INTRODUCTION
Complex, hierarchical social systems, termed multi-level societies, are
present in species from many distantly related taxa, such as birds
(Papageorgiou et al., 2019), cetaceans (Whitehead et al., 2012), equids
(Rubenstein & Hack, 2004), proboscideans (Wittemyer, Douglas-Hamilton,
& Getz, 2005), primates (Grueter, Matsuda, Zhang, & Zinner, 2012), and
chiropterans (Kerth, Perony, & Schweitzer, 2011). Determining why these
types of societies evolve and how they function are key questions in
biology. In multi-level societies, stable subgroups (hereafter core
units) associate in a hierarchical manner (Grueter, Qi, Li, & Li,
2017). Up to four tiers of non-random association have been documented,
with higher tiers numbering hundreds of individuals in some species
(Grueter, Matsuda, Zhang, & Zinner, 2012; Snyder-Mackler, Beehner, &
Bergman, 2012; Schreier & Swedell, 2012a; Wittemeyer et al., 2005). The
factors that determine the number and composition of different social
tiers and the ways that ecological and social pressures affect their
stability are still poorly understood for most species (Grueter et al.,
2017; Farine et al., 2015).
Several hypotheses have been proposed to explain the function of
different tiers in multi-level societies. The advantages and
disadvantages of group living for animals have been well documented
(Krause & Ruxton, 2002) and multi-level societies appear to have
evolved because they allow animals to adjust group size more fluidly
than is possible in stable groups (Aureli et al., 2008; Grueter et al.,
2017). Large aggregations are beneficial, primarily because of the
multiple ways that they lower predation risk (i.e., detection, dilution,
predator confusion, defence, Hamilton, 1971; Pulliam & Caraco, 1984),
while the chief cost of large group size is the increase in food
competition that results from many conspecifics together (Terborgh &
Janson, 1986). Indeed, there are examples of multi-level societies
forming large aggregations at higher tiers when predators are nearby
(e.g., Papio hamadryas , Schreier & Swedell, 2012b;Physeter microcephalus , Whitehead et al., 2012), and fissioning
to lower tiers when resource availability is reduced (e.g.,Loxodonta africana , Wittemyer et al., 2005; Orcinus orca,Foster et al., 2012; Papio hamadryas , Schreier & Swedell, 2012b;Rhinopithecus roxellana , Qi et al., 2014). An alternative
explanation for the evolution of multi-level societies, the bachelor
threat hypothesis (Rubenstein, 1986), has garnered support, particularly
in zebras and primates (e.g., Rubenstein & Hack, 2004; Pappano,
Snyder-Mackler, Bergman, & Beehner, 2012; Xiang et al., 2014). This
hypothesis suggests that core units (which are one-male/multi-female
(OMUs) in many species) associate to decrease the amount of harassment
they receive from extra-unit males (Grueter & van Schaik, 2009;
Rubenstein, 1986).
In addition to predation, food competition, and conspecific threat, the
degree that animals associate can be influenced by breeding seasonality
(Baden, Webster, & Kamilar, 2016), migration (Colbeck et al., 2013),
genetic structure (kinship) (Reisinger, Beukes, Hoelzel, & de Bruyn,
2017), and phylogeny (Balasubramaniam et al., 2018). Some of these
factors fluctuate over time, often in a predictable, seasonal manner
that can lead to adjustments in association patterns as animals try to
balance the costs and benefits of group living. Thus, to understand if
and how temporal environmental changes influence tier formation in
multi-level societies, it is important to study social behaviour over
time, both within and between the social tiers (Grueter, Chapais, &
Zinner, 2012). Primates are good study subjects to examine the various
factors influencing tier formation and stability in multi-level
societies because researchers are often able to collect detailed
observational data on many identifiable individuals.
Our goal was to determine the degree of temporal variability in
inter-unit associations in a recently discovered multi-level society of
Rwenzori Angolan colobus monkey (Colobus angolensis ruwenzorii ),
and to determine which social and ecological factors may influence this
variability. This multi-level society, described for our population at
Lake Nabugabo, Uganda, is unique among primates in that it contains not
only OMUs, but also core units that are multi-male/multi-female (MMUs),
with up to eight socially-integrated, reproductive males (Stead &
Teichroeb, 2019). There are at least three tiers of social organization;
core units fission and fuse with one another throughout the day but
associate preferentially with core units from the same clan and clans
share a home range in a band tier of organization. Initial cluster
analyses with one year of data revealed two clans in our study band of
12 core units (Stead & Teichroeb, 2019). We do not yet know the
selective pressures that influence tier formation or if tiers are stable
over time.
In this study, we applied social network analysis (SNA) to core unit
associations observed over 21 months at Nabugabo. SNA has proven
extremely useful in elucidating the form of multi-level societies (e.g.,
Papageorgiou et al., 2019; Snyder-Mackler et al., 2012; Zhang, Li, Qi,
MacIntosh, & Watanabe, 2012) and determining how within-unit
interactions structure them (Matsuda et al., 2012). Further application
of SNA to understanding the associations between the higher tiers in
multi-level societies offers a view of the dynamics of these complex
social systems (Yeager, 1991). We first examined whether clan-level
groupings of C. a. ruwenzorii core units stayed the same over
time. Unlike many other social orders of mammals, primates tend to form
stable groups over relatively long periods of time that are structured
by the bonding of the philopatric sex (Altmann et al., 1996; Silk, 2001;
2002; Di Fiore, 2012). These kin-based systems extend beyond the
smallest social unit to higher tiers in primate multi-level societies
(Colmenares, 2004; Snyder-Mackler, Alberts, & Bergman, 2014; Morrison,
Groenenberg, Breuer, Manguette, & Walsh, 2019). Preliminary data thus
far suggest that though both males and females disperse from their natal
core unit in C. a. ruwenzorii , and males transfer into other core
units within the band while most females emigrate out of the band (Stead
& Teichroeb, 2019). Thus, male kinship could structure relations
between core units, leading to stable clans over time. Second, we
examined temporal variation in core unit clustering relative to
ecological (seasonality in rainfall and food availability) and social
(inter-unit dispersals) conditions. Greater overall food availability
should allow larger aggregations to form because food competition is
alleviated (e.g., Foster et al., 2012; Schreier & Swedell, 2012b;
Wittemyer et al., 2005). This temporal clustering of groups due to
resource availability may then allow individuals to assess dispersal
opportunities in other groups (Clobert, Le Galliard, Cote, Meylan, &
Massot, 2009; Mares, Bateman, English, Clutton-Brock, & Young., 2014),
which could potentially lead to a seasonal pattern in dispersals (e.g.,
Ekernas & Cords, 2007; Yao et al., 2011; Young et al., 2019). In
addition, groups that have recently had individuals disperse between
them may associate more closely during these periods compared to when no
transfers are occurring; likely because it takes time for bonds among
former group members to sever and to establish bonds in the new group
(Isbell & Van Vuren, 1996).
Accordingly, we hypothesized that both ecological and social variables
(i.e., male relationships) would influence clan stability and the degree
of clustering among C. a. ruwenzorii core units. We predicted
that clans would be stable over time, due to tolerance of close
proximity between core units that share male kin or familiar males.
Fruits are the only food type positively selected for and these are high
in quality compared to the rest of this species’ diet, which consists
largely of young leaves (JAT, unpubl. data). We therefore predicted that
core unit clustering would be influenced most strongly by the
availability of fruits, and that core units would associate more during
times of high fruit availability when food competition is minimized. We
further predicted that greater clustering of core units at times of peak
fruit availability, would allow males to assess the possibilities for
immigration in other core units, leading to a seasonal pattern of
dispersal between core units. Finally, we predicted that associations
between core unit dyads would be more frequent during and immediately
after male transfer between them.