Grueter, C C; van Schaik, C P (2010). Evolutionary determinants of modular societies in colobines. Behavioral Ecology, 21(1):63-71. Postprint available at: http://www.zora.uzh.ch University of Zurich Posted at the Zurich Open Repository and Archive, University of Zurich. Zurich Open Repository and Archive http://www.zora.uzh.ch Originally published at: Behavioral Ecology 2010, 21(1):63-71.
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Year: 2010
Evolutionary determinants of modular societies in colobines
Grueter, C C; van Schaik, C P
Grueter, C C; van Schaik, C P (2010). Evolutionary determinants of modular societies in colobines. Behavioral Ecology, 21(1):63-71. Postprint available at: http://www.zora.uzh.ch
Posted at the Zurich Open Repository and Archive, University of Zurich. http://www.zora.uzh.ch
Originally published at: Behavioral Ecology 2010, 21(1):63-71. Evolutionary determinants of modular societies in colobines
Abstract
Modular societies are structurally characterized by nuclear one-male units (OMUs, or harems) embedded within larger relatively coherent social bands. Within the order Primates, modular societies are uncommon, found in only a few species, including humans. Asian colobines (Presbytini) principally form either unimale groups that forage independently and are often territorial, or modular associations, which range from tight bands composed of OMUs to loose neighborhoods of OMUs. A phylogenetic reconstruction of modularity in the Presbytini revealed that the single OMU pattern is probably the ancestral state while the modular pattern is derived. The selective forces favoring the evolution of modular societies have thus far been virtually unexplored. Although some ecological explanations cannot be ruled out at the moment due to lack of comparative and quantitative data, preliminary circumstantial evidence does not seem to support them. Instead, a social factor, bachelor threat, is consistent with many observations. This hypothesis argues that where the pressure from nonreproductive bachelor males is unusually high, OMUs aggregate as a means of decreasing the amount of harassment and the risk of takeovers and infanticide. A comparative test found an association between modular societies and bachelor threat, as proxied by sex ratio within social units. The concentration of modular systems in colobines may be due to their unusual ecology, which leads to unusually low intensity of scramble competition. Modular colobines rely more on nonlimiting ubiquitous resources than nonmodular ones and thus can afford to gather in bands. Moreover, by comparing the slopes of regressions between group size and daily travel distance for several groups of one modular and one nonmodular colobine, we found slopes in the nonmodular to be steeper by a factor 30, indicating that ecological constraints associated with scramble competition prevent higher level groupings in nonmodulars. Thus, modular sociality in Asian colobines may have arisen because both social benefits are substantial and ecological costs are relatively low. 1 Evolutionary Determinants of Modular Societies in Colobines
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4 Cyril C. Grueter1,2, Carel P. van Schaik1
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6 1Anthropological Institute and Museum, University of Zurich, Switzerland
7 2To whom correspondence should be addressed at: Max Planck Institute for Evolutionary Anthropology,
8 Department of Primatology, Deutscher Platz 6, 04103 Leipzig, Germany; [email protected]
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10 Short title: Modular Societies in Colobines
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1 27 Abstract
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29 Modular societies are structurally characterized by nuclear one-male units (OMUs, or
30 harems) embedded within larger relatively coherent social bands. Within the order Primates,
31 modular societies are uncommon, found in only a few species, including humans. Asian
32 colobines (Presbytini) principally form either uni-male groups that forage independently and
33 are often territorial, or modular associations, which range from tight bands composed of
34 OMUs to loose neighborhoods of OMUs. A phylogenetic reconstruction of modularity in the
35 Presbytini revealed that the single OMU pattern is probably the ancestral state while the
36 modular pattern is derived. The selective forces favoring the evolution of modular societies
37 have thus far been virtually unexplored. While some ecological explanations cannot be ruled
38 out at the moment due to lack of comparative and quantitative data, preliminary
39 circumstantial evidence does not seem to support them. Instead, a social factor, bachelor
40 threat, is consistent with many observations. This hypothesis argues that where the pressure
41 from non-reproductive bachelor males is unusually high, OMUs aggregate as a means of
42 decreasing the amount of harassment and the risk of takeovers and infanticide. A comparative
43 test found an association between modular societies and bachelor threat, as proxied by sex
44 ratio within social units. The concentration of modular systems in colobines may be due to
45 their unusual ecology, which leads to unusually low intensity of scramble competition.
46 Modular colobines rely more on non-limiting ubiquitous resources than non-modular ones
47 and thus can afford to gather in bands. Moreover, by comparing the slopes of regressions
48 between group size and daily travel distance for several groups of one modular and one non-
49 modular colobine, we found slopes in the non-modular to be steeper by a factor 30, indicating
50 that ecological constraints associated with scramble competition prevent higher-level
2 51 groupings in non-modulars. Thus, modular sociality in Asian colobines may have arisen
52 because both social benefits are substantial and ecological costs are relatively low.
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54 Key Words: colobine; snub-nosed monkey; multilevel society; one-male unit; conspecific
55 threat; ecological constraints; phylogeny
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57 Introduction
58 Whereas in most animals living in stable and individualized social groups there are no
59 levels of social organization beyond the social group, there are some exceptions, known as
60 multilevel social systems or modular societies, which comprise two levels of distinguishable
61 social grouping. They have been documented in several mammal species. Thus, African
62 elephants (Loxodonta africana) regularly form large aggregations of stable subunits
63 consisting of female bonded family groups (Moss and Poole 1983; Wittemyer et al. 2005). In
64 plains zebras (Equus burchelli) and khulans (Equus hemionus), harems regularly join to form
65 large, spatially cohesive herds (Feh et al. 2001; Rubenstein and Hack 2004). Other
66 mammalian taxa with comparable multilevel social systems include sperm whales (Physeter
67 macrocephalus) (Whitehead et al. 1991), killer whales (Orcinus orca) (Baird 2000) and
68 prairie dogs (Cynomys ludovicianus) (Hoogland 1995).
69 Among primates, a few species have been shown to have modular societies, e.g. snub-
70 nosed monkeys (Rhinopithecus spp.) (Kirkpatrick 1998), proboscis monkeys (Nasalis
71 larvatus) (Yeager 1990), gelada baboons (Theropithecus gelada) (Kawai et al. 1983),
72 hamadryas baboons (Papio hamadryas) (Kummer 1984), and humans (e.g. Chapais 2008).
73 The foremost structural characteristics of primate modular systems are stable entities, usually
74 one-male units (OMUs), which frequently or permanently associate, and thus form a higher
75 grouping level, often termed the band (Grueter and Zinner [2004] and references therein)
3 76 (Fig. 1). Bands can be very large in size, with up to several hundred members (ibid.).
77 Sociopositive and sexual behavior is largely restricted to the first tier, the OMU, while inter-
78 unit interactions are limited (e.g. Dunbar and Dunbar 1975; Grueter 2009; Zhang et al. 2006).
79 Most modular taxa share other traits that distinguish them from the non-modular ones:
80 conspicuous sexual size dimorphism (Grueter and van Schaik 2009), prominent male
81 adornments (Grueter and Zinner 2004), large relative testes size (ibid.), large home ranges,
82 and low population density (Grueter 2009).
83 In Asian colobines (Presbytini), three forms of social organization can be recognized:
84 (i) separate, often territorial OMUs with little range overlap and few inter-unit encounters
85 (and if so, rather aggressive) (e.g. Presbytis hosei (Mitchell 1994), Trachypithecus vetulus
86 (Rudran 1973)); (ii) large coherent multimale-multifemale groups (only found in
87 Semnopithecus spp., e.g. (Borries 2000); (iii) modular societies, with OMUs having large
88 (>40%) range overlap, at times coordinating travel and occupying adjacent sleeping trees
89 (Stanford 1991a, b), or co-feeding in the same patch or adjacent patches (Bennett 1983;
90 Mukherjee and Saha 1974), or OMUs exhibiting complete range overlap and forming tight
91 cohesive bands that rarely split (e.g. Rhinopithecus bieti (Kirkpatrick et al. 1998)). In
92 modular societies, relations among units are generally rather neutral (e.g. (Yeager 1992)).
93 In this paper we examine the evolution of modular societies in Asian colobines. We
94 first ask whether modular societies are derived in this taxon, as assumed by the hypothesis
95 that follows. We then examine the conditions that led to the evolution of modular societies,
96 focusing on social or ecological determinants in turn. The bachelor threat hypothesis
97 (Rubenstein 1986) posits that OMUs assemble and OMU males may form coalitions to
98 decrease the amount of harassment, in particular the risk of takeovers and infanticide by non-
99 reproductive bachelor groups. Rubenstein (1986) argued that bachelor threat is the most
100 plausible scenario for the evolution of multi-level societies in plains zebras. He found that
4 101 when coalitions form, female contact by bachelors was significantly reduced. OMU males
102 thus benefit from a reduced risk of being ousted from their OMU, whereas females benefit
103 from a reduced risk of infanticide. Sexual conflict, in the form of coercion and infanticide,
104 may have been a critical selective factor shaping primate social systems (Chapman and
105 Pavelka 2005; Harcourt and Stewart 2007; Smuts and Smuts 1993; Sterck et al. 1997; van
106 Schaik 1996). Nonetheless, this hypothesis has not been applied to modular primate societies.
107 R. Wrangham (personal communication), Mori (1979) and Dunbar and Dunbar (1975) noted
108 that several gelada unit leaders sometimes engaged in a collective challenge to confront and
109 chase invading all-male groups. A few comparative studies on primates living in other types
110 of social organization also demonstrated that conspecific threat influences group size (Janson
111 and van Schaik 2000; Treves and Chapman 1996).
112 To test the bachelor threat hypothesis, we developed the following prediction: across
113 species, presence/absence of modularity (categorical) and home range overlap (as continuous
114 proxy variable for modularity) are positively correlated with the number of bachelor males in
115 the population (cf. Rubenstein and Hack 2004). Assuming an even male female sex ratio at
116 birth, the adult sex ratio (F:M) in mixed-sex units can serve as a proxy measure for bachelor
117 threat. The higher the value, the more males are expected to be excluded from breeding units.
118 That sex ratio is an accurate proxy for bachelor threat has been corroborated by the
119 significant positive correlation between the actual number of nongroup males per bisexual
120 group and sex ratio of bisexual groups in 19 groups of Semnopithecus spp. (rs = 0.596, p =
121 0.007; data from Treves & Chapman 1996).
122 Many ecological benefits have been proposed to have favored group living in primates
123 and other animals: localized resources (Altmann 1974), harvest efficiency (Altmann 1974;
124 Cody 1971; Cords 1987; Rodman 1988), predation avoidance (Alexander 1974; van Schaik
125 1983), between-group resource competition (Yeager 1992, Wrangham 1980), and thermal
5 126 benefits (Bleisch and Xie 1998). Table 1 presents empirical and circumstantial evidence that
127 these non-exclusive hypotheses are rather unlikely to explain why some Asian colobines
128 evolved a tendency toward modularity. However, a more systematic assessment is needed
129 once comparative data become available. Moreover, the predation hypothesis is not easy to
130 characterize in quantitative terms and thus will be difficult to be ruled out completely. The
131 localized resource hypothesis does not appear to be applicable to the strictly modular
132 societies, but may be an explanation for the loose neighborhoods found in some colobine
133 species.
134 Even if there are no pervasive ecological benefits, however, the ecological conditions
135 must permit the large groups associated with modular societies, and we will compare the
136 extent of scramble competition, which is a direct function of group size (van Schaik and van
137 Noordwijk 1988; Janson and Goldsmith 1995), among modular and non-modular colobines.
138 We would expect that modular colobines should be less ecologically constrained to form
139 bands than non-modular ones. Specifically, we predict a weaker effect of group size on
140 foraging effort, as estimated by daily travel distance (DTD), in modulars. Comparing groups
141 of different sizes of a given species provides the best test case to assess these ecological
142 costs. We present intraspecific data for Rhinopithecus bieti, a modular taxon, and Presbytis
143 thomasi, a non-modular colobine; these are the only species of Asian colobines for which
144 data on several groups (>3) are available. Additionally, we predict that the percentage of
145 ‘grazing’ foods is higher in modular than non-modular colobines and DTDs are not
146 substantially longer in modulars relative to non-modulars. These latter two predictions are
147 based on the assumption that in order for large groups to form at modest costs, the resource
148 base must consist of superabundant and ubiquitous items such as mature leaves and lichens
149 (Rodman 1988; Kirkpatrick et al 1998), i.e. grazing foods that reduce competition and would
6 150 not force larger groups to exhibit longer DTDs to sustain per capita energy intake of group
151 members (Janson and Goldsmith 1995; but see Snaith and Chapman 2008).
152
153 Methods
154 The evolution of the trait modularity in the Presbytini was reconstructed in MacClade
155 4.07 (Maddison and Maddison 1992). We used different rules to reconstruct character
156 evolution: parsimony, DELTRAN (resolving states that remain ambiguous when using
157 parsimony so as to delay changes), and ACCTRAN (forcing ambiguous reconstructions to
158 occur closer to the root and therefore reducing the number of transitions). In the cladogram of
159 Fig. 2, we consider the colobine social organization states ordered.
160 Information on the variables used here (i.e. social organization, home range overlap,
161 sex ratio, % mature leaves/lichens in the diet, daily travel distance) was obtained from the
162 published literature (and additional unpublished theses and personal communications) and is
163 presented as supplementary data. Populations of colobines in extremely degraded and
164 disturbed habitats (plantations, highly degraded secondary forest) were omitted from the
165 analyses. If a population was represented by two data sets taken at different points in time, we
166 used only the more extensive study. For the variable sex ratio, we used weighted species
167 means, i.e. means weighted by the number of groups studied, due to large differences in
168 sample sizes. For the variables DTD and home range overlap in interspecific comparisons,
169 we used means of population means. Different sample sizes across analyses are the result of
170 missing data. For interspecific regression analyses, all variables (except % mature leaves)
171 were ln-transformed prior to analysis to correct problems of unequal variances in non-
172 phylogenetic analyses and to meet the assumptions of independent contrasts in phylogenetic
173 trees.
7 174 We excluded Semnopithecus from tests of the bachelor threat hypotheses because a
175 previous analysis has already dealt with the effect of conspecific threat on size and
176 composition of Semnopithecus groups (Treves and Chapman 1996). Semnopithecus
177 represents the only taxon of Asian colobines that exhibits a variable social system: mostly
178 large multimale-multifemale groups (mean group size: 27) and some uni-male groups. There
179 are no modular populations in this taxon, which makes it methodologically difficult and
180 biologically unjustified to include Semnopithecus in the analysis, although large multimale-
181 multifemale groups may be functionally analogous to modular societies.
182 Since all species with modular systems also show substantial home range overlap, we
183 used home range overlap as a continuous proxy measure for modularity. Such a continuous
184 variable is better suited for testing comparative predictions than a categorical variable
185 because it provides more fine-grained variation and is more likely to meet parametric
186 statistical assumptions (Nunn 1999; Nunn and Barton 2001). Between-group encounter rate
187 was found to be correlated with home range overlap in this sample of Asian colobines
188 (Spearman rs = 0.935, p < 0.001, n = 11), so there was no need to include encounter
189 frequency as an additional variable (contra van Schaik et al. 1992).
190 Due to their shared ancestry, species values are often not considered to represent
191 independent data points in comparative analyses of cross-species patterns (Abouheif 1999;
192 Harvey and Pagel 1991; Martins and Hansen 1996). This phylogenetic non-independence
193 increases Type I error rates because the degrees of freedom are not properly partitioned
194 (Pagel 1993). We thus controlled for phylogeny by means of the independent contrasts
195 method (Felsenstein 1985), as implemented by the PDAP module (Garland et al. 1999) of the
196 program Mesquite (Maddison and Maddison 2005).
197 The phylogeny used was primarily based on a molecular supertree containing
198 estimates of divergence dates for various nodes (Bininda-Emonds et al. 2007). Since the
8 199 topology is not fully resolved for Asian colobines, additional species (for which data on the
200 variables of interest were available) were added to the tree based on phylogenetic information
201 obtained from other sources (Li et al. 2004; Nadler and Roos 2002; Osterholz et al. 2008;
202 Sterner et al. 2006; Wang et al. 1997; Zhang and Ryder 1998). If unequivocal information on
203 divergence dates from these additional sources could not be extracted, we arbitrarily spaced
204 nodes evenly along branches (cf. Plavcan 2004).
205 Since the independent contrast method is relatively robust to inaccuracies in the
206 available phylogenetic information (branching sequence, branch lengths) and since mostly
207 terminal branches were unresolved, such ambiguities have been found to hardly affect the
208 outcome of the analysis (Martins and Garland 1991). When repeating the contrast analysis
209 under a ‘punctuated evolution’ model, i.e. setting all branch lengths equal to 1, the results did
210 not differ in the level of significance from the ones presented here. Absolute contrasts were
211 also standardized by dividing them by the square root of the sum of the branch lengths. This
212 was done because the further back on the roots of the tree, toward the most primitive
213 character states, the contrasts are more and more removed from the observed values and are
214 estimated through an averaging process. Thus, the estimated primitive characters states were
215 given less weight than the topmost states (Garland et al. 1999; cf. Barrickman et al. 2008).
216 Contrasts were statistically analyzed with least squares regression, and following standard
217 practice, contrasts slopes were forced through the origin (Garland et al. 1992).
218 Comparative analyses were also performed using species data, i.e. without controlling
219 for phylogeny. Both nonphylogenetic and phylogenetic results are reported. We used model I
220 linear regressions to test for relationships between a dependent and an independent variable.
221 Analyses were run in JMP 7 and SPSS 16.0. All probabilities reported are for two-tailed tests.
222 Statistics were considered significant at p < 0.05.
223
9 224 Results
225
226 Historical Origins of Modularity
227 Reconstruction of the social organization of the Presbytini (with Colobini as an
228 outgroup) confirms that a non-modular system was ancestral and modularity is a derived
229 feature (Fig. 2). DELTRAN, ACCTRAN and parsimony all yielded the same pattern.
230 Modularity evolved three or four times independently in the Presbytini: twice in the odd-
231 nosed colobines (only once if we assume a monophyletic relationship for the odd-nosed
232 colobines (Sterner et al. 2006)), once in Presbytis (Presbytis siamensis) and once in
233 Trachypithecus (T. geei and T. pileatus). Modularity was likely lost secondarily in Simias,
234 which has a tiny geographical distribution on the Mentawai Islands, possibly because its
235 groups are very small due to the absence of feline predators or because recent anthropogenic
236 infiltration and hunting on the Mentawai Islands has reduced population numbers of this
237 species to a level where modularity cannot be expressed anymore (cf. Watanabe 1981). Strict
238 modularity is phylogenetically confined to the odd-nosed colobines.
239
240 Bachelor Threat Hypothesis
241 As shown in Figure 3, there was a significant difference in sex ratio of bisexual
242 groups (proxy measure for bachelor threat) between the categorical variables modular vs.
243 non-modular (t test, t = -2.353, p = 0.0290, df = 20). When using home range overlap as a
244 continuous proxy measure for modularity, sex ratio of bisexual groups showed a significant
2 2 245 positive correlation with home range overlap (F1,16 = 5.835, p = 0.0280, R = 0.267, R adj. =
246 0.221). The regression equation would be:
247
248 ln home range overlap = 1.87 + 1.24 x ln sex ratio (Fig. 4a).
10 249
250 After removal of phylogenetic dependence, this relationship became highly significant (F =
251 18.573, p = 0.0005) (Fig. 4b).
252
253 Ecological Constraints on Band Formation
254 We investigated the effect of group size on DTD for several groups of Rhinopithecus
255 bieti and Presbytis thomasi, respectively (Fig. 5). We found a significant positive linear
2 2 256 relationship for P. thomasi (F1,12 = 17.57, p = 0.0013, R = 0.594, R adj. = 0.560) while DTD
257 tended to increase with group size in R. bieti, but not significantly so (F1,3 = 3.73 , p = 0.1490,
258 R2 = 0.554, R2 adj. = 0.406) (see Fig. 5 for data sources). An analysis of covariance was then
259 performed with both species to test if the two slopes were significantly different. The effect
260 of group size on DTD was found to be higher for P. thomasi than for R. bieti (F = 7.68, p =
261 0.0143, df = 1). The two slopes differed by a factor of 29.5; while P. thomasi have to travel
262 another 60 m per additional individual added to the group, DTD increases by only 2 m per
263 individual in R. bieti. The relative ranging cost RRC (Janson and Goldsmith 1995), which
264 measures the increased ranging cost of an additional group member scaled relative to the
265 DTD of a hypothetical group of 1, is 0.083 for P. thomasi and 0.003 for R. bieti.
266 DTD did not differ significantly between modular and non-modular colobines (t = -
267 1.101, p = 0.2909, df = 14). The difference between modular and non-modular species in the
268 percentage of low quality foods in the diet (mature leaves and lichens) was significant (t = -
269 2.240, p = 0.0432, df = 14).
270
271 Discussion
272 The correlations between the suspected number of bachelor males and the prevalence
273 of modularity confirm the prediction of the bachelor threat hypothesis for Asian colobines. In
11 274 addition, there is also ample circumstantial evidence that incursions by bachelors pose a real
275 and significant threat to colobine unit leaders and also females. First, infanticide is a common
276 male reproductive strategy among primates (van Schaik and Janson 2000), and also pays in
277 seasonally breeding colobines via reduction of interbirth interval of the mother (e.g. Borries
278 1997; Cui et al. 2006). Second, takeover and infanticide by putative bachelor males has been
279 documented in several modularly organized colobine societies (e.g. Agoramoorthy and Hsu
280 2005; Qi et al. 2008; Xiang and Grueter 2007). Third, all-male units (AMUs) are an
281 influential part of modular societies and habitually follow the mixed-sex bands and associate
282 with them (Bennett and Sebastian 1988; Grueter and Zinner 2004; Hoang 2007; Kirkpatrick
283 1998; Stanford 1991a; Yeager 1990). Fourth, males respond differently to other OMU males
284 than AMU males. While encounters between reproductive units and non-reproductive units
285 are often characterized by high levels of tension, encounters between OMUs evoke more
286 casual responses (Boonratana 1993; Stanford 1991a; C. C. Grueter, personal observation).
287 Fifth, OMU males exhibit non-aggressive relations with extra-unit males that are known to
288 them, i.e. encountered on a regular basis (Stanford 1991a). In Rhinopithecus bieti, males of
289 different OMUs are consistently in close proximity and tend to be neutral toward each other
290 most of the time unless a male encroaches upon another male’s space (Grueter 2009).
291 The explanatory power of the bachelor threat hypothesis for modular colobines is
292 further bolstered by observations of unit holders actually collectively defending the group
293 against incursions by bachelor males (cf. Rubenstein and Hack 2004). Cases of OMU leaders
294 collaboratively attacking intruding AMU males have recently been reported for a habituated
295 group of Rhinopithecus roxellana (Zhao and Li 2009). The reason why such cases are not
296 more widely reported in the colobine literature may be due the extremely difficult
297 observation conditions that characterize most study sites (poor habituation, dense foliage etc.)
298 and the fact that modular colobines have been the focus of relatively few field studies.
12 299 Even if male cooperation is uncommon in some modular colobine societies, this does
300 not necessarily invalidate the bachelor threat hypothesis. First, it is possible that males of
301 different units do not need to show deliberate coordination against bachelors. Sterck and van
302 Hooff (2000) mention that male Asian colobines “seem neither to check the actions of other
303 males nor to coordinate their behavior with other males actively, [but] they may well act in
304 parallel because similar behavior is triggered by the same stimulus (e.g. (Curtin 1980) for
305 banded langurs)”. Second, even if intentional cooperation is not exhibited by males in bands,
306 a benefit for males may accrue simply for numerical reasons: the probability of being targeted
307 and ousted by bachelors is supposed to decline as units gather in larger bands. This is
308 analogous to the dilution effect, a supposedly adaptive response to predation (Caro 2005;
309 Pulliam and Caraco 1984).
310 The principle of OMU leaders gathering together for safety reason is similar to the
311 acceptance of ‘follower’ males, as found in some OMU-based equid and primate societies. In
312 some equids, male followers at times also help dominant stallions to protect females against
313 harassment by outside males and to hold off outside males from matings with band females
314 (Feh 1999; Miller 1981; Stevens 1990; but see Linklater et al. 1999). In mountain gorillas,
315 follower males can participate in interunit encounters and aid the dominant male in defending
316 the group from potentially infanticidal external males (Harcourt and Stewart 2007; Robbins
317 2001; Sicotte 2001). In hamadryas baboons, there is some evidence that males belonging to a
318 clan cooperate to prevent non-clan males from kidnapping females (Sigg et al. 1982). In
319 chimpanzees, males cooperatively defend estrous females from mating with other males
320 when the number of group males reaches a certain threshold and single males are no longer
321 able to monopolize the females on their own (Watts 1998). In gelada baboons, Dunbar (1984)
322 has suggested that by allowing an extra male to join the harem as a follower, the current
323 leader may reduce the chances of his unit being the target of a takeover attempt by a bachelor
13 324 male and may thus prolong his tenure as a breeding male. Dunbar (1984, p. 177) explains that
325 “the benefits that unit holders derive from accepting a follower have nothing to do with the
326 latter’s playing any active role in supporting the unit leader during takeover attempts by rival
327 males. It seems to work, however, because harems with followers reduce the effective size of
328 the units (i.e., the number of unit females actually bonded with the harem male), thus
329 increasing the females’ loyalty to the leader and reducing the probability of being evicted by
330 other males.” The same reasoning may be appropriate for a modular colobine system.
331 Another factor possibly affecting the formation of bands is kinship among units. A
332 network of (male) kin among those units may facilitate OMUs keeping closer together (cf.
333 Bradley et al. 2004). In proboscis monkeys and capped langurs, one-male units form
334 differentiated relationships in which they tolerate some groups but not others (Yeager 1989,
335 1991; Stanford 1991). Investigating such kinship factors among units in a modular colobine
336 society would lead to a better understanding of how these complex societies operate.
337 The question arises as to whether the multimale-multifemale groups of Semnopithecus
338 represent an alternative solution to the same fundamental evolutionary stimulus, viz.
339 conspecific threat? Treves and Chapman (1996) found partial support for this idea, i.e. when
340 the risk of infanticidal attack from all-male bands was high, groups of Semnopithecus were
341 larger and contained proportionately more adult females, but not males. However, other
342 hypotheses have been proposed, and no consensus as to the functional significance of the
343 dichotomous social organization of Semnopithecus - with some populations showing unimale
344 and others multimale groups - has been reached (Koenig and Borries 2001). While habitat
345 does not appear to have power to explain social structure (Newton 1988), other potentially
346 determining factors have been invoked, viz. population density (Moore 1999; but see Newton
347 1988), the risk of predation (Treves and Chapman 1996; but see Newton 1988), and male
348 monopolization potential of females (Newton 1988; Srivastava and Dunbar 1996), the latter
14 349 being dependent on length of breeding season (Moore 1999; Srivastava and Dunbar 1996). It
350 is also conceivable that these large multimale-multifemale groups are phylogenetically
351 constrained in the Semnopithecus clade.
352 Resource distribution and availability do not appear to have a constraining effect on
353 modularity, but several lines of evidence demonstrate that costs of assembling may be reduced
354 in modular colobines relative to non-modulars. First, modulars include a higher percentage of
355 abundant staple foods of low quality, such as lichens and mature leaves, into their diet than
356 non-modulars. Second, there was no significant difference in DTD between modular and non-
357 modular colobines, despite big differences in mean group size, which is compatible with lower
358 relative ranging costs for species that became modular. Third, intraspecific regressions of
359 DTD on group size for the only two species with the relevant information showed that
360 modulars faced much lower scramble competition costs than non-modulars (Fig. 5). This does
361 not mean that modular colobines do not face scramble competition, because the correlation
362 between group size and DTD in Rhinopithecus bieti was still positive, but rather that the
363 scramble is so weak that even the largest groups of R. bieti have only marginally higher DTD
364 than the largest Presbytis thomasi groups, despite being nearly 40 times larger. This finding is
365 especially compelling since the ratio of females to males in P. thomasi is at the upper range of
366 non-modulars, i.e. P. thomasi would benefit from band formation due to high bachelor
367 pressure, but ecological costs seem to prevent modularity. However, it has to be kept in mind
368 that these conclusions are founded on an analysis of two species only and thus have to be
369 considered provisional. Resource competition in modular colobines is probably more
370 pronounced on ephemeral foods than staple foods, but does not seem to be strong enough to
371 limit group size (Grueter et al. 2009). The predominance of modular societies in other grazers
15 372 such as plains zebras and gelada baboons may also be permitted by low levels of feeding
373 competition.
374 In sum, modular societies in Asian colobines originate from autonomous OMUs that
375 sought aggregation. At least one ecological benefit, namely thermal benefit, did not
376 determine the formation of bands in Asian colobines. While this study did not discount the
377 other ecological theories such as predation avoidance and harvest efficiency on empirical
378 grounds, there is no compelling evidence in favor of them. Nevertheless, more rigorous
379 testing is needed once comparative data become available. We considered the threat of
380 bachelor males as a plausible alternative scenario, which was found to be consistent with all
381 known facts, but needs to be strengthened by further in situ observations. This finding adds to
382 a growing body of evidence showing the importance of conspecific threat as a constraint in
383 driving the evolution of mammalian societal patterns and social strategies (Arnqvist and
384 Rowe 2005; Muller and Wrangham 2009; Nunn and van Schaik 2000; Pradhan and van
385 Schaik 2008). Furthermore, the modular colobines were better able to respond to bachelor
386 threat than non-modulars because the abundant and non-localized resource base of the former
387 keeps foraging costs low and permitted the formation of bands in the first place.
388
389 Acknowledgments
390
391 We thank Craig Kirkpatrick for stimulating discussions and sharing ideas, Karin Isler for
392 assistance with MacClade analyses and Dietmar Zinner, Charlie Nunn and the anonymous
393 reviewers for comments on earlier versions of the manuscript. Financial support was
394 provided by the A.H. Schultz Foundation.
395
396
16 397
398
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656 657 658
659
660
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663
664
665
666
667
668
669
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671
672
27 673
674
675 Tab. 1. Ecological hypotheses for band formation in Asian colobines. ‘Band’ refers to a large
676 social group composed of subunits. Arguments are given in disfavor of the hypotheses and
677 references are listed of studies that have rejected the predictions.
Hypothesis Description Predictions Applicability / Evaluation Localized Highly localized essential or Units should assemble only Modular construction is a resources ephemeral food resources temporally when these relatively persistent feature in such fruit trees attract several resources are available or in at least the strictly modular OMUs or force OMUs to spatially restricted places. colobines (e.g. Kirkpatrick et congregate at such places. al. 1998; Zhang et al. 2006). Harvest Bands form because foraging Individual net food intake Through theoretical modeling, efficiency as a band rather than separate should be higher in bands it has been borne out that group units maximizes individual than in autonomous units or foragers obtain food at lower feeding efficiency by higher when living in rate than solitary foragers minimizing returns to groups than when foraging (Beauchamp 2005). depleted food patches. independently.
Ibid. Subordinate units may experience less competition for access to dispersed profitable patches when separating from the band and foraging independently (Grueter 2009; sensu Harcourt and Stewart 2007).
Modularity should be Band formation is not limited to restricted to populations species inhabiting habitats living in habitats with where food resource slowly regenerating and regeneration time is low. thus depletable foods (e.g. lichens) (cf. Kirkpatrick et al. 1998). Predation Protection from predators is Groups should be A group size benefit (dilution, avoidance an aggregative force for units. sufficiently large to be vigilance) from predation buffered against predator quickly saturates, so bands of
28 attacks. several hundred seem unnecessarily large (Hamilton 1971; Pulliam 1973; cf. Kirkpatrick et al. 1998).
Band formation should be Many tropical langurs live in more common in habitats small isolated OMUs despite with an intact predator the presence of arboreal feline community. predators (e.g. clouded leopards) in these habitats. Between- Units associate with other As a prerequisite for inter- In the genus Rhinopithecus band resource units to avoid displacement at band competition to be (modular), bands have no or competition resource sites. relevant, home range little range overlap and inter- overlap among bands band competition does not should be large. seem to be strong (Bleisch and Xie 1998; Chen et al. 1989; Kirkpatrick et al. 1998). Thermal Bands emerge because The lower the mean annual By comparing average annual benefit individuals in large bands temperature within the habitat temperatures of modular have many partners for natural habitat of a given vs. non-modular colobine huddling and thus gain species is, the higher should species, we found no statistical thermoregulatory benefits. be the prevalence of difference (t test, t = 1.54, p = modular systems. 0.141, df = 18) (this study).
Modular societies should Modular societies are common not exist in tropical in tropical climates. climates, where animals would rarely if ever need to form big huddles to minimize heat loss.
Larger groups should form Rhinopithecus bieti (modular) distinctively during the cold live in a seasonally freezing season. climate, but the bands seem to be equally cohesive year round or even less cohesive during the cold season (Grueter 2009; Kirkpatrick et al. 1998).
Huddling clusters should Since OMUs are discrete social
29 include members of other entities, huddling does not units. involve more than one unit (Chen et al. 1989; Grueter 2009; Qi et al. 2004). 678
679
680 Fig.1. Structure of a modular system, exemplified by snub-nosed monkeys. The illustrated
681 hypothetical band consists of five OMUs and one all-male unit (AMU; a).
682
683 Fig. 2. Colobine phylogeny, indicating the distribution of the three character states as defined
684 in the text. Phylogeny is based on Bininda-Emonds et al. (2007), with terminal branches
685 having been modified after Geissmann et al. (unpublished manuscript), Li et al. (2004),
686 Nadler and Roos 2002, Osterholz et al. 2008, Sterner et al. 2006, Wang et al. 1997, and
687 Zhang and Ryder 1998, where necessary. Note that the phylogenetic relation of the Nasalis-
688 Simias branch with regard to the other colobines differs between the composite estimate of
689 Purvis (1995) and the supertree of Bininda-Emonds et al. (2007).
690
691 Fig. 3. Adult sex ratio (F/M) of bisexual groups compared between modular and non-modular
692 colobines.
693
694 Fig. 4. Association between home range overlap and sex ratio (F/M) in Asian colobines. (a)
695 Species data, (b) independent contrasts.
696
697 Fig. 5. Regressions of group size against DTD for several groups of Rhinopithecus bieti and
698 Presbytis thomasi. Group size refers to band size in R. bieti. The small squares designate R.
699 bieti, the large ones P. thomasi. The following equations were obtained: R. bieti: DTD = 631
30 700 + 2.04 x group size; P. thomasi: DTD = 666 + 60.17 x group size. Data for P. thomasi were
701 taken from Steenbeek and van Schaik (2001), data for R. bieti from Grueter (unpublished
702 manuscript), Kirkpatrick et al. (1998), Liu et al. (2004), Ren et al. (2009), and Xiang (2005).
703
704 Supplementary Data
705
706 List of socioecological traits of Asian colobines used for the analyses in this article.
AF/ DTD Species Soc Org %HR overlap %ML/lichens3 AM1 [m]2
Presbytis comata non-mod 1.9 9 500 6
Presbyis siamensis mod 6.7 52 684 6
Presbytis thomasi non-mod 3.6 41 1070 13.4
Presbytis potenziani non-mod 1.2 34 670 12.1
Presbytis rubicunda non-mod 3.0 12 819 1
Presbytis hosei non-mod 2.5 10 743 5
Trachypithecus auratus non-mod 5.4 23 585 6.7
Trachypithecus obscurus non-mod 2.4 3 559 22
Trachypithecus geei mod 4.9 UNK UNK UNK
Trachypithecus vetulus non-mod 3.3 UNK UNK UNK
Trachypithecus johnii non-mod 3.4 10 UNK 27
Trachypithecus phayrei non-mod 3.5 UNK 961 UNK
Trachypithecus leucocephalus non-mod 4.5 16 UNK 10.5
Trachypithecus pileatus mod 3.7 84 325 42
Trachypithecus francoisi non-mod 1.6 UNK 541 13.9
Simias concolor non-mod 1.9 8 UNK UNK
Rhinopithecus bieti mod 4.1 100 1061 79.7
Rhinopithecus roxellana mod 4.5 100 1721 46.8
Rhinopithecus brelichi mod 2.2 100 UNK UNK
Rhinopithecus avunculus mod 4.8 100 UNK UNK
Pygathrix nemaeus UNK 2.8 UNK UNK UNK
Pygathrix nigripes mod 2.1 10 929 UNK
31 Nasalis larvatus mod 6.4 94 731 1.3
707 1 AF = adult female, Am = adult male.
708 2 DTD = daily travel distance.
709 3 ML = mature leaves (in diet). 710
711 The data were extracted from the following sources:
712 Presbytis comata: Ruhiyat 1983; Presbytis siamensis: Davies et al. 1988; Bennett 1983, 1986; Johns 1983; Presbytis
713 thomasi: Assink and van Dijk 1990; Steenbeek and van Schaik 2001; Sterck and van Hooff 2000; van Schaik et al. 1992;
714 Presbytis potenziani: Fuentes 1994, 1996; Sangchantr 2004; Watanabe 1981; Presbytis rubicunda: Bennett and Davies 1994;
715 Davies 1984; Davies 1987; Salafsky 1988; van Schaik et al. 1992; Waterman et al. 1988; Presbytis hosei: Mitchell 1994;
716 Nijman 2004; Trachypithecus auratus: Kool 1989, 1993; Vogt 2003; Trachypithecus obscurus: Curtin 1980; Trachypithecus
717 geei: Srivastava 2006; Srivastava et al. 2001; Trachypithecus vetulus: Rudran 1973a b; Trachypithecus johnii: Bennett and
718 Davies 1994; Hohmann 1989; Joseph and Ramachandran 2003; Oates et al. 1980; Poirier 1968, 1969a, b, 1970; Tanaka
719 1965; Trachypithecus phayrei: Borries et al. 2004; Gupta and Kumar 1994; Pages et al. 2005; Trachypithecus leucocephalus:
720 Huang and Li 2005; Li and Rogers 2004, 2006; Trachypithecus pileatus: Biswas et al. 2004; Solanki et al. 2007; Stanford
721 1991a, b; Trachypithecus françoisi: Zhou et al. 2006a, b; Simias concolor: Tenaza and Fuentes 1995; Tilson 1977; Watanabe
722 1981; Rhinopithecus bieti: Cui et al. 2008; Grueter 2009; Huo 2005; Kirkpatrick 1996; Kirkpatrick et al. 1998; Liu et al.
723 2004, 2007; Ren et al. 2009; Xiang 2005; Xiang et al. 2007; Yang 2000; Rhinopithecus roxellana: Guo et al. 2007; Hu et al.
724 1980; Kirkpatrick and Gu 1999; Li 2006; Ren et al. 1998, 2000; Su et al. 1998; Tan et al. 2007; Zhang et al. 2006;
725 Rhinopithecus brelichi: Bleisch et al. 1993; Bleisch and Xie 1998; Rhinopithecus avunculus: Boonratana and Le 1998; Dong
726 and Boonratana 2006; Kirkpatrick 1998; Le and Boonratana 2006; Pygathrix nemaeus: Lippold 1977, 1998; Pygathrix
727 nigripes: Eames and Robson 1993; Hoang 2007; Lippold 1998; Rawson, personal communication; Nasalis larvatus:
728 Agoramoorthy and Hsu 2005; Bennett and Sebastian 1988; Boonratana 1993, 2000, 2002; Matsuda et al. 2009; Murai et al.
729 2007; Yeager 1989, 1990.
730
731 The most frequent social system is given.
732 Whenever data on DTD and home range overlap were given as ranges rather than averages, we took the midpoint.
733 Values for the variable ‘sex ratio’ represent species means weighted by the number of groups studied. Values for ‘home
734 range overlap’ represent means of population means.
735 The social organization of Pygathrix nemaeus is treated as unknown since available reports are mixed.
736 For additional information on data extraction criteria, see Methods. 737
738 References
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