smith et al. 2010; Archie et al. 2011).

The assumption of higher genetic relatedness in the philopatric sex and, by implication, higher affiliation and cooperation has not gone unchallenged, particularly in species that have been typically characterized as ‘male philopatric’. For example, in at least two studies on chimpanzees, relatedness among males was not significantly higher than that among females (Vigilant et al. 2001; Lukas et al. 2005). In a more recent study of East African chimpanzees (P. troglodytes schwienfurthii), Langergraber et al. (2009) found that the highest subgroup association indices were consistently found in non-related female, as opposed to male dyads, and that party association was as strongly correlated with spatial proximity and grooming for females as it was for males. Such observations have led some to propose that sex-biased dispersal may not necessarily lead to disparate degrees of relatedness between sexes, as well as that the immigrating sex (i.e., females in

male-philopatric species) may form close social bonds in the absence of relatedness (Lukas et al. 2005, Lehmann & Boesch 2008, 2009).

Two factors that might affect the degree of male relatedness in male-philopatric species are the size of the social group and the amount of reproductive skew caused by differential mating access among males (Lukas et al. 2005; Inoue et al. 2008). Small social groups containing few reproductively active males could result in increased genetic relatedness in subsequent generations of offspring. Similarly, differential access to fertile females could result in reproductive skew in favour of one or just a few males (Lukas et al.

2005; Boesch et al. 2006). As social groups become larger, the number of potential male competitors and reproductively synchronous females will increase and thus dampen the effects of reproductive skew (Boesch et al. 2006).

A third possible factor, of course, that might affect the degree of relatedness among males is immigration. Although rarely reported in male-philopatric species such as chimpanzees (e.g. Sugiyama 1999), factors such as habitat ecology and disturbance, population density, and severity of intragroup male-male competition may affect the likelihood and ability of males to either transfer groups, start new groups or, at the very least, reproduce outside their natal groups despite the potential costs of doing so. Any one or all of these scenarios may be mechanisms for increasing genetic diversity both within and between social groups, and populations more widely.

As with studies on chimpanzees, the available data on spider monkeys concerning dispersal patterns, genetic relatedness, and the effects of both on within-sex association 67

and affiliation are somewhat mixed with respect to identifying species-wide traits. In general, spider monkeys have been characterized as described above; that is, as having strong male alliances that result from life-long residency in the natal group, in contrast to immigrant females who have largely undifferentiated social relationships, except in specific contexts such as among longer-resident females at the arrival of a new immigrant or among females with infants (Aureli & Schaffner 2008). The implication of such a social system for expected relatedness patterns is that males should exhibit a higher degree of genetic relatedness than females. Indeed, in an analysis of a large group of white-bellied spider monkeys (A. belzebuth) living in an undisturbed habitat, Di Fiore et al. (2009) found that adult males were, on average, more related to each other than were adult females.

Although available data support this general picture of Ateles, a handful of more recent studies that have capitalized on long-term datasets also point to the possibility of greater social flexibility than previously considered. For example, in a population of A. geoffroyi from Costa Rica, Aureli et al. (2013) report the immigration of eight adult males over a two-year period into a group from which all resident males had previously disappeared. In addition, the cohort of immigrant males exhibited an overall low degree of relatedness that was not statistically different from that of the females in the group. These authors also report the consistent occurrence of coalitions among the unrelated immigrant males, and relatively infrequent male-male aggression (Aureli et al. 2013). This study provided further empirical support for an earlier one on a population of white-bellied spider monkeys (A. belzebuth) comprised of two distinct but adjacent groups, one of which contained an unrelated male among a cohort of related males, and in the other, males 68

exhibited a low overall degree of relatedness (Di Fiore at al. 2009). These authors suggest that demographic factors, such as the number of adult males in a group, might affect the likelihood of male emigration/immigration; if the number of resident males becomes too large, transfers may occur, especially if the number of resident males in a candidate transfer group (such as an adjacent one) is low.

It seems likely, then, that spider monkeys do not conform to the ‘rule’ of male philopatry, and that sex-biased dispersal is not exclusively weighted in favour of females.

Nor does it appear that relatedness plays a predominant role in determining within-sex association patterns and cooperation; unrelated females can form lasting associations that equal those of males in strength and duration, and males can cooperate to defend a territory and resident females even when their overall relatedness to one another is relatively low.

It remains, then, to explore further the variability between populations of spider monkeys in relatedness patterns to establish a foundation from which to predict when and in what contexts the degree of relatedness might have consequences on social behaviour and the evolution of social systems.

In this chapter, I conduct a genetic analysis of a group of wild spider monkeys

(Ateles geoffroyi yucatanensis) in Belize to: 1) assess the genetic evidence for sex-biased dispersal; 2) document the amount of reproductive ‘skew’; and 3) to investigate the role of relatedness in shaping patterns of association in a society with high fission-fusion dynamics where subgroup membership is variable.

Specific Hypotheses

1. Based on previously published demographic and behavioural data

(reviewed above), it is generally assumed that male spider monkeys are philopatric and are more closely related to each other than are females to each other. However, other findings have challenged this assumption, suggesting that there may be more flexibility in sex- dispersal patterns than previously appreciated (Di Fiore et al. 2009; Aureli et al. 2013). I will therefore examine the degree of relatedness among adult males compared to adult females, as well as between the sexes, and test if there is a sex-bias in dispersal patterns.

While I make no formal prior predictions about the direction of sex-bias in relatedness (and dispersal), I suspect, based on my observations of the monkeys, that males will be more closely related than are females, reflecting a female-biased dispersal pattern.

2. Male spider monkeys are generally seen to be dealing with high levels of between-group competition for mates (Link et al. 2009). They travel further and faster than females on a daily basis, apparently in an effort to maintain exclusive access to the widely dispersed and weakly bonded females. While male-male interactions are affiliative within a group, encounters with males from outside the group are aggressive and can be lethal

(Aureli et al. 2006; Wallace 2008b). Additionally, there is no evidence of a male dominance hierarchy, and all males are observed mating. Male spider monkeys appear to experience high between-group competition and low within-group competition for access to mates.

Therefore, I hypothesize that all adult males sire offspring and therefore reproductive skew among males will be low.

3. Assuming that there is variation in relatedness among group members and within and between the sexes, I will examine the role of genetic relatedness on association patterns of same-sex and mixed-sex dyads by comparing pairwise estimates of relatedness to association indices of subgroup membership. Because females are believed to be unrelated, I do not expect relatedness to be a determinant of female association in subgroups. I expect most male-female dyads to be unrelated with the exception of a few mother-son dyads (assuming that males are philopatric and their mothers are still alive).

Because spider monkeys live sexually segregated for most of the year (Hartwell et al.

2014a), I do not expect relatedness to correlate with association of male-female dyads.

Since I suspect that the males are related and they typically travel together, I predict the degree of relatedness is more likely to correlate with association among males.

Methods

Study Area and Study Group

Runaway Creek Nature Reserve is a 2,469 ha private reserve in central Belize

(88°35’ W and 17°22’N) comprising two main vegetative zones: pine savannah and semi- deciduous, broadleaf tropical forest, and is part of a much larger area of continuous forest.

At 20-120 meters above sea level, the landscape at Runaway Creek is dominated by steep limestone karst hills, low valleys, and seasonal swamps. This area of Belize has a dry season from December-May and a wet season from June-November, in which it receives an estimated 2,000-2,200 mm of rain annually (Meerman 1999).

Since 2008, I have been part of a research team studying the behaviour and ecology of a group of wild spider monkeys at Runaway Creek. All individuals in the study group are habituated to being followed by researchers and are individually recognizable by differences in size, pelage color, and facial markings. During the study years of 2008-2013, group size varied from 31 to 37 individuals (5-7 adult and subadult males, 12-14 adult and subadult females, and 12-18 immatures) due to births, immigrations, disappearances, and immatures maturing to adulthood. For this study, I use the following age classes and age estimates for each class: adult ≥ 8 years, subadult 5-8 years, and immatures < 5 years. I distinguished immatures from subadults as those always traveling with their mothers, and following other research on spider monkeys, I considered a male to be subadult when he was older than five years of age and sexually mature (i.e. descended testes), but not yet full adult size (van Roosmalen & Klein 1988; Shimooka et al. 2008; Aureli et al. 2013).

Behavioural and Molecular Data Collection

With the help of field assistants, I conducted full or part day follows on spider monkey subgroups. I defined a subgroup using a “chain-rule” (Ramos-Fernández 2005) of

50 meters; any individual seen within 50 meters of another individual was considered to be part of the same subgroup. “Fissions” occurred when an individual moved further than

50 meters from any other subgroup member, and “fusions” occurred when an individual moved within 50 meters of another subgroup member. During subgroup follows, I conducted an instantaneous scan every 30 minutes to record the subgroup size and composition, as well as the identity and behaviour of each monkey present.

I opportunistically collected fecal samples from recognizable individuals to use as a source of DNA for genetic analysis of relatedness. I collected at least 3 samples per individual, although for a few of the juveniles I was only successful in collecting one sample. I stored the samples in a vial of 5mg RNAlater (QIAGEN), a reagent that stabilizes cellular RNA and DNA until the sample is processed. The fecal samples were stored at room temperature and then at -20°C once shipped to Dr. Anthony Di Fiore at the Primate

Molecular Ecology and Evolution Lab (PMEEL) at the University of Texas at Austin (UT

Austin) for genotyping.

DNA Extraction

After receiving training by Dr. Di Fiore and PhD candidate Amely Martins at the

PMEEL at UT Austin, I extracted DNA from the fecal samples using commercially available nucleic acid isolation mini stool kits (QIAGEN, QIAmp). I followed the manufacturer’s protocol for isolation of DNA from stool for human DNA analysis with the following modifications recommended by Dr. Di Fiore: a) samples were left to lyse in ASL buffer at 56°C for 12-26 hours, b) samples incubated in proteinase K and buffer AL for 30 minutes, c) buffer AE was heated to 70°C prior to application, d) extracted DNA incubated in buffer AE at room temperature for 30 minutes, and d) DNA was eluted for six minutes in a centrifuge.

Following extraction, I genotyped the DNA samples of 39 spider monkeys from the study group using a panel of 11 polymorphic short tandem repeat (STR) loci (Table 7), which are shown to be polymorphic in other spider monkey populations (Di Fiore et al. 73

2009; Aureli et al. 2013). I genotyped loci using a modification of the multiple tubes approach (Taberlet et al. 1996; Di Fiore et al. 2009) and with commercially available kits

(Qiagen, Inc.) for multiplex polymerase chain reactions (PCR) with 5’ fluorescently labeled forward or reverse primers (Vigilant et al. 2001). I followed the manufacturer’s protocols, but ran the PCRs at a total reaction volume of 8μl. I sent the microsatellite PCR products for fragment analysis to the Core facility at UT Austin where they were separated via capillary electrophoresis in an automated fluorescent sequencer (ABI 3730). Using the software program GeneMapper 4.2, I viewed the fragment analysis results and called the allele sizes. Following Di Fiore et al. (2009), I replicated genotypes for each individual at each locus a minimum of two times for heterozygotes and four times for homozygotes.

Analyses of Microsatellite Genotypes

Using the multilocus genotypes of the 39 individuals, I calculated allele frequencies in the computer program ML-Relate (Kalinowski et al. 2006), and performed a Hardy-

Weinberg test to detect the presence of null alleles using Nei’s (1978) unbiased estimate of expected heterozygosity. The level of observed heterozygosity in Locus #5 was significantly lower than expected (permutations, p = 0.027; Table 7), suggesting the presence of null alleles. Since null alleles were present in Locus#5, ML-Relate used maximum likelihood estimates of the frequency of null alleles in all calculations of relatedness.

Table 7. Panel of microsatellite markers used for genotyping the Runaway Creek spider monkeys. N = number of individuals genotyped; Na = number of alleles, Hobs = observed heterozygosity; Hexp = expected heterozygosity under Hardy-Weinberg equilibrium = 1 - Sum π2; ns = not significant; *= significant deviation between Hobs and

Hexp (p < 0.05).

Locus N Na Hobs Hexp Significance Apm01 37 6 0.946 0.833 ns D5S111 21 2 0.714 0.494 ns D8S165 38 3 0.579 0.56 ns D8S260 37 6 0.892 0.767 ns Leon 2 38 5 0.789 0.703 ns Leon 21 24 4 0.708 0.621 ns LL 1-1#10 21 3 0.667 0.575 ns LL 1-5#7 38 4 0.553 0.518 ns Locus#5 33 6 0.636 0.747 * SB 30 36 4 0.778 0.626 ns SB 38 28 3 0.75 0.608 ns Average 4.25 0.728 0.641

To meet my first objective, I calculated maximum likelihood estimates of relatedness (R) in ML-Relate using the multilocus genotypes of the 39 spider monkeys.

This method accommodates null alleles during the relatedness estimations, and is considered to be more accurate than other estimators (Milligan 2003). Maximum likelihood estimate of relatedness calculates a dyadic R-value ranging from zero to one, where values closer to one indicate individual dyads that are genetically more similar to one another than what would be expected given the allele frequencies in the population, and values closer to zero indicate individuals who are genetically less similar than expected. Using the 75

estimated R-values, I then calculated mean relatedness among all male-male dyads (N =

21) and female-female dyads (N = 105) and tested whether the means were significantly different by running permutation tests in Visual Basic for Applications within Microsoft

Excel (permute code available from Di Fiore; Di Fiore & Fleischer 2005).

To further investigate genetic evidence for sex-biased dispersal, I calculated population assignment indices by determining the likelihood that an individual’s multilocus genotype originated in the population from which it was sampled (Paetkau et al. 1995). I standardized the assignment indices by subtracting the mean assignment index of the population from each individual’s index value (Favre et al. 1997). Individuals with a positive “corrected” assignment index (AIc) values are more likely to have been born in the study group, whereas individuals with negative AIc values are more likely immigrants.

I calculated AIc values for all individuals of reproductive age (7 males and 15 females) in

GenAlEx 6.5 (Peakall & Smouse 2006) and compared males versus females using a Mann-

Whitney test.

For my second objective, I examined the distribution of assigned paternities of the

19 immatures genotyped in the study group and tested for reproductive skew to evaluate the level of competition for mates among intra-group males. Using the genotypes of immatures, candidate sires, and known mothers, I ran a paternity analysis in Cervus, which calculates a ‘likelihood ratio’ by comparing the probability that a male is a sire with the probability that a male is not the sire. This method takes into account the allele frequencies in the population when calculating the probability of obtaining a particular offspring’s

genotype given the genotypes of the mother and candidate sire (Edwards 1972). For each assigned offspring-sire pair, Cervus calculates an ‘LOD’ score (Kalinowski et al. 2007), where a positive LOD score indicates a male who is more likely to be the true sire than not the true sire, and a negative LOD score indicates that a male is more likely to not be the true sire than the true sire. I assigned paternity based on the delta score, which is the difference between LOD scores of the first most-likely candidate sire and the second most- likely candidate sire. This method minimizes the risk of incorrectly assigning a male as the true sire when another male also shares a high LOD score with an offspring. To account for the probability that the actual sire was not sampled and genotyped, I ran a paternity simulation test assuming that 90% of the population was sampled, 80% of the loci were genotyped, and that there was a 1% chance of mistyping the genotypes. I completed the paternity analysis using both a strict (95%) and relaxed (80%) confidence interval. I tested all adult males as potential sires depending on the birth year of the immature. There were five potential sires for offspring born prior to 2011 and seven potential sires for offspring born after 2011, which represents roughly the time when two males (Fiddle and Fryjack) matured to sub-adulthood and were observed copulating with adult females.

To test for reproductive skew, I calculated Nonacs’ B-index (Nonacs 2000) using the number of assigned paternities and breeding tenure length (the number of study years as a potential sire) for each adult male. This index calculates a B-value, which indicates the degree of reproductive skew among the males—negative values indicate that the reproductive contribution among the males is lower than expected by chance, and values

close to zero indicate that reproductive contribution does not differ from random expectation (no reproductive skew).

For my third objective, I used social analyses in SOCPROG 2.5 (Whitehead 2009) to evaluate whether genetic relatedness predicts association among adult spider monkeys in the study group. Here I defined association as presence in the same subgroup (subgroup membership was recorded every 30-mins during scan samples). I used the simple ratio association index (SRI), which is considered an unbiased estimate of the proportion of time two individuals spend together (Ginsberg & Young 1992). For each dyad, I calculated an

SRI value which is the ratio of the number of scan samples in which two individuals were recorded in the same subgroup divided by the number of scan samples in which at least one of them was identified. Following Gilby and Wrangham (2008), I standardized each value by dividing by the mean of all dyads to ensure meaningful comparison across indices.

Next, I used Dietz (1983) R-test to determine whether there is a linear relationship between association in the same subgroup and degree of relatedness by constructing and comparing a matrix of dyadic SRI values with a matrix of dyadic R-values. Dietz R-test, a variation of the Mantel test (Mantel 1967; Schnell et al. 1985), replaces the values in the matrices by their ranks, and is less strongly affected by large (or small) outlying values than the Mantel test (Whitehead 2009). The identities of the individuals in the matrices were permutated 10,000 times and a matrix correlation coefficient (r) was calculated for each permutation. The true (observed) value of r for the association matrix was then compared to the distribution of the randomly generated r values to determine statistical

significance. I tested for a correlation between SRI values and relatedness R-values for all female-female dyads (15 females, 105 unique dyads), male-male dyads (7 males, 21 unique dyads), and male-female dyads (22 individuals, 231 unique dyads).

Results

Male vs. Female Relatedness & Dispersal Patterns

The first objective of this study was to examine the distribution of relatedness among male and female dyads and to test whether the study group has greater male philopatry and female-biased dispersal. The distribution of estimates of relatedness (R- values) reveal that the majority of male-male and female-female dyads share no genetic relatedness with R-values close to zero (Figure 18). The remaining distributions of R-values for male and female dyads are similar and overlap, with the set of most-closely-related dyads containing both male-male and female-female pairs. The average estimated relatedness (mean R-value) among the seven adult males is 0.15 (SD: ± 0.181), whereas that among the 15 adult females is slightly lower at 0.079 (SD: ± 0.125), but this difference is not significant (permutation test: p = 0.974). In other words, males are not more closely related on average than are females, contrary to what would be expected if males are philopatric and females disperse.

0.7

0.6

0.5

0.4

0.3

Proportionof Dyads 0.2

0.1

0 0 0.1 0.2 0.3 0.4 0.5 Relatedness

Figure 18. Distribution of relatedness values among male-male (black bars) and female-female (grey bars) dyads of spider monkeys at Runaway Creek. Shown is the proportion of dyads whose estimate of relatedness falls within the noted range.

Similarly, corrected population assignment indices (AIc) reveal that both males and females are residents, and both males and females are immigrants (Table 8; Figure 19).

There is no significant difference in mean AIc values of males compared to females (N1 =

7, N2 = 15, z = 0.388, p = .698), meaning there is no direct evidence for sex-biased dispersal in the study group. AIc frequency distributions reveal a division among the adult males

(Figure 19): three males with positive “more resident” values and four males with negative

“more immigrant” values. Among the adult females, AIc values vary greatly and include the two most negative and positive values in the study group. Fig is scored with the most

“resident” value (AIc = +1.829) and Fro is scored with the most “immigrant” value (AIc =

-2.893). However, most of the adult females had AIc values close to zero, suggesting that

they are no more likely to be immigrants than they are to be residents based on their genotypes.

Table 8. Corrected population assignment indices (AIc) of the 7 adult males and 15 adult females in the spider monkey study group at Runaway Creek. Individuals with negative AIc values are more likely to be immigrants, and those with positive AIc values are more likely to have been born in the study group.

Individual ID Sex AIc Fro F -2.893 False-Frog M -1.132 Flirt F -1.036 Freckles F -0.983 Fer-de-lance M -0.767 Flora F -0.567 Flower F -0.562 Fryjack M -0.372 Flame F -0.349 Fiddle M -0.262 Fugly F -0.031 Forget F 0.074 Ficus F 0.248 Fury F 0.353 Forest M 0.508 Faita M 0.541 Fungus F 0.883 Fanta F 0.925 Frog M 1.045 Frugivory F 1.090 Franjipani F 1.457 Fig F 1.829

Figure 19. Frequency distributions of corrected assignment index (AIc) values of adult males (dark grey bars) and adult females (light grey bars) at Runaway Creek.

The dispersing sex will typically exhibit more negative values, but genetic evidence from members of this study group suggest no sex bias in dispersal.

Paternity Analysis & Reproductive Skew

The second objective of this study was to investigate whether intra-group males experience low reproductive competition by examining the distribution of paternity and testing for reproductive skew among the seven adult males. Paternity was assigned to 14 of the 19 immatures genotyped in the study group—13 were assigned using a strict (95%) confidence interval and one additional offspring was assigned using a relaxed (80%) confidence interval (Table 9). The paternity results reveal that all adult males in the study group sired offspring except for one of the younger adult males (Fiddle).

Table 9. Assigned paternities and associated significance measures for 19 immatures in the study group over the years 2008-2013. LOD score is the natural log of the overall likelihood ratio, where positive LOD scores signify that the candidate sire is more likely to be the true sire than not the true sire (positive LOD = the father) and negative LOD scores signify that the candidate sire is more likely to not be the true sire (negative LOD = not the father). * = most likely sire with strict (95%) confidence interval; + for relaxed (80%) confidence interval.

Offspring Most Likely Trio Loci Trio Loci Trio Trio Trio

ID Sire Compared Mismatching LOD Delta Confidence 1 Fig Faita 10 0 5.42 5.42 * 2 Frijoles Faita 7 0 6.25 6.25 * 3 Fufu Faita 8 0 3.79 3.79 * 4 Fullmoon Faita 6 0 4.23 4.23 *

5 Fauna Faita 7 1 -1.17 0.00

6 Fire Faita 7 1 -1.81 0.00

7 Flip Faita 9 1 -1.15 0.00 8 Fruit False-Frog 7 1 4.12 4.12 + 9 Fiddle False-Frog 8 0 6.70 6.70 * 10 Frugal False-Frog 7 1 2.89 2.89 * 11 Falcon Fer-de-lance 7 0 4.76 4.76 * 12 Fickle Fer-de-lance 7 0 3.47 3.47 * 13 Flea Fer-de-lance 9 0 4.32 4.32 * 14 Fingers Forest 8 1 9.90 9.90 * 15 Frodo Frog 8 1 2.87 2.87 *

16 Fifi Frog 8 1 -1.25 0.00

17 Fryjack Frog 8 2 -4.56 0.00 18 Finch Fryjack 8 0 2.64 2.64 * 19 Fossil Fryjack 7 1 1.06 1.06 *

Based on the number of offspring sired during the study years 2008-2013

(excluding offspring born prior to the onset of the study) and the breeding tenure of each of the seven adult males in the study group (Table 10), the result of the Nonacs’ B-index is close to zero, indicating that there is no difference between the observed distribution of sires and what would be expected by chance (B = -0.01, p = 0.5931). In other words, there is no sign of reproductive skew among the seven adult males in the study group.

Table 10. Number of offspring sired per adult male and the number of study years as a breeding male. The number of offspring sired is based on the paternity analysis at 95% confidence interval and includes offspring born during the study years 2008-2013, excluding offspring born prior to the onset of the study.

# of offspring # of study years as breeding Offspring per Father ID sired male year Faita 3 5 (2008-2013) 0.6 Fer-de-lance 3 4 (2008-2012) 0.75 False-Frog 2 4 (2008-2012) 0.5 Fryjack 2 2 (2011-2013) 1 Frog 1 5 (2008-2013) 0.2 Forest 1 4 (2009-2013) 0.25 Fiddle 0 2 (2011-2013) 0

Correlation between Subgroup Membership (Association) & Relatedness

To meet my third objective, I tested whether there was a correlation between association (SRI values) and degree of relatedness (R-values) between same-sex and mixed-sex dyads. Mean SRI values are highest in male-male dyads (mean SRI: 1.67, SD: 84

±1.14, range: 0.25 – 3.58), followed by female-female dyads (mean SRI: 1.25, SD: ±0.62, range: 0.17 – 2.92), and are lowest in dyads of the opposite sex (mean SRI: 0.68, SD: ±0.30, range: 0.08 – 1.58). Based on dyadic SRI and R-values, the results of the Dietz R-test reveal no correlation between association and relatedness in either same-sex dyad (male-male: r

= -0.01, p = 0.51; female-female: r = 0.07, p = 0.24), or mixed-sex dyads (male-female: r

= 0.11, p = 0.1). Interestingly, several female-female dyads are close relatives, but associate at levels below average, such as Frugivory and Franjipani (R-value = 0.5, SRI = 0.87) and

Fungus and Flirt (R-value = 0.5, SRI = 0.93). In contrast, some male-male dyads share little to no genetic relatedness, yet associate at levels far above average, e.g. Forest and Fer-de- lance (R-value = 0, SRI = 2.8), Faita and False-Frog (R-value = 0.17, SRI = 2.87). See

Appendix B for a complete list of dyadic SRI and R-values.

Discussion

Male vs. Female Relatedness & Dispersal Patterns

In this chapter, I examined the genetic structure of 39 spider monkeys from one group in Belize, and investigated the role of genetic relatedness in influencing subgroup membership, which has been identified as an important dimension of fission-fusion dynamics. My first objective was to examine the average genetic relatedness of males compared to females, and by calculating corrected population assignment indices (AIc) to detect whether there is a sex-bias in dispersal patterns. These analyses reveal that males are no more closely related on average than are females, contrary to what would be expected

if males were exclusively philopatric and females disperse. This observation was supported by the AIc values, which revealed that both females and males are potential residents and immigrants.

While this finding is surprising given previously held assumptions about the genetic

(and behavioural) consequences of sex-biased dispersal, it is not without precedent and it does support a growing body of evidence that is emerging from other spider monkey sites that challenge this long-held view of the species. As reviewed earlier, low overall male relatedness has been reported in two other spider monkey sites (Di Fiore at al. 2009; Aureli et al. 2013). Taken together, my and other studies suggest that sex-biased dispersal is not necessarily a species-wide characteristic, or that male-philopatry does not always result in high male relatedness (Langergraber et al. 2009; Wikberg et al. 2012). This latter possibility could result from demographic factors, such as a high number of males coupled with low male reproductive skew, or intermittent male immigration.

Although male immigration has not been observed directly at Runway Creek, an individual in my sample with one of the lowest AIc values (i.e., likely to have immigrated) is an adult male, False-Frog. Although an adequate sample of long-term datasets on spider monkey dispersal patterns from different sites is still lacking, for the most part the data suggest that male dispersal/immigration is rare and might occur under certain demographic conditions, such as when there is a small number of adult males, a high female-to-male ratio, or, conversely, when there is a surplus of extra-group males (Aureli et al. 2013;

Hohmann 2001; Korstjens et al. 2007; Struhsaker 2010). For instance, Di Fiore et al.

(2009) suggest that the loss of several resident males due to hunting may have created an opportunity for male immigration in a group of A. belzebuth in Ecuador. Groups with only a few adult males might be vulnerable to immigration and take over by extra-group males who are drawn to the high female-to-male ratio (Aureli et al. 2013). Indeed, at the start of the study in 2008, there were only three adult males including, False-Frog. It is possible that he immigrated into the study group during a time when there were a small number of resident adult males. Indeed, a census of a neighbouring group to the study group counted up to 11 adult males (unpublished data). That two adjacent groups would have such unequal numbers of males might have facilitated a transfer into the study group before data collection began.

My finding that some females may also be philopatric in this group is more puzzling. In a review of long-term studies on wild populations of spider monkeys

(Shimooka et al. 2008), emigration and immigration typically occurs in nulliparous females around the age of four to six years. In my study, the individuals with the most “resident”

(i.e., highest) AIc values were adult females, Fig, Franjipani, and Frugivory. However, female philopatry has been reported in spider monkeys (Aureli et al. 2013). Chimpanzees, who are also traditionally classified as female dispersed show occasional female philopatry, particularly by the daughters of long-resident (high-ranking) females who occupy higher-quality areas of a home range (Pusey et al. 1997), which may in turn confer reproductive benefits (Thompson et al. 2007). Interestingly, I observed a similar pattern at Runaway Creek with at least one female. Fig, who at the end of the study I estimated to be at least ten years old, has remained in her natal group with her mother and two younger 87

siblings even though three other females from her age cohort disappeared by 2010 and are assumed to have emigrated. Fig was always observed in association with her mother

(Flower) and rarely associated in a subgroup without her mother present. Even Fig’s younger sister (born in 2009) displayed indications of readying herself for emigration, such as distancing herself from her mother and ranging without her.

In contrast to the females that stayed in their natal group, Fro, another adult female, has the lowest AIc value, which strongly suggests that she immigrated from another group.

When this study began in 2008, Fro was a subadult and I did not know whether she was pre- or post-dispersal. Three years later she gave birth to her first infant. Fro’s genotype contains unique alleles at two different loci (Locus#5 and SB30) that are not found in any other individual (except she passed one of the unique alleles to her son), suggesting that she may have come from a spider monkey population outside of Runaway Creek.

Paternity & Reproductive Skew

The results of the paternity analysis reveal that all adult males in the study group sired offspring (with the exception of one younger adult male) and there is no significant evidence of reproductive skew, confirming that male spider monkeys, at least within this study group, experience low intra-group competition for mates. These results are consistent with my own observations of the strong social bonds between males of the same group, but they contrast with reports from other sites at which incidences of intra-group male aggression and competition have been observed (Campbell 2006; Valero et al. 2006; Vick

2008; Aureli & Schaffner 2008; Rebecchini et al. 2011). In almost six years of continuous 88

study at Runaway Creek, no incidences of intra-group male aggression have been reported thus far, and all adult/subadult males have been observed copulating with females

(unpublished data).

Correlation between Relatedness and & Association Patterns

For my third objective, I used a combination of behavioural and genetic data to examine the extent to which association (presence in the same subgroup) is correlated with the degree of relatedness of subgroup members, as previous studies on a variety of primate species have suggested that kinship might govern association patterns such as subgroup membership and proximity (Guilhem et al. 2000; Kapsalis 2004; Carter et al. 2013,

Wikberg et al. 2014b). The results of the Mantel Dietz R-test reveal that degree of relatedness has no effect on association between individuals. My analysis revealed that there are close relatives that do not associate as well as nonrelatives that do. Some female- female dyads are close relatives, but overall associate at rates lower than average.

Similarly, some male-male dyads share little to no genetic relatedness, yet they associate at rates higher than average.

That unrelated females might associate together in the same subgroups is not that surprising, as chance predicts that, in the absence of active avoidance tactics, limited feeding sites and limited degrees of freedom in dyad partners will eventually lead to unrelated individuals coinciding in the same subgroups. In addition, some unrelated females might preferentially choose to associate, particularly longer-tenured, resident

females who have established core areas and who may form coalitions against younger, immigrant females (Watts 1991, 1994; Kahlenberg et al. 2008; Wikberg et al. 2014c).

More surprising is the degree of cooperation among potentially unrelated males, in the form of consistent subgroup membership, proximity, and affiliative behaviours. If male spider monkeys are truly ‘male-bonded’ (as their behaviour suggests) while at the same time no more related to one another than are females, what keeps them together? One possible mechanism for cohesion among male spider monkeys might be their behavioural synchrony. Previous studies have suggested that behavioural synchrony might provide a mechanism for social cohesion in species that exhibit fission-fusion dynamics, particularly among socially homogeneous groups (i.e., those comprised of individuals of similar age and size; Ruckstuhl 1999; Conradt & Roper 2000), or in species that display low levels of affiliative behaviour (Pavelka 2011). In a study looking at the mechanisms behind sexual segregation in spider monkeys, Hartwell et al. (2014a) found that males were highly synchronous in their behaviour, travelling, resting, and feeding together at the same time, in a way that females were not. These authors suggest that both the fitness and energetic demands on adult male cohorts overlap sufficiently to enable greater cohesion (and synchrony) than that found in females, whose asynchronous energetic demands (as determined by fertility status, tenure [rank], and differential access to foods) might force greater independence from each other and from males.

The results of this study reveal that spider monkeys at Runaway Creek do not closely conform to previous assumptions regarding male-philopatry/female dispersal in

Ateles. The prediction that male-philopatry would yield greater relatedness among males vis-à-vis females was not supported by my results, as males in the study population appeared to be no more related to each other than were females. (Although I made no specific prediction about the direction of sex-biased relatedness, given recent studies that have also challenged the classic “male-philopatry” assumption in spider monkeys, I did informally assume that my results would yield a stronger relatedness among males than they did). Lower degrees of relatedness among males might be the result of some combination of factors that may include male immigration from other groups, low reproductive skew, or larger groups that contain many reproductive males and females, either currently or in the recent past.

Summary and Future Research

In this chapter I analyzed the genetic structure of a group of spider monkeys (Ateles geoffroyi yucatanensis) at Runaway Creek Nature Reserve, Belize in an effort to 1) document and describe patterns of relatedness among and between individuals, 2) compare relatedness with and between sexes in order to determine whether there was genetic evidence for sex-biased dispersal and reproductive skew, and 3) to examine whether there is a correlation between relatedness between individuals and association in the same subgroups. I predicted that males would be more related to each other than are females due to female-biased dispersal, and this prediction extended to my expectation that female association patterns would not be related to their association patterns. I also predicted that

there would be little reproductive skew, as within-group male competition is assumed to be low in male-philopatric species.

My analysis shows, however, that males are no more related to one another than are females, which raises the possibility that males are not exclusively philopatric. This possibility was supported by the observation that some females displayed genotypes indicating that they could also be life-long residents (philopatric) in the group. My prediction that the spider monkeys would exhibit low reproductive skew was confirmed.

Taken together, these data suggest that male emigration and immigration may occur more consistently than previously recognized, or at least occasionally in the recent past, and demographic factors at the start of the study (i.e., low number of adult males living next to a group with many adult males) further hint at this possibility.

I also found that degree of relatedness did not correlate with the likelihood of associating in the same subgroup in males or females, despite my prediction that it would do so in males. This raises the question of what mechanism(s) other than relatedness and the fitness benefits of kin selection might be responsible for observed levels of cohesion and cooperation among males at Runaway Creek and elsewhere. One possibility considered here is that cohesion is facilitated by within-subgroup behavioural synchrony, which is facilitated by overlapping metabolic and fitness interests that are shared by adult males.

While my results do support a growing body of research that recognizes greater variability in primate social organization and behaviour than previously considered, there 92

remains room for research that, on the one hand, casts a wider sampling net at the population (as opposed to the group) level of genetic analyses, while on the other looks more closely at aspects of inter-individual relationships among spider monkey males and females. Population-level analyses would provide a broader view of genetic relatedness between groups that might help us to better understand some of the genetic patterns observed within groups. The questions of whether, and how frequently male migration and female philopatry actually occur could be addressed by an analysis of population-level genotypes from neighbouring groups.

CHAPTER 5. GENERAL DISCUSSION

My initial aim in beginning this project was to better understand the subgrouping patterns, or fission-fusion dynamics, in the spider monkey population at Runaway Creek

Nature Reserve in Belize, where I had completed my Master’s thesis project on sexual segregation. I wanted to describe and quantify the kinds of subgroups that the spider monkeys were forming and better understand the causes and consequences of the subgrouping patterns. The spider monkeys are very different from the black howler monkeys at Runaway Creek and at Monkey River where I have also worked. Black howlers are folivores that live in consistently small and tightly cohesive groups (low fission-fusion dynamics) with small ranges and group spread. Spider monkeys, on the other hand, are frugivores that live in ‘classic’ fission-fusion societies: large, highly fluid social groups with large home ranges over which flexible subgroups are widely dispersed. I wanted to understand which monkeys associated with which other monkeys, and when, and why. Toward this much larger objective, in this thesis I described fission-fusion dynamics by quantifying temporal variation in subgroup size, spatial cohesion, and stability, and examined these three measures for all-female, all-male, and mixed-sex subgroups. Second, I examined the diet composition of the spider monkeys across seasons and years and investigated the relationship between fruit availability and the three subgrouping measures. Lastly, I assessed genetic evidence for sex-biased dispersal, examined the amount of reproductive skew among intra-group males, and investigated the role of relatedness in shaping patterns of association (subgroup membership).

The emerging picture is one of spider monkey subgroups that are mostly just one or two females and their immature offspring associating (that is, feeding and ranging roughly 10 meters apart) for only a short period of time. A change in subgroup membership, by the leaving or joining of (an) individual(s) occurs on average every 30-40 minutes. Occasionally larger subgroups form; however, contrary to what I expected, these larger subgroups were not predicted by the habitat-wide index of fruit availability that I calculated. It may be that different measures of fruit availability would produce different results. For example, one future research direction will be to try to link subgroup size to the size of the patch of fruit occupied at any one time. Another may be to consider the role of fallback food (flowers at Runaway Creek, unpublished data) which, owing to their importance during periods of fruit scarcity, may affect the distribution of the monkeys, particularly females, at least at certain times. My habitat-wide measure of fruit availability, however, did explain 25% of the variance in subgroup stability, with subgroups changing membership more often when fruit availability was high.

All-female subgroup size is smaller on average than all-male or mixed-sex subgroups, but more variable over time, which is at least in part related to fruit availability.

In addition, although there are more precise ways to measure subgroup spatial cohesion, the method that I used (subgroup spread/subgroup size) revealed that female subgroup spatial cohesion is much less variable over time than all-male subgroups. Females consistently space themselves (even in mixed-sex subgroups) about 8-10m apart on average, regardless of season or fruit availability.

All-male subgroups were the least common subgroup type observed, which is not surprising given the sex ratio of the study group with twice as many females as males. In addition, males travel faster and further than females which makes them difficult to follow, especially over the hilly and steep terrain at Runaway Creek. Similar to the descriptions of male spider monkeys at other sites (Fedigan & Baxter 1984; Chapman 1990a; Shimooka

2003; Wallace 2005), all-male subgroups were larger on average and had greater spatial cohesion than subgroups containing females. Surprisingly, it was rare to see more than four males together, and only once were all seven males observed together in a subgroup.

In the data presented in this thesis, male subgroups were also more fluid (i.e. subgroup membership changed more often) than all-female subgroups. This may be a function of the difficulty of maintaining observation on all-male subgroups given their speed of travel and the difficult terrain at Runaway Creek. Male spider monkeys at Runaway Creek do appear to be strongly bonded to one another (e.g. frequent affiliative interactions such as embraces, body contact while resting, and mutual maintenance of proximity), as would be expected if they have a regime of high between-group and low within-group competition for access to females (Link et al. 2009). Close spatial cohesion may help them maintain strong bonds and aid in their cooperation against extra-group males. The assumption that male-male competition is also mitigated by kin selection was challenged, however, by my genetic analysis which revealed that group males are no more related to one another than are females, and that males in the group are equally likely to be immigrants as they are natal residents. The assumption of low within-group competition for females, however, was supported by the paternity analysis showing all males in the group sired offspring.

To the question of who associates with whom, this is the first study on spider monkeys to investigate relatedness as a factor predicting the tendency for females to associate in the same subgroups. Spider monkeys are generally assumed to be characterized by male philopatry and female dispersal, meaning that relatedness is not expected to be influencing female-female association patterns. However as noted above, this study revealed that at Runaway Creek males are not more closely related on average than are females, contrary to what would be expected if males are philopatric and females disperse. Thus it is not surprising that female-female dyads reflect a range of relatedness scores (R-values), which I tested against the tendency for that dyad to appear together in the same subgroup. In neither males nor females, however, did association and relatedness correlate significantly. In fact, only one of the dyads (Fig and Flower) that had both a high

R-value and a high index of association made sense to me when I saw the results. In 2010, a group of young females that I considered to be members of an age cohort disappeared and are assumed to have emigrated. Fig is the only member of that cohort that did not leave, and I understood this to be because of her very strong association with Flower, whom I assumed was Fig’s mother. Otherwise, apparently closely related females are not disproportionately associating with each other, and a few of the dyads with 0.5 R-values were a surprise to me, meaning that I had not perceived them to be a social “pair”. In contrast, Frugivory and Forget had a very high association index and an R-value of zero.

Another possibility, one that I was not able to investigate with my data, is that association between females is a function of geography, or location. If, as Shimooka et al.

(2008) suggested, female spider monkeys tend to range within smaller, overlapping core 97

areas or ‘neighborhoods,’ subgroup association may be a by-product of this. This is somewhat consistent with my impressions in the field, however I was not able to test this because my association index and the location in which the females were seen were basically the same thing. I have no measure of female range use that is independent of my observations of the subgroups and their membership. The finding that female subgroups are more stable in membership, with less frequent changes in membership than either of the other two subgroup types could be a function of association based on proximity to

“home”.

My association index was a measure of the likelihood of two females being in the same subgroup, however the extent to which they are “associating” as a result of being in the same subgroup is worth questioning. I used membership in the same subgroup rather than more active measure of affiliation (what Ramos-Fernández et al. 2009 call “active companionship”), such as approaching, grooming, and sitting in body contact, because these behaviors are very rare among females, and in most of the dyads did not occur, at all, over the course of the study. The absence of directly affiliative behaviors between females when they are in the same subgroup leaves open the possibility that females are simply distributing themselves in relation to, or “mapping on to”, the food supply, and apparent subgroup association is an incidental by-product of this. Perhaps the females just tolerate each other’s proximity, for short periods of time, under some circumstance. The small and temporary nature of the subgroups demonstrated in this study could suggest this. In fact, I considered the question of whether the females should even be considered to be members of a group or community, or whether they might simply be a collection of individuals 98

whose ranging is limited by a group of bonded males who use direct or indirect coercion to monopolize shared access to them.

Aggression directed by males to females is fairly common at Runaway Creek and may be a reproductive strategy of bonded males in response to high fission-fusion dynamics among females. Female-directed aggression involves aggressive chasing, open mouth threats and physical altercations, and it causes considerable distress to females, even though they are generally not visibly injured (Link et al. 2009; personal observation). A similar pattern has been described for fission-fusion dolphins and chimpanzees (Connor &

Vollmer 2009). Female directed aggression from males could function as a male strategy for assessing female reproductive status by inducing the release of pheromones via urinary and fecal excretion during targeted attacks (Symington 1987), or it may be a function of direct (Smuts & Smuts 1993) or indirect (Link et al. 2009) sexual coercion through cooperative social control of group females by resident males.

Mixed-sex subgroups were more common than all-male subgroups - roughly 30% of subgroups are mixed-sex compared to all-male at 10%. One reason for this may be that male subgroups were notoriously difficult to find and follow, and the majority of my time was spent with the more common and more accessible female subgroups. The majority of the times that mixed-sex subgroups occurred was when I was collecting data on an all- female subgroup and a small subgroup of males would come upon them. These subgroups were likely to change membership in less than 30 minutes as the males did not usually stay long. They typically create a disruption by directing aggression against the females (as

described above), which the females appeared to anticipate. In an earlier analysis (Hartwell et al. 2012) of patterns of aggression at Runaway Creek, and based on my familiarity with the individuals, I came to know certain adult male-female pairs that were typically involved in friendly rather that aggressive interactions when a subgroup of males came upon a subgroup of females. The later genetic analysis (presented in this thesis) confirmed what I suspected: these were probably adult son-mother pairs.

I have been asked if, based on my study, I think that all females in the study group even “know” all other females in the group. From a social network analysis (Hartwell et al. 2014b) that is not included in this thesis, I do know that all possible female dyads were observed in the same subgroup at least once over the course of the study. And although the entire spider monkey study group was never observed all together at the same time, I do have a sense that the group females are members of a “community”. During my first year of research at Runaway Creek, I learned what constituted the study social group

(versus the neighboring group) by identifying individual monkeys and slowly piecing together the social network by linking individual members together based on who was seen with whom. After six to seven months, I eventually saw every combination of individuals together in a subgroup at least once. And the members of this study group (F group) were never observed to associate with any members of the neighbouring G group, whose members I also know. With the exception of immigration or emigration of subadult females, I have never observed a female to cross over into G group’s range. Over the course of this study, three subadult females have disappeared and are assumed to have emigrated, while three others (previously unknown) randomly appeared one day and then 100

never left (all three have since sired offspring with intra-group males). I have never seen resident females with anyone outside the study group other than these three subadult females when they were new immigrants. And even then, the new females were not fully

“accepted” by the longer-tenured resident females until they sired their first infant two- three years later. By accepted, I mean allowed in close spatial proximity and tolerated rather than being chased out of fruiting trees.

My subjective impression is that bonds among some females with high association indices might in part be explained by their overlapping nutritional and energetic requirements, particularly when they have offspring of a similar age. In addition, it is possible that these similarly-aged immatures form “friendships” with each other that might have an influence on who their mothers associate with. Indeed, one of the female dyads with the highest association index (Frugivory and Forget) gave birth to infants within the same week. In the field I came to regard some of the subgroup associations of adult females as “play dates” for their offspring. Adult females might forage more efficiently when their offspring are occupied playing rather than clinging to their mothers. Although the females in a subgroup rarely display outright affiliation towards one another, I regularly observed the juveniles playing together. This possibility, although speculative at this stage, warrants further study.

Individuals traveling together suggests a shared goal or agenda that cannot be explained simply by meeting up in same tree by chance, or being lead together by their offspring. Once I observed a subgroup containing all 12 female members of the study

101

group. They (plus their immature offspring = 26 individuals in total) traveled together as one large, cohesive subgroup and traveled almost the full length of their range without stopping until they reached a large cave near the border to a neighboring group. For the next hour the females scent-marked tree branches (from pectoral glands on chest) and fed on aerial roots and soil on top of the cave. Eventually the females started to disperse and go their separate ways, but the observation of them traveling together until they reached the cave suggests that the females had a shared goal.

Hurricane Richard provided another opportunity, I believe, to observe the adaptive flexibility in female social relationships (association patterns), as well as evidence that the study group females are members of a meaningful larger social group. Female spider monkeys exhibit the social flexibility to come together under certain circumstances and to remain apart for very long periods of time. The degree of gregariousness among intra-group females can be remarkably variable over time. For example, 26% of female-female dyads were never observed together in a subgroup for two years following Hurricane Richard

(Hartwell et al. 2014b). Network analysis measures revealed that mean strength and eigenvector centrality (measures of gregariousness and ‘connectedness’) among female dyads decreased significantly post-hurricane. In contrast, male eigenvector centrality increased post-hurricane, suggesting that male relationships played a key role in the network’s structure after the hurricane by linking individuals together, including females that did not otherwise associate. After two years, however, all possible combinations of female dyads were once again seen together.

102

The overall impression that I derive from my study is that the underlying causes of spider monkey subgrouping patterns are complex, and are likely determined by a multitude of factors. Overall fruit availability appears to exert only a moderate effect on subgroup size and stability that I measured here, and relatedness does not appear to fully explain observed patterns of association in males or females. It is possible that other aspects of food sources, such as patch size, density, and distribution, have more powerful effects on subgrouping patterns, and future studies should include consideration of these variables.

Future studies should also include finer-grained analyses of patterns of active affiliation between specific individuals to determine the role that social relationships might play in structuring subgroup membership. Finally, there is no doubt that spider monkey males and females experience different ecological and social pressures that influence their behaviour with respect to if, when and for how long they form and remain in subgroups, and future studies should address ways of identifying exactly how the socio-ecology of males and females differ, and how they might be conceptually integrated to better understand fission- fusion dynamics in this species.

103

References

Ahumada, J., Stevenson, P., & Quinones, M. (1998). Ecological response of spider

monkeys to temporal variation in fruit abundance: The importance of flooded forest

as a keystone habitat. Primate Conservation, 18, 10-14.

Altringham, J. D., & Senior, P. (2005). Social systems and ecology of bats. In K. E.

Ruckstuhl, & P. Neuhaus (Eds.), Sexual segregation in vertebrates: Ecology of the

two sexes (pp. 303-326). New York: Cambridge University Press.

Anderson, D. P., Nordheim, E. V., Boesch, C., & Moermond, T. (2002). Factors

influencing fission-fusion grouping in chimpanzees in the Taï National Park, Côte

d'Ivoire. Behavioural diversity in chimpanzees and bonobos (pp. 20-101).

Cambridge: Cambridge University Press.

Archie, E. A., Moss, C. J., & Alberts, S. C. (2006). The ties that bind: Genetic relatedness

predicts the fission and fusion of social groups in wild African elephants.

Proceedings of the Royal Society of London, B., 273, 513-522.

Archie, E. A., Moss, C. J., & Alberts, S. C. (2011). Friends and relations: Kinship and the

nature of female elephant social relationships. In C.J. Moss, H. Croze, & P.C. Lee

(Eds.), The Amboseli elephants: A long-term perspective on a long-lived mammal

(pp. 238-245). Chicago: The University of Chicago Press.

104

Asensio, N., Korstjens, A. H., Schaffner, C. M., & Aureli, F. (2008). Intragroup aggression,

fission-fusion dynamics and feeding competition in spider monkeys. Behaviour,

145(7), 983-1001.

Asensio, N., Korstjens, A. H., & Aureli, F. (2009). Fissioning minimizes ranging costs in

spider monkeys: A multiple-level approach. Behavioral Ecology and Sociobiology,

63(5), 649-659.

Aureli, F., Schaffner, C. M., Verpooten, J., Slater, K., & Ramos-Fernández, G. (2006).

Raiding parties of male spider monkeys: Insights into human warfare? American

Journal of Physical Anthropology, 131, 486-497.

Aureli, F., & Schaffner, C. M. (2007). Aggression and conflict management at fusion in

spider monkeys. Biology Letters, 3(2), 147-149.

Aureli, F., & Schaffner, C. M. (2008). Social interactions, social relationships and the

social system of spider monkeys. In C. J. Campbell (Ed.), Spider monkeys:

Behavior, ecology and evolution of the genus Ateles (pp. 236-265). New York:

Cambridge University Press.

Aureli, F., Schaffner, C. M., Boesch, C., Bearder, S. K., Call, J., Chapman, C. A., . . .

Henzi, S. P. (2008). Fission-fusion dynamics: New research frameworks. Current

Anthropology, 49(4), 627-654.

105

Aureli, F., Schaffner, C. M., Asensio, N., & Lusseau, D. (2012). What is a subgroup? How

socioecological factors influence inter-individual distance. Behavioral Ecology,

ars122.

Aureli, F., Di Fiore, A., Murillo-Chacon, E., Kawamura, S., & Schaffner, C. M. (2013).

Male philopatry in spider monkeys revisited. American Journal of Physical

Anthropology, 152(1), 86-95.

Basabose, A. K. (2004). Fruit availability and chimpanzee party size at Kahuzi Montane

forest, Democratic Republic of Congo. Primates, 45(4), 211-219.

Bearder, S. K. (1999). Physical and social diversity among nocturnal primates: A new view

based on long term research. Primates, 40, 267-282.

Boesch, C. (1991). The effects of leopard predation on grouping patterns in forest

chimpanzees. Behaviour, 117(3-4), 220-242.

Boesch, C. (1996). Social grouping in Tai chimpanzees. Great ape societies (pp. 101-113).

Cambridge: Cambridge University Press.

Boesch, C., & Boesch-Achermann, H. (2000). The chimpanzees of the Tai forest:

Behavioural ecology and evolution. New York: Oxford University Press.

Boesch, C., Hohmann, G., & Marchant, L. F. (2002). Behavioural diversity in chimpanzees

and bonobos. New York: Cambridge University Press.

106

Boesch, C., Kohou, G., Néné, H., & Vigilant, L. (2006). Male competition and paternity in

wild chimpanzees of the Taï forest. American Journal of Physical Anthropology,

130(1), 103-115.

Campbell, C. J. (2003). Female-directed aggression in free-ranging Ateles geoffroyi.

International Journal of Primatology, 24(2), 223-237.

Campbell, C. J. (2006). Lethal intragroup aggression by adult male spider monkeys (Ateles

geoffroyi). American Journal of Primatology, 68(12), 1197-1201.

Campbell, C. J., & Gibson, K. (2008). Spider monkey reproduction and sexual behavior.

In C. J. Campbell (Ed.), Spider monkeys: Behavior, ecology, and evolution of the

genus Ateles (pp. 266-287). Cambridge: Cambridge University Press.

Carter, K. D., Seddon, J. M., Frère, C. H., Carter, J. K., & Goldizen, A. W. (2013). Fission-

fusion dynamics in wild giraffes may be driven by kinship, spatial overlap and

individual social preferences. Animal Behaviour, 85(2), 385-394.

Castellanos, H. G., & Chanin, P. (1996). Seasonal differences in food choice and patch

preference of long-haired spider monkeys (Ateles belzebuth). In M. Norconk, A.L.

Rosenberger, & P.A. Gerber (Eds.), Adaptive radiations of Neotropical primates

(pp. 451-466). New York: Plenum Press.

107

Champion, J. (2013). The Effects of a Hurricane and Fire On Feeding Ecology, Activity

Budget, And Social Patterns of Spider Monkeys (Ateles geoffroyi) in Central Belize

(MA Thesis). University of Calgary, Calgary.

Chapman, C. A. (1988). Patch use and patch depletion by the spider and howling monkeys

of Santa Rosa National Park, Costa Rica. Behaviour, 105(1), 99-116.

Chapman, C. A. (1990a). Association patterns of spider monkeys: The influence of ecology

and sex on social organization. Behavioral Ecology and Sociobiology, 26, 409-414.

Chapman, C. A. (1990b). Ecological constraints on group size in three species of

Neotropical primates. Folia Primatologica, 55(1), 1-9.

Chapman, C. A., Chapman, L. J., Wrangham, R., Hunt, K., Gebo, D., & Gardner, L. (1992).

Estimators of fruit abundance of tropical trees. Biotropica, 24(4), 527-531.

Chapman, C. A., Wrangham, R. W., & Chapman, L. J. (1995). Ecological constraints on

group size: An analysis of spider monkey and chimpanzee subgroups. Behavioral

Ecology and Sociobiology, 36(1), 59-70.

Chapman, C. A., & Chapman, L. J. (2000). Determinants of group size in primates: The

importance of travel costs. In S. Boinski & P.A. Garber (Eds.), On the move: How

and why animals travel in groups (pp. 24-42). Chicago: Chicago University Press.

108

Chapman, C. A., & Rothman, J. M. (2009). Within-species differences in primate social

structure: Evolution of plasticity and phylogenetic constraints. Primates, 50(1), 12-

22.

Chávez, O. M., Stoner, K. E., & Arroyo-Rodríguez, V. (2012). Differences in diet between

spider monkey groups living in forest fragments and continuous forest in Mexico.

Biotropica, 44(1), 105-113.

Clutton-Brock, T. H. (1989). Review lecture: Mammalian mating systems. Proceedings of

the Royal Society of London B: Biological Sciences, 236(1285), 339-372.

Coles, R. C., Lee, P. C., & Talebi, M. (2012). Fission-fusion dynamics in southern muriquis

(Brachyteles arachnoides) in continuous Brazilian Atlantic Forest. International

Journal of Primatology, 33, 93-114.

Connor, R. C., Wells, R. S., Mann, J., & Read, A. J. (2000). The bottlenose dolphin: Social

relationships in a fission-fusion society. In J. Mann, R. C. Connor, P. L. Tyack &

H. Whitehead (Eds.), Cetacean societies: Field studies of dolphins and whales (pp.

91-125). Chicago: Chicago University Press.

Connor, R. C., Smolker, R., & Bejder, L. (2006). Synchrony, social behaviour and alliance

affiliation in Indian Ocean bottlenose dolphins, Tursiops aduncus. Animal

Behaviour, 72(6), 1371-1378.

109

Connor, R. C., & Vollmer, N. (2009). Sexual coercion in dolphin consortships: A

comparison with chimpanzees. In M.N. Muller & R.W. Wrangham (Eds.), Sexual

coercion in primates: An evolutionary perspective on male aggression against

females (pp. 218-243). Cambridge: Harvard University Press.

Conradt, L., & Roper, T. J. (2000). Activity synchrony and social cohesion: A fission-

fusion model. Proceedings of the Royal Society of London B: Biological Sciences,

267, 2213-2218.

Dew, J. L. (2005). Foraging, food choice, and food processing by sympatric ripe-fruit

specialists: Lagothrix lagotricha poeppigii and Ateles belzebuth belzebuth.

International Journal of Primatology, 26(5), 1107-1135.

Di Fiore, A. (2003). Molecular genetic approaches to the study of primate behavior, social

organization, and reproduction. American Journal of Physical Anthropology,

122(S37), 62-99.

Di Fiore, A., & Fleischer, R. C. (2005). Social behavior, reproductive strategies, and

population genetic structure of Lagothrix poeppigii. International Journal of

Primatology, 26(5), 1137-1173.

Di Fiore, A., Link, A., & Dew, J. (2008). Diets of wild spider monkeys. In C. J. Campbell,

(Ed.), Spider monkeys: Behavior, ecology and evolution of the genus Ateles (pp.

81-137). New York: Cambridge University Press.

110

Di Fiore, A., Link, A., Spehar, S. N., & Schmitt, C. A. (2009). Dispersal patterns in

sympatric woolly and spider monkeys: Integrating molecular and observational

data. Behaviour, 146(4-5), 437-470.

Dias, L.G., & Strier, K.B. (2003). Effects of group size on ranging patterns in Brachyteles

arachnoides hypoxanthus. International Journal of Primatology, 24(2), 209-221.

Dietz, E. J. (1983). Permutation tests for association between two distance matrices.

Systematic Biology, 32(1), 21-26.

Dolado, R., Cooke, C., & Beltran, F. S. (2016). How many for lunch today? Seasonal

fission-fusion dynamics as a feeding strategy in wild red-capped mangabeys

(Cercocebus torquatus). Folia Primatologica, 87(3), 197-212. doi:000449220

Dunbar, R. I. M. (1988). Primate social systems. Ithaca: Cornell University Press.

Eberle, M., & Kappeler, P.M. (2002). Mouse lemurs in space and time: A test of the

socioecological model. Behavioural Ecology and Sociobiology, 51(2), 131-139.

Edwards, A. (1972). Likelihood. an account of the statistical concept of likelihood and its

application to scientific inference. London-New York: Cambridge University

Press.

Evans, K.E., Pavelka, M.S.M., Hartwell, K.S., & Notman, H. (2012). Do adult male spider

monkeys (Ateles geoffroyi) preferentially handle male infants? International

Journal of Primatology, 33(4), 799-808.

111

Favre, L., Balloux, F., Goudet, J., & Perrin, N. (1997). Female-biased dispersal in the

monogamous mammal Crocidura russula: Evidence from field data and

microsatellite patterns. Proceedings of the Royal Society of London B: Biological

Sciences, 264(1378), 127-132. doi:10.1098/rspb.1997.0019

Fedigan, L. M. (1992). Primate paradigms: Sex roles and social bonds. Chicago:

University of Chicago Press.

Fedigan, L. M., & Baxter, M. J. (1984). Sex differences and social organization in free-

ranging spider monkeys (Ateles geoffroyi). Primates, 25(3), 279-294.

Furuichi, T. (2009). Factors underlying party size differences between chimpanzees and

bonobos: A review and hypotheses for future study. Primates, 50, 197-209.

Fury, C. A., Ruckstuhl, K. E., & Harrison, P. L. (2013). Spatial and social sexual

segregation patterns in indo-pacific bottlenose dolphins (Tursiops aduncus). PloS

One, 8(1), e52987.

Ghiglieri, M. P. (1984). The chimpanzees of Kibale forest: A field study of ecology and

social structure. New York: Columbia University Press.

Gilby, I. C., & Wrangham, R. W. (2008). Association patterns among wild chimpanzees

(Pan troglodytes schweinfurthii) reflect sex differences in cooperation. Behavioral

Ecology and Sociobiology, 62(11), 1831-1842.

112

Ginsberg, J. R., & Young, T. P. (1992). Measuring association between individuals or

groups in behavioural studies. Animal Behaviour, 44, 377-379.

Goldberg, T. L., & Wrangham, R. W. (1997). Genetic correlates of social behaviour in

wild chimpanzees: Evidence from mitochondrial DNA. Animal Behaviour, 54(3),

559-570.

González-Zamora, A., Arroyo-Rodríguez, V., Chaves, Ó M., Sánchez-López, S., Stoner,

K. E., & Riba-Hernández, P. (2009). Diet of spider monkeys (Ateles geoffroyi) in

Mesoamerica: Current knowledge and future directions. American Journal of

Primatology, 71(1), 8-20.

Goodall, J. (1986). The chimpanzees of Gombe: Patterns of behavior. Cambridge: Harvard

University Press.

Guilhem, C., Bideau, E., Gerard, J., & Maublanc, M. (2000). Agonistic and proximity

patterns in enclosed mouflon (Ovis gmelini) ewes in relation to age, reproductive

status and kinship. Behavioural Processes, 50(2), 101-112.

Hamilton, W.D. (1963). The evolution of altruistic behavior. The American Naturalist,

97(896), 354-356.

Hamilton, W.D. (1964). The genetical evolution of social behaviour. Journal of

Theoretical Biology, 7(1), 1-16.

113

Hartwell, K.S., Notman, H., & Pavelka, M.S.M. (2012). Patterns of aggression in spider

monkeys (Ateles geoffroyi yucatanensis) at Runway Creek Nature Reserve, Belize

[Abstract]. Presentation at the XXIV Congress of the International Primatological

Society, 12-17 August 2012 in Cancun, Mexico.

Hartwell, K. S., Notman, H., Bonenfant, C., & Pavelka, M. S. (2014a). Assessing the

occurrence of sexual segregation in spider monkeys (Ateles geoffroyi

yucatanensis), its mechanisms and function. International Journal of Primatology,

35(2), 425-444.

Hartwell, K. S., Champion, J. E., Notman, H., & Pavelka, M. S. (2014b). Using social

network analysis to study the effects of a hurricane on association patterns in spider

monkeys (Ateles geoffroyi) in Belize [Abstract]. American Journal of Physical

Anthropology, Suppl 153, 137-137.

Hashimoto, C., Furuichi, T., & Tashiro, Y. (2001). What factors affect the size of

chimpanzee parties in the Kalinzu Forest, Uganda? Examination of fruit abundance

and number of estrous females. International Journal of Primatology, 22(6), 947-

959.

Hashimoto, C., Suzuki, S., Takenoshita, Y., Yamagiwa, J., Basabose, A.K.& Furuichi, T.

(2003). How fruit abundance affects the chimpanzee party size: A comparison

between four study sites. Primates, 44, 77-81.

114

Heithaus, M. R., & Dill, L. M. (2002). Food availability and tiger shark predation risk

influence bottlenose dolphin habitat use. Ecology, 83(2), 480-491.

Hohmann, G. (2001). Association and social interactions between strangers and residents

in bonobos (Pan paniscus). Primates, 42(1), 91-99.

Hohmann, G., & Fruth, B. (2002). Dynamics in social organization of bonobos (Pan

paniscus). In C. Boesch, G. Hohmann & L. F. Marchant (Eds.), Behavioural

diversity in chimpanzees and bonobos (pp. 138-150). Cambridge: Cambridge

University Press.

Hohmann, G., & Fruth, B. (2003). Culture in bonobos? Between-species and within-

species variation in behavior. Current Anthropology, 44(4), 563-571.

Holekamp, K.E., Cooper, S.M., Katona, C.I., Berry, N.A., Frank, L.G., & Smale, L. (1997).

Patterns of association among female spotted hyenas (Crocuta crocuta). Journal of

Mammalogy, 78(1), 55-64.

Holmes, S. M., Gordon, A. D., Louis, E. E., & Johnson, S. E. (2016). Fission-fusion

dynamics in black-and-white ruffed lemurs may facilitate both feeding strategies

and communal care of infants in a spatially and temporally variable environment.

Behavioral Ecology and Sociobiology, 70(11), 1949-1960.

115

Inoue, E., Inoue-Murayama, M., Vigilant, L., Takenaka, O., & Nishida, T. (2008).

Relatedness in wild chimpanzees: Influence of paternity, male philopatry, and

demographic factors. American Journal of Physical Anthropology, 137(3), 256-

262.

Itoh, N., & Nishida, T. (2007). Chimpanzee grouping patterns and food availability in

Mahale Mountains National Park, Tanzania. Primates, 48(2), 87-96.

IUCN. (2015). IUCN Red List of Threatened Species. www.iucnredlist.org. Accessed

August 24, 2016.

Jones, C., & Sabater Pi, J. (1968). Comparative ecology of Cercocebus albigena (gray) and

Cercocebus torquatus (kerr) in Rio Muni, West Africa. Folia Primatologica, 9(2),

99-113.

Kahlenberg, S. M., Thompson, M. E., Muller, M. N., & Wrangham, R. W. (2008).

Immigration costs for female chimpanzees and male protection as an immigrant

counterstrategy to intrasexual aggression. Animal Behaviour, 76(5), 1497-1509.

Kalinowski, S. T., Wagner, A. P., & Taper, M. L. (2006). ML-RELATE: A computer

program for maximum likelihood estimation of relatedness and relationship.

Molecular Ecology Notes, 6(2), 576-579.

116

Kalinowski, S. T., Taper, M. L., & Marshall, T. C. (2007). Revising how the computer

program CERVUS accommodates genotyping error increases success in paternity

assignment. Molecular Ecology, 16(5), 1099-1106.

Kano, T. (1992). The last ape: Pygmy chimpanzee behavior and ecology. Stanford, C.A.:

Stanford University Press.

Kapsalis, E. (2004). Matrilineal kinship and primate behavior. In B. Chapais & C. M.

Berman (Eds.), Kinship and behavior in primates (pp. 153-176). New York: Oxford

University Press.

Kerth, G., & König, B. (1999). Fission, fusion and nonrandom association in female

Bechstein's bats (Myotis bechsteinii). Behaviour, 136(9), 1187-1202.

Kinzey, W. G., & Cunningham, E. P. (1994). Variability in Platyrrhine social organization.

American Journal of Primatology, 34(2), 185-198.

Klein, L. L., & Klein, D. B. (1977). Feeding behaviour of the Colombian spider monkey

Ateles belzebuth. In T. H. Clutton-Brock (Ed.), Primate ecology: Studies of feeding

and ranging behaviour in lemurs, monkeys, and apes (pp. 153-181). London:

Academic Press.

Korstjens, A. H., Verhoeckx, I. L., & Dunbar, R. I. (2006). Time as a constraint on group

size in spider monkeys. Behavioral Ecology and Sociobiology, 60(5), 683-694.

117

Korstjens, A. H., Bergmann, K., Deffernez, C., Krebs, M., Nijssen, E. C., van Oirschot, B.

A. M., ... & Schippers, E. P. (2007). How small-scale differences in food

competition lead to different social systems in three closely related sympatric

Colobines. Cambridge Studies in Biological and Evolutionary Anthropology,

1(51), 72-108.

Kummer, H. (1968). Social organization of Hamadryas baboons (Vol. 765). Chicago:

University of Chicago Press.

Kummer, H. (1971). Primate societies: Group techniques of ecological adaptation.

Chicago: Aldine.

Kuroda, S. (1979). Grouping of the pygmy chimpanzees. Primates, 20(2), 161-183.

Langergraber, K.E., Mitani, J.C., & Vigilant, L. (2007). The limited impact of kinship on

cooperation in wild chimpanzees. Proceedings of the National Academy of the

Sciences of the USA, 104(19), 7786-7790.

Langergraber, K., Mitani, J., & Vigilant, L. (2009). Kinship and social bonds in female

chimpanzees (Pan troglodytes). American Journal of Primatology, 71(10), 840-

851.

Lehmann, J., & Boesch, C. (2003). Social influences on ranging patterns among

chimpanzees (Pan troglodytes verus) in the Tai National Park, Cote d'Ivoire.

Behavioral Ecology, 14(5), 642-649.

118

Lehmann, J., & Boesch, C. (2004). To fission or to fusion: Effects of community size on

wild chimpanzee (Pan troglodytes verus) social organisation. Behavioral Ecology

and Sociobiology, 56, 207-216.

Lehmann, J., & Boesch, C. (2008). Sexual differences in chimpanzee sociality.

International Journal of Primatology, 29(1), 65-81.

Lehmann, J., & Boesch, C. (2009). Sociality of the dispersing sex: The nature of social

bonds in West African female chimpanzees, Pan troglodytes. Animal Behaviour,

77(2), 377-387.

Lehmann, J., Korstjens, A. H., & Dunbar, R. (2007). Fission-fusion social systems as a

strategy for coping with ecological constraints: A primate case. Evolutionary

Ecology, 21(5), 613-634.

Leighton, M., & Leighton, D. R. (1982). The relationship of size of feeding aggregate to

size of food patch: Howler monkeys (Alouatta palliata) feeding in Trichilia cipo

fruit trees on Barro Colorado Island. Biotropica, 14(2), 81-90.

Link, A., Di Fiore, A., & Spehar, S. N. (2009). Female directed aggression and social

control in spider monkeys. In M. N. Muller, & R. W. Wrangham (Eds.), Sexual

coercion in primates and humans: An evolutionary perspective on male aggression

against females (pp. 157-183). Cambridge: Harvard University Press.

119

Lukas, D., Reynolds, V., Boesch, C., & Vigilant, L. (2005). To what extent does living in

a group mean living with kin? Molecular Ecology, 14(7), 2181-2196.

Lusseau, D. (2007). Evidence for social role in a dolphin social network. Evolutionary

Ecology, 21(28), 357-366.

Lynch Alfaro, J. W. (2007). Subgrouping patterns in a group of wild Cebus apella nigritus.

International Journal of Primatology, 28(2), 271-289.

Mantel, N. (1967). The detection of disease clustering and a generalized regression

approach. Cancer Research, 27(2), 209-220.

Marlowe, F. W. (2005). Hunter-gatherers and human evolution. Evolutionary

Anthropology, 14, 54-67.

Matsumoto-Oda, A., Hosaka, K., Huffman, M. A., & Kawanaka, K. (1998). Factors

affecting party size in chimpanzees of the Mahale mountains. International Journal

of Primatology, 19(6), 999-1011.

Meerman, J. C. (1999). Rapid ecological assessment of Runaway Creek Belize. Zoological

Society of Milwaukee.

Milligan, B. G. (2003). Maximum-likelihood estimation of relatedness. Genetics, 163(3),

1153-1167.

120

Mitani, M. (1989). Cercocebus torquatus: Adaptive feeding and ranging behaviors related

to seasonal fluctuations of food resources in the tropical rain forest of south-western

Cameroon. Primates, 30(3), 307-323.

Mitani, J. C., Merriwether, D. A., & Zhang, C. (2000). Male affiliation, cooperation and

kinship in wild chimpanzees. Animal Behaviour, 59(4), 885-893.

Mitani, J. C., Watts, D. P., & Lwanga, J. S. (2002). Ecological and social correlates of

chimpanzee party size and composition. In C. Boesch, G. Hohmann & L. F.

Marchant (Eds.), Behavioural diversity in chimpanzees and bonobos (pp. 102-111).

Cambridge: Cambridge University Press.

Morin, P.A., Moore, J.J., Chakraborty, R., Jin, L., Goodall, J., & Woodruff, D.S. (1994).

Kin selection, social structure, gene flow, and the evolution of chimpanzees.

Science, 265(5176), 1193-1201.

Muller, M. N. (2002). Agonistic relations among Kanyawara chimpanzees. In C. Boesch,

G. Hohmann & L. F. Marchant (Eds.), Behavioural diversity in chimpanzees and

bonobos (pp. 112-124). Cambridge: Cambridge University Press.

Muller, M.N., Thompson, M. E., & Wrangham, R.W. (2006). Male chimpanzees prefer

mating with old females. Current Biology, 16(22), 2234-2238.

121

Murray, C. M., Mane, S. V., & Pusey, A. E. (2007). Dominance rank influences female

space use in wild chimpanzees, Pan troglodytes: Towards an ideal despotic

distribution. Animal Behaviour, 74(6), 1795-1804.

Nei, M. (1978). Estimation of average heterozygosity and genetic distance from a small

number of individuals. Genetics, 89(3), 583-590.

Newton-Fisher, N. E. (1999). Association by male chimpanzees: A social tactic?

Behaviour, 136(6), 705-730.

Newton-Fisher, N. E., Reynolds, V., & Plumptre, A. J. (2000). Food supply and

chimpanzee (Pan troglodytes schweinfurthii) party size in the Budongo Forest

Reserve, Uganda. International Journal of Primatology, 21(4), 613-628.

Nishida, T., & Hiraiwa-Hasegawa, M. (1987). Chimpanzees and bonobos: Cooperative

relationships among males. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W.

Wrangham & T. Struhsacker (Eds.), Primate societies (pp. 165-177). Chicago:

University of Chicago Press.

Nonacs, P. (2000). Measuring and using skew in the study of social behavior and evolution.

The American Naturalist, 156(6), 577-589.

Paetkau, D., Calvert, W., Stirling, I., & Strobeck, C. (1995). Microsatellite analysis of

population structure in Canadian polar bears. Molecular Ecology, 4(3), 347-354.

122

Patriquin, K. J., & Ratcliffe, J. M. (2016). Should I stay or should I go? Fission-fusion

dynamics in bats. Sociality in bats (pp. 65-103). New York: Springer.

Pavelka, M. S. M. (2011). Mechanisms of cohesion in black howler monkeys. In R. W.

Sussman, & C. R. Cloninger (Eds.), Origins of altruism and cooperation (pp. 167-

178). New York: Springer.

Peakall, R., & Smouse, P. E. (2006). GENALEX 6: Genetic analysis in excel. Population

genetic software for teaching and research. Molecular Ecology Notes, 6(1), 288-

295.

Pearson, H. (2009). Influences on dusky dolphin (Lagenorhynchus obscurus) fission-

fusion dynamics in Admiralty Bay, New Zealand. Behavioral Ecology and

Sociobiology, 63, 1437-1446.

Pepper, J. W., Mitani, J. C., & Watts, D. P. (1999). General gregariousness and specific

social preferences among wild chimpanzees. International Journal of Primatology,

20, 613-632.

Peters, R., Cloutier, S., Dube, D., Evans, A., Hastings, P., Kaiser, H., . . . Sarwer-Foner, B.

(1988). The allometry of the weight of fruit on trees and shrubs in Barbados.

Oecologia, 74(4), 612-616.

Pusey, A.E., Williams, J., & Goodall, J. (1997). The influence of dominance rank on the

reproductive success of female chimpanzees. Science, 277(5327), 828-831.

123

Radespiel, U., Sarikaya, Z., Zimmermann, E., & Bruford, M.W. (2001). Sociogenetic

structure in a free-living nocturnal primate population: Sex-specific differences in

the grey mouse lemur (Microcebus murinus). Behavioural Ecology and

Sociobiology, 50(6), 493-502.

Ramos-Fernández, G. (2005). Vocal communication in a fission-fusion society: Do spider

monkeys stay in touch with close associates? International Journal of Primatology,

26(5), 1077-1092.

Ramos-Fernández, G., Boyer, D., Aureli, F., & Vick, L. G. (2009). Association networks

in spider monkeys (Ateles geoffroyi). Behavioral Ecology and Sociobiology, 63,

999-1013.

Range, F. (2006). Social behavior of free-ranging juvenile sooty mangabeys (Cercocebus

torquatus atys). Behavioral Ecology and Sociobiology, 59(4), 511-520.

Rebecchini, L., Schaffner, C. M., & Aureli, F. (2011). Risk is a component of social

relationships in spider monkeys. Ethology, 117(8), 691-699.

Rimbach, R., Link, A., Montes-Rojas, A., Di Fiore, A., Heistermann, M., & Heymann, E.

W. (2014). Behavioral and physiological responses to fruit availability of spider

monkeys ranging in a small forest fragment. American Journal of Primatology,

76(11), 1049-1061.

124

Rodseth, L., Wrangham, R. W., Harrigan, A. M., & Smuts, B. B. (1991). The human

community as a primate society. Current Anthropology, 32, 221-254.

Rubenstein, D. I., Sundaresan, S. R., Fischhoff, I. R., Tantipathananandh, C., & Berger-

Wolf, T. Y. (2015). Similar but different: Dynamic social network analysis

highlights fundamental differences between the fission-fusion societies of two

equid species, the onager and Grevy's zebra. PloS One, 10(10), e0138645.

Ruckstuhl, K. E. (1999). To synchronise or not to synchronise: A dilemma for young

bighorn males? Behaviour, 136(6), 805-818.

Ruckstuhl, K. E. (2007). Sexual segregation in vertebrates: Proximate and ultimate causes.

Integrative and Comparative Biology, 47(2), 245-257.

Ruckstuhl, K. E., & Neuhaus, P. (2005). Sexual segregation in vertebrates. Cambridge

University Press.

Schaffner, C. M., Rebecchini, L., Ramos-Fernández, G., Vick, L. G., & Aureli, F. (2012).

Spider monkeys (Ateles geoffroyi yucatanensis) cope with the negative

consequences of hurricanes through changes in diet, activity budget, and fission-

fusion dynamics. International Journal of Primatology, 33(4), 922-936.

Schnell, G. D., Watt, D. J., & Douglas, M. E. (1985). Statistical comparison of proximity

matrices: Applications in animal behaviour. Animal Behaviour, 33(1), 239-253.

125

Schreier, A. L., & Swedell, L. (2009). The fourth level of social structure in a multi-level

society: Ecological and social functions of clans in hamadryas baboons. American

Journal of Primatology, 71, 948-955.

Shimooka, Y. (2003). Seasonal variation in association patterns of wild spider monkeys

(Ateles belzebuth belzebuth) at La Macarena, Colombia. Primates, 44(2), 83-90.

Shimooka, Y. (2005). Sexual differences in ranging of Ateles belzebuth belzebuth at La

Macarena, Colombia. International Journal of Primatology, 26(2), 385-406.

Shimooka, Y., Campbell, C., Di Fiore, A., Felton, A., Izawa, K., Link, A., . . . Wallace, R.

(2008). Demography and group composition of Ateles. In C. J. Campbell (Ed.),

Spider monkeys: Behavior, ecology and evolution of the genus Ateles (pp. 329-348).

New York: Cambridge University Press.

Silk, J. B. (2006). Practicing Hamilton's rule: Kin selection in primate groups. In P.M.

Kappeler & C.P. van Schaik (Eds.), Cooperation in primates and humans (pp. 25-

46). Heidelberg: Springer.

Slater, K. Y., Schaffner, C., & Aureli, F. (2007). Embraces for infant handling in spider

monkeys: Evidence for a biological market? Animal Behaviour, 74(3), 455-461.

Slater, K.Y., Schaffner, C.M., & Aureli, F. (2009). Sex differences in the social behavior

of wild spider monkeys (Ateles geoffroyi yucatanensis). American Journal of

Primatology, 71(1), 21-29.

126

Smith, J. E., Kolowski, J. M., Graham, K. E., Dawes, S. E., & Holekamp, K. E. (2008).

Social and ecological determinants of fission-fusion dynamics in the spotted

hyaena. Animal Behaviour, 76, 619-636.

Smith, J. E., Van Horn, R. C., Powning, K. S., Cole, A. R., Graham, K. E., Memenis, S.

K., & Holekamp, K. E. (2010). Evolutionary forces favoring intragroup coalitions

among spotted hyenas and other animals. Behavioral Ecology, 21(2), 284-303.

Smith-Aguilar, S. E., Ramos-Fernández, G., & Getz, W. M. (2016). Seasonal changes in

socio-spatial structure in a group of free-living spider monkeys (Ateles geoffroyi).

PloS One, 11(6), e0157228.

Smolker, R.A., Richards, A.F., Connor, R.C.& Pepper, J.W. (1992). Association patterns

among bottlenose dolphins in Shark Bay, western Australia. Behaviour, 128, 38-

69.

Smuts, B. B. & Smuts, R.W. (1993). Male aggression and sexual coercion of females in

nonhuman primates and other mammals: Evidence and theoretical implications.

Advances in the study of behavior, Volume 22 (pp. 1-63). San Diego: Academic

Press, Inc.

Sterck, E. H. M., Watts, D. P., & van Schaik, C. P. (1997). The evolution of female social

relationships in nonhuman primates. Behavioral Ecology and Sociobiology, 41(5),

291-309.

127

Stevenson, P. R., Quinones, M. J., & Ahumada, J. A. (2000). Influence of fruit availability

on ecological overlap among four Neotropical primates at Tinigua National Park,

Colombia. Biotropica, 32(3), 533-544.

Stokke, S., & Du Toit, J.T. (2002). Sexual segregation in habitat use by elephants in Chobe

National Park, Botswana. African Journal of Ecology, 40(4), 360-371.

Strier, K. B. (1989). Effects of patch size on feeding associations in muriquis (Brachyteles

arachnoides). Folia Primatologica, 52(1-2), 70-77.

Strier, K. B. (1994). Myth of the typical primate. American Journal of Physical

Anthropology, 37(S19), 233-271.

Strier, K.B. (2009). Seeing the forest through the seeds: Mechanisms of primate behavioral

diversity from individuals to populations and beyond. Current Anthropology, 50(2),

213-228.

Struhsaker, T. (2010). The red colobus monkeys: Variation demography behavior and

ecology of endangered species. Oxford: Oxford University Press.

Stumpf, R. (2007). Chimpanzees and bonobos: Diversity within and between species. In

C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger & S. K. Bearder (Eds.),

Primates in perspective (pp. 321-334). New York: Oxford University Press.

Sugiyama, Y. (1999). Socioecological factors of male chimpanzee migration at Bossou,

Guinea. Primates, 40(1), 61-68.

128

Sugiyama, Y., & Koman, J. (1979). Social structure and dynamics of wild chimpanzees at

Bossou, Guinea. Primates, 20(3), 323-339.

Sundaresan, S. R., Fischhoff, I. R., Dushoff, J., & Rubenstein, D. I. (2007). Network

metrics reveal differences in social organization between two fission-fusion

species, Grevy's zebra and onager. Oecologia, 151, 140-149.

Symington, M. M. (1987). Sex ratio and maternal rank in wild spider monkeys: When

daughters disperse. Behavioral Ecology and Sociobiology, 20(6), 421-425.

Symington, M. M. (1988). Demography, ranging patterns, and activity budgets of black

spider monkeys (Ateles paniscus chamek) in the Manu National Park, Peru.

American Journal of Primatology, 15(1), 45-67.

Symington, M. M. (1990). Fission-fusion social organization in Ateles and Pan.

International Journal of Primatology, 11(1), 47-61.

Taberlet, P., Griffin, S., Goossens, B., Questiau, S., Manceau, V., Escaravage, N., . . .

Bouvet, J. (1996). Reliable genotyping of samples with very low DNA quantities

using PCR. Nucleic Acids Research, 24(16), 3189-3194.

Te Boekhorst, I. J., Schürmann, C. L., & Sugardjito, J. (1990). Residential status and

seasonal movements of wild orang-utans in the Gunung Leuser Reserve (Sumatera,

Indonesia). Animal Behaviour, 39(6), 1098-1109.

129

Thompson, M. E., Kahlenberg, S. M., Gilby, I. C., & Wrangham, R. W. (2007). Core area

quality is associated with variance in reproductive success among female

chimpanzees at Kibale National Park. Animal Behavior, 73(3), 501-512.

Valero, A., Schaffner, C. M., Vick, L. G., Aureli, F., & Ramos-Fernández, G. (2006).

Intragroup lethal aggression in wild spider monkeys. American Journal of

Primatology, 68(7), 732-737. van Roosmalen, M. G. M., & Klein, L. L. (1988). The spider monkeys, genus Ateles. In R.

A. Mittermeier, A. B. Rylands, A. F. Coimbra-Filho & G. A. B. da Fonseca (Eds.),

Ecology and behaviour of Neotropical primates (2nd ed., pp. 455-537).

Washington D.C.: World Wildlife Fund. van Schaik, C.P., & Aureli, F. (2000). The natural history of valuable relationships in

primates. In F. Aureli & F.B.M. de Waal, (Eds.), Natural conflict resolution (pp.

307-333). Berkley: University of California Press.

Vick, L. G. (2008). Immaturity in spider monkeys: A risky business. In C.J. Campbell

(Ed.), Spider monkeys: Behavior, ecology, and evolution of the genus Ateles (pp.

288-328). Cambridge: Cambridge University Press.

Vigilant, L., Hofreiter, M., Siedel, H., & Boesch, C. (2001). Paternity and relatedness in

wild chimpanzee groups. Proceedings of the National Academy of Sciences of the

United States of America, 98(23), 12890-12895.

130

Wakefield, M. L. (2008). Grouping patterns and competition among female Pan

troglodytes schweinfurthii at Ngogo, Kibale National Park, Uganda. International

Journal of Primatology, 29(4), 907-929.

Wallace, R. B. (2005). Seasonal variations in diet and foraging behavior of Ateles chamek

in a southern Amazonian tropical forest. International Journal of Primatology,

26(5), 1053-1075.

Wallace, R. B. (2008a). Factors influencing spider monkey habitat use and ranging

patterns. In C.J. Campbell, (Ed.), Spider monkeys: Behavior, ecology and evolution

of the genus Ateles (pp. 138-154). New York: Cambridge University Press.

Wallace, R. B. (2008b). Towing the party line: Territoriality, risky boundaries and male

group size in spider monkey fission-fusion societies. American Journal of

Primatology, 70(3), 271-281.

Wallace, R. B. (2008c). The influence of feeding patch size and relative fruit density on

the foraging behavior of the black spider monkey Ateles chamek. Biotropica, 40(4),

501-506.

Watts, D. P. (1991). Harassment of immigrant female mountain gorillas by resident

females. Ethology, 89(2), 135-153.

131

Watts, D. P. (1994). Social relationships of immigrant and resident female mountain

gorillas, II: Relatedness, residence, and relationships between females. American

Journal of Primatology, 32(1), 13-30.

Watts, D. P. (2005). Sexual segregation in non-human primates. In K.E. Ruckstuhl & P.

Neuhaus (Eds.), Sexual segregation in vertebrates: Ecology of the two sexes (pp.

327-347). Cambridge: Cambridge University Press.

Weghorst, J. A. (2007). High population density of black-handed spider monkeys (Ateles

geoffroyi) in Costa Rican lowland wet forest. Primates, 48(2), 108-116.

White, F. J. (1992). Pygmy chimpanzee social organization: Variation with party size and

between study sites. American Journal of Primatology, 26(3), 203-214.

Whitehead, H. (2009). SOCPROG programs: Analysing animal social structures.

Behavioral Ecology and Sociobiology, 63(5), 765-778.

Wikberg, E. C., Sicotte, P., Campos, F. A., & Ting, N. (2012). Between-group variation in

female dispersal, kin composition of groups, and proximity patterns in a black-and-

white colobus monkey (Colobus vellerosus). PLoS One, 7(11), e48740.

Wikberg, E. C., Jack, K. M., Campos, F. A., Fedigan, L. M., Sato, A., Bergstrom, M. L., .

. . Kawamura, S. (2014a). The effect of male parallel dispersal on the kin

composition of groups in white-faced capuchins. Animal Behaviour, 96, 9-17.

132

Wikberg, E. C., Ting, N., & Sicotte, P. (2014b). Kinship and similarity in residency status

structure female social networks in black-and-white colobus monkeys (Colobus

vellerosus). American Journal of Physical Anthropology, 153(3), 365-376.

Wikberg, E. C., Ting, N., & Sicotte, P. (2014c). Familiarity is more important than

phenotypic similarity in shaping social relationships in a facultative female

dispersed primate, Colobus vellerosus. Behavioural Processes, 106, 27-35.

Williams, J.M., Liu, H.Y., & Pusey, A.E. (2002). Costs and benefits of grouping for female

chimpanzees at Gombe. In C. Boesch, G. Hohmann, & L.F. Marchant, (Eds.),

Behavioural diversity in chimpanzees and bonobos (pp. 192-203). New York:

Cambridge University Press.

Willis, C.K.R., & Brigham, R.M. (2004). Roost switching, roost sharing and social

cohesion: Forest-dwelling big brown bats, Eptesicus fuscus, conform to the fission-

fusion model. Animal Behaviour, 68(3), 495-505.

Wiszniewski, J., Allen, S. J., & Moller, L. M. (2009). Social cohesion in a hierarchically

structured embayment population of indo-pacific bottlenose dolphins. Animal

Behaviour, 77, 1449-1457.

Wittemyer, G., & Getz, W. M. (2005). Hierarchical dominance structure and social

organization in African elephants, Loxodonta Africana. Animal Behaviour, 73(4),

671-681.

133

Wittemyer, G., Douglas-Hamilton, I., & Getz, W.M. (2005). The socioecology of

elephants: analysis of the process creating multitiered social structures. Animal

Behaviour, 69(6), 1357-1371.

Wrangham, R.W. (1979). Sex differences in chimpanzee dispersion. In D.A. Hamburg &

E.R. McCown, (Eds.), The great apes (pp. 13-53). Menlo Park:

Benjamin/Cummings.

Wrangham, R.W. (1980). An ecological model of female-bonded primate groups.

Behaviour, 75(3-4), 262-300.

Wrangham, R. W. (1986). Ecology and social relationships in two species of chimpanzee.

In D. I. Rubenstein, & R. W. Wrangham (Eds.), Ecological aspects of social

evolution: Birds and mammals (pp. 352-378). Princeton: Princeton University

Press.

Wrangham, R.W. (2000). Why are male chimpanzees more gregarious than mothers? A

scramble competition hypothesis. In P.M. Kappeler, (Ed.), Primate males: Causes

and consequences of variation in group composition (pp. 248-258). Cambridge:

Cambridge University Press.

Wrangham, R. W., & Smuts, B. B. (1980). Sex differences in the behavioural ecology of

chimpanzees in the Gombe National Park, Tanzania. Journal of Reproduction and

Fertility, Suppl 28, 13-31.

134

Wrangham, R.W., Clark, A.P., & Isabirye-Basuta, G. (1992). Female social relationships

and social organization of Kibale Forest chimpanzees. In T. Nishida, W.C.

McGrew, P. Marler, M. Pickford, & F.D.M. de Waal, (Eds.), Topics in primatology:

Human origins (pp. 81-98). Tokyo: University of Tokyo Press.

135

APPENDIX A: LIST OF PLANT SPECIES CONSUMED BY THE SPIDER

MONKEYS AT RUNAWAY CREEK

*Plant part consumed includes the following items: FR= fruit ripe, FU= fruit unripe, (S)= seed, LB= leaf bud, LN= leaf new, LM= leaf mature, LS= leaf stem, FLB= flower bud,

FLM= flower mature

Plant Part Family: Genus: Species: Common Name: Consumed*: Anacardiaceae Astroneum graveolens Jobillo FR, LN Anacardiaceae Metopium brownei Black FR, FU, LN, Poisonwood FLB Anacardiaceae Spondias radlkoferi Hog Plum FR, FU, LN

Annonaceae sp. Wild Coffee LN, FLM Apocynaceae Aspidosperma megalocarpon White My Lady FU(S), LB, LN, LM, FLB, FLM Apocynaceae Plumeria obtusa Franjipani LN Apocynaceae Stemmadenia donnell-smithii Horse Balls FR Araceae Anthurium schlechtendalii Anthurium/ LB, LN, LS, Pheasant's Tail FLM Araceae Philodendron radiatum Philodendron LB, LN, LS Araceae Philodendron sp. Split-Leaf LB, LN, LS Philodendron Araliaceae Dendropanax arboreus White FR, FU, FLM Gumbolimbo Arecaceae Attalea cohune Cohune Palm FR, FU Arecaceae Cryosophila stauracantha Give and Take FR, FU Palm Arecaceae Gaussia maya Gaussia Maya FR, FU, FLB Palm Arecaceae Sabal mauritiiformis Bay Leaf Palm FR Arecaceae Sabal yapa Tiger Bay Leaf FR, FU, FLM, Palm FLB Begoniaceae Begonia sericoneura Begonia LS Bombacaceae Ceiba pentandra Cotton Tree/ LN, LS Ceiba

136

Plant Part Family: Genus: Species: Common Name: Consumed*: Bombacaceae Pseudobombax ellipticum Psuedo Bombax/ FLB, FLM Mapola Boraginaceae Cordia diversifolia Swiddle Wood FR, LN, FLB Burseraceae Bursera simaruba Red Gumbolimbo FR, FU, LN Burseraceae Protium copal Copal FR, FU, LN, FLM Caesalpiniaceae Dialium guianense Ironwood FR, FU, LN, FLM Calophyllaceae Calophyllum brasiliense Santa Maria FR Caricaceae Carica papaya Wild Papaya FR Cecropiaceae Cecropia peltata Cecropia FR, LB, LN, LM, LS, FLM Chrysobalanaceae Hirtella americana Pigeon Plum FR, FU Combretaceae Combretum fruticosum Maiden Hair FLB, FLM Brush Vine Combretaceae Terminalia amazonia Nargusta FR

Connaraceae Cnestidium rufescens FR Convolvulaceae Ipomoea sepacultensis Wood Rose Vine LB, LN Dilleniaceae Davilla? sp. Sandpaper Vine FR Dracaenaceae Dracaena americana Candle Wood FR Ebenaceae Diospyros digyna Black Sapote FR

Ebenaceae Diospyros salicifolia FR Euphorbiaceae Drypetes browneii Male Bull Hoof FR, FU, LN, FLB, FLM

Euphorbiaceae Sebastiania sp. LN Fabaceae Acacia cookii Red Bullhorn FR, FU Acacia Fabaceae Acacia dolichostachya Acacia/ Wild FR Tamarind Fabaceae Andira inermis Ball Seed LN Fabaceae Caesalpinia gaumeri Warrie Wood FR, FU(S), LN Fabaceae Cojoba arborea Barba Jolote FR Fabaceae Inga affinis Bri-Bri FR Fabaceae Inga sapindoides Tama-Tama Bri- FR Bri Fabaceae Lonchocarpus guatemalensis (?) Dog Wood FR, LN Fabaceae Lonchocarpus minimiflorus White Cabbage LB, LN, FLB Bark 137

Plant Part Family: Genus: Species: Common Name: Consumed*: Fabaceae Lonchocarpus rugosus Red Cabbage LN, FLM Bark Fabaceae Schizolobium parahyba Quam Wood FR(S) Fabaceae Swartzia cubensis Bastard FR Rosewood Fabaceae Zygia confusa Turtle Bone LN Flacourtiaceae Laettia corymbosa Paletillo FR Flacourtiaceae Xylosma sp. Wild Lime LN

Lauraceae Licaria peckii FR Lauraceae Nectandra belizensis Timbersweet FR Lauraceae Nectandra sp. Aguacatillo FR Loganiaceae Strychnos panamensis Snake Vine FR, LB Loranthaceae Psitticanthus calyculata Phoradendron/ FR, LN Mistletoe Malpighiaceae Byrsonima crassifolia Wild Craboo FR

Meliaceae Guarea sp. (cf. glabra) FR, FU, LN Meliaceae Trichilia pallida Carbon del Rio FR

Menispermaceae Abuta panamensis FR(S) Moraceae Brosimum alicastrum Wild Breadnut FR, FU(S), LB, LN, LM, FLB, FLM Moraceae Castilla elastica Rubber Tree FR

Moraceae Coussapoa oligocephala FR, FLM Moraceae Ficus guajavoides Fig FR Moraceae Ficus insipida Fig FR, FU, LB, LN Moraceae Ficus maxima Fig FR Moraceae Ficus pertusa Fig FR, FU, LB, LN Moraceae Ficus popenoei Fig FR, FU, LB, LN, LM Moraceae Pseudolmedia spuria Wild Cherry FR, FU(S), LN, FLB, FLM Moraceae Trophis racemosa Red Ramon FR, FU, FLB

Moraceae Trophis sp. FR

Moraceae sp. Bastard Breadnut FR

Myrtaceae Eugenia aeruginea FR

138

Plant Part Family: Genus: Species: Common Name: Consumed*: Myrtaceae Eugenia sp. Guayavillo FR

Oleaceae sp. LN Passifloraceae Passiflora biflora Passion Flower FR, FU Vine Polygonaceae Coccoloba belizensis Wild Grape FR, LN

Polygonaceae Coccoloba hondurensis FR, FU

Rhamnaceae Zizyphus sp. FR, FU Rubiaceae Alseis yucatanensis Wild Mammee FR Rubiaceae Guettarda combsii Glassy Wood FR, FU, FLM Rubiaceae Hamelia patens Polly Red Head FR

Rubiaceae Psychotria costivenia FR

Rubiaceae sp. FR, LB Sapindaceae Cupania belizensis Grande Betty FR, FU

Sapindaceae Sapindus sp. FR, FU Sapindaceae Sapindus saponaria Soap Tree LN Sapindaceae sp. FR

Sapindaceae sp. LB Sapotaceae Manilkara chicle Sapodilla/ Chicle FR, FU, LN Sapotaceae Manilkara staminodella Sapodilla FR, FU, LB, FLB Sapotaceae Paullinia sp. FR Sapotaceae Pouteria amygdalina Red Sillion FR, LN Sapotaceae Pouteria durlandii Mammee Cirela FR, FU Sapotaceae Pouteria reiticulata Sapotillo FR, LN Sapotaceae Sideroxylon floribundum Cream Wood/ FR Cream Tree

Sapotaceae sp. FR, FU, LN Simaroubaceae Simarouba glauca Negrito FR Smilacaceae Smilax china China Root LB Smilacaceae Smilax sp. Wild Yam Vine LB, LN Solanaceae Cestrum noctornum Night Bloom LN, LM Tiliaceae Luhea speciosa Mountain Moho FR, FU, FLM Tiliaceae Trichospermum grewiifolium Narrow Leaf FLM Moho Ulmaceae Ampelocera hottlei Female Bull Hoof FR, FU, FLM, FLB, LB, LN Verbenaceae Petrea volubilis Royal Petrea Vine LB, LN, FLM 139

Plant Part Family: Genus: Species: Common Name: Consumed*: Verbenaceae Vitex gaumeri Fiddle Wood LB, FLB, FLM Viscaceae Phoradendron sp. Phoradendron/ LB Scorn the Earth Vitaceae Cissus gossypiifolia Water Vine FR, LB, LN

140

APPENDIX B: DYADIC ESTIMATES OF RELATEDNESS AND ASSOCIATION

INDEX VALUES

FEMALE-FEMALE DYADS: List of estimates of relatedness values (R) and simple ratio association indices (SRI) for all female-female dyads (N= 105). On the left table, dyads are sorted by R-values highest to lowest (R mean= 0.08; range= 0 – 0.5). On the right table, dyads are sorted by SRI values highest to lowest (SRI mean= 1.25, range= 0.2 – 2.9).

ID1 ID2 R-value ↓ SRI ID1 ID2 R-value SRI ↓ Fig Flower 0.5 2.42 Frugivory Freckles 0.22 2.92 Flirt Ficus 0.5 1.25 Frugivory Forget 0 2.83 Fungus Flirt 0.5 1.17 Fury Flora 0.14 2.75 Frugivory Franjipani 0.5 1.08 Freckles Forget 0 2.67 Freckles Franjipani 0.37 1.5 Fro Flower 0 2.5 Fig Flora 0.3 0.33 Fig Flower 0.5 2.42 Fungus Frugivory 0.29 1.58 Fury Flower 0.25 2.42 Fugly Frugivory 0.29 1.42 Fungus Fro 0.01 2.33 Fugly Freckles 0.26 1.83 Fury Fro 0 2.25 Fungus Franjipani 0.26 1.42 Freckles Flame 0.07 2.17 Fanta Flora 0.26 0.5 Flower Flirt 0.15 2 Fury Flower 0.25 2.42 Fungus Ficus 0 2 Fig Fanta 0.25 1.42 Fugly Ficus 0.01 1.92 Fanta Franjipani 0.24 0.5 Fugly Freckles 0.26 1.83 Fanta Frugivory 0.24 0.5 Frugivory Flame 0.07 1.83 Frugivory Freckles 0.22 2.92 Flower Ficus 0 1.83 Fungus Freckles 0.21 1.67 Fro Ficus 0 1.83 Flower Flame 0.21 1.17 Fugly Fro 0 1.83 Flirt Flame 0.21 1 Fungus Flower 0 1.83 Fury Frugivory 0.19 1.5 Freckles Ficus 0 1.75 Fugly Forget 0.16 1.33 Fungus Fugly 0 1.75 Flower Flirt 0.15 2 Fury Fungus 0 1.75 Fro Flirt 0.15 1.67 Fungus Freckles 0.21 1.67 Fury Forget 0.15 1.25 Fro Flirt 0.15 1.67 Franjipani Flirt 0.15 0.67 Flower Flora 0 1.67 Fury Flora 0.14 2.75 Fungus Frugivory 0.29 1.58 141

ID1 ID2 R-value ↓ SRI ID1 ID2 R-value SRI ↓ Fig Fugly 0.14 0.25 Fro Freckles 0.12 1.58 Fro Freckles 0.12 1.58 Forget Flame 0 1.58 Fanta Forget 0.12 0.58 Frugivory Ficus 0 1.58 Fanta Fungus 0.1 0.67 Fury Ficus 0 1.58 Fungus Flora 0.09 1.25 Freckles Franjipani 0.37 1.5 Freckles Flower 0.08 1.33 Fury Frugivory 0.19 1.5 Freckles Flame 0.07 2.17 Fugly Flower 0 1.5 Frugivory Flame 0.07 1.83 Fugly Frugivory 0.29 1.42 Flame Ficus 0.07 1.42 Fungus Franjipani 0.26 1.42 Fugly Flirt 0.07 0.83 Fig Fanta 0.25 1.42 Fig Flame 0.07 0.17 Flame Ficus 0.07 1.42 Frugivory Flower 0.06 1.25 Forget Flower 0 1.42 Franjipani Flora 0.06 0.75 Fugly Franjipani 0 1.42 Freckles Flirt 0.05 1 Fury Flirt 0 1.42 Fro Flame 0.04 1 Fugly Forget 0.16 1.33 Freckles Flora 0.03 0.92 Freckles Flower 0.08 1.33 Fig Ficus 0.03 0.25 Fro Flora 0 1.33 Forget Flora 0.02 1 Fro Forget 0 1.33 Fungus Fro 0.01 2.33 Fugly Flame 0 1.33 Fugly Ficus 0.01 1.92 Fungus Flame 0 1.33 Franjipani Ficus 0.01 1.08 Fury Freckles 0 1.33 Frugivory Forget 0 2.83 Fury Fugly 0 1.33 Freckles Forget 0 2.67 Flirt Ficus 0.5 1.25 Fro Flower 0 2.5 Fury Forget 0.15 1.25 Fury Fro 0 2.25 Fungus Flora 0.09 1.25 Fungus Ficus 0 2 Frugivory Flower 0.06 1.25 Flower Ficus 0 1.83 Forget Ficus 0 1.25 Fro Ficus 0 1.83 Fungus Forget 0 1.25 Fugly Fro 0 1.83 Fungus Flirt 0.5 1.17 Fungus Flower 0 1.83 Flower Flame 0.21 1.17 Freckles Ficus 0 1.75 Flora Ficus 0 1.17 Fungus Fugly 0 1.75 Fro Franjipani 0 1.17 Fury Fungus 0 1.75 Frugivory Fro 0 1.17 Flower Flora 0 1.67 Frugivory Franjipani 0.5 1.08 Forget Flame 0 1.58 Franjipani Ficus 0.01 1.08 Frugivory Ficus 0 1.58 Fanta Freckles 0 1.08 142

ID1 ID2 R-value ↓ SRI ID1 ID2 R-value SRI ↓ Fury Ficus 0 1.58 Fanta Fury 0 1.08 Fugly Flower 0 1.5 Franjipani Forget 0 1.08 Forget Flower 0 1.42 Frugivory Flora 0 1.08 Fugly Franjipani 0 1.42 Flirt Flame 0.21 1 Fury Flirt 0 1.42 Freckles Flirt 0.05 1 Fro Flora 0 1.33 Fro Flame 0.04 1 Fro Forget 0 1.33 Forget Flora 0.02 1 Fugly Flame 0 1.33 Flora Flirt 0 1 Fungus Flame 0 1.33 Forget Flirt 0 1 Fury Freckles 0 1.33 Franjipani Flower 0 1 Fury Fugly 0 1.33 Freckles Flora 0.03 0.92 Forget Ficus 0 1.25 Fanta Fro 0 0.92 Fungus Forget 0 1.25 Fig Fury 0 0.92 Flora Ficus 0 1.17 Flora Flame 0 0.92 Fro Franjipani 0 1.17 Franjipani Flame 0 0.92 Frugivory Fro 0 1.17 Frugivory Flirt 0 0.92 Fanta Freckles 0 1.08 Fugly Flora 0 0.92 Fanta Fury 0 1.08 Fury Flame 0 0.92 Franjipani Forget 0 1.08 Fury Franjipani 0 0.92 Frugivory Flora 0 1.08 Fugly Flirt 0.07 0.83 Flora Flirt 0 1 Fig Fro 0 0.83 Forget Flirt 0 1 Franjipani Flora 0.06 0.75 Franjipani Flower 0 1 Fanta Flower 0 0.75 Fanta Fro 0 0.92 Franjipani Flirt 0.15 0.67 Fig Fury 0 0.92 Fanta Fungus 0.1 0.67 Flora Flame 0 0.92 Fanta Forget 0.12 0.58 Franjipani Flame 0 0.92 Fanta Flora 0.26 0.5 Frugivory Flirt 0 0.92 Fanta Franjipani 0.24 0.5 Fugly Flora 0 0.92 Fanta Frugivory 0.24 0.5 Fury Flame 0 0.92 Fanta Ficus 0 0.5 Fury Franjipani 0 0.92 Fanta Flame 0 0.5 Fig Fro 0 0.83 Fanta Flirt 0 0.5 Fanta Flower 0 0.75 Fig Flirt 0 0.5 Fanta Ficus 0 0.5 Fanta Fugly 0 0.42 Fanta Flame 0 0.5 Fig Flora 0.3 0.33 Fanta Flirt 0 0.5 Fig Freckles 0 0.33 143

ID1 ID2 R-value ↓ SRI ID1 ID2 R-value SRI ↓ Fig Flirt 0 0.5 Fig Fugly 0.14 0.25 Fanta Fugly 0 0.42 Fig Ficus 0.03 0.25 Fig Freckles 0 0.33 Fig Forget 0 0.25 Fig Forget 0 0.25 Fig Fungus 0 0.25 Fig Fungus 0 0.25 Fig Flame 0.07 0.17 Fig Franjipani 0 0.17 Fig Franjipani 0 0.17 Fig Frugivory 0 0.17 Fig Frugivory 0 0.17

MALE-MALE DYADS: List of estimates of relatedness values (R) and simple ratio association indices (SRI) for all male-male dyads (N= 21). On the left table, dyads are sorted by R-values highest to lowest (R mean= 0.15; range= 0 – 0.53). On the right table, dyads are sorted by SRI values highest to lowest (SRI mean= 1.7, range= 0.25 – 3.6).

ID1 ID2 R-value ↓ SRI ID1 ID2 R-value SRI ↓ Frog Ferdelance 0.53 2.5 FalseFrog Faita 0.17 3.58 Fryjack Frog 0.52 0.42 Forest Ferdelance 0 3.5 Fiddle FalseFrog 0.5 0.33 Frog FalseFrog 0.3 3.33 Frog FalseFrog 0.3 3.33 Frog Faita 0.21 3.33 Ferdelance FalseFrog 0.27 2.08 Frog Forest 0 2.75 Fiddle Frog 0.22 0.58 Frog Ferdelance 0.53 2.5 Fryjack Ferdelance 0.22 0.92 Ferdelance Faita 0 2.33 Frog Faita 0.21 3.33 Forest Faita 0 2.25 FalseFrog Faita 0.17 3.58 Ferdelance FalseFrog 0.27 2.08 Fryjack Forest 0.14 1.17 Fryjack Fiddle 0 1.75 Fiddle Faita 0.07 0.42 Forest FalseFrog 0 1.58 Ferdelance Faita 0 2.33 Fryjack Forest 0.14 1.17 Fiddle Ferdelance 0 0.67 Fryjack Ferdelance 0.22 0.92 Fiddle Forest 0 0.92 Fiddle Forest 0 0.92 Forest Faita 0 2.25 Fiddle Ferdelance 0 0.67 Forest FalseFrog 0 1.58 Fiddle Frog 0.22 0.58 Forest Ferdelance 0 3.5 Fryjack Frog 0.52 0.42 Frog Forest 0 2.75 Fiddle Faita 0.07 0.42 Fryjack Faita 0 0.42 Fryjack Faita 0 0.42 Fryjack FalseFrog 0 0.25 Fiddle FalseFrog 0.5 0.33 Fryjack Fiddle 0 1.75 Fryjack FalseFrog 0 0.25 Frog Ferdelance 0.53 2.5 FalseFrog Faita 0.17 3.58 144

ID1 ID2 R-value ↓ SRI ID1 ID2 R-value SRI ↓ Fryjack Frog 0.52 0.42 Forest Ferdelance 0 3.5 Fiddle FalseFrog 0.5 0.33 Frog FalseFrog 0.3 3.33 Frog FalseFrog 0.3 3.33 Frog Faita 0.21 3.33

145