Evolutionary Anthropology 16:94–106 (2007)

ARTICLES

Primate Group Size and Interpreting Socioecological Models: Do Folivores Really Play by Different Rules?

TAMAINI V. SNAITH AND COLIN A. CHAPMAN

Because primates display such remarkable diversity, they are an ideal taxon tion and group size. We conclude by within which to examine the evolutionary significance of group living and the ec- suggesting future refinements of both ological factors responsible for variation in social organization. However, as with empirical inquiry and theoretical any social vertebrate, the ecological determinants of primate social variability models that we hope will improve are not easily identified. Interspecific variation in group size and social organiza- our ability to adequately characterize tion results from the compromises required to accommodate the associative and the competitive regime and social or- dissociative forces of many factors, including predation,1–3 conspecific harass- ganization of folivorous primates. ment and infanticide,4–6 foraging competition1,7 and cooperation,8 dominance interactions,9 reproductive strategies, and socialization.10–12 Causative explana- tions have emerged primarily through the construction of theoretical models that EXPLANATORY MODELS OF organize the observed variation in primate social organization and group size rel- PRIMATE SOCIAL ORGANIZATION ative to measurable ecological variation.1,2,13–16 Early assessments of primate soci- oecology relied primarily on correla- In the first portion of this paper, tional analyses to examine the rela- Tamaini Snaith is a Ph.D. candidate in we take a historical perspective, Biology and Anthropology at McGill Uni- tionships between ecological and versity in Montreal. Her research has reviewing the development of exist- social variation, and generally cate- dealt with the behavior, ecology, and con- ing models of primate socioecology. gorized primates according to group servation of orangutans in Borneo and moose in Nova Scotia, and she worked We pay particular attention to the size, the number of males per group, as a conservation biologist and advocate manner in which these models have or broad ecological categories based for the Alberta Wilderness Association. been applied to folivores because, Colin Chapman is a Canada Research on diet, locomotion, and habi- 1,3,18,19 Chair Professor of Anthropology and the recently, contradictions have em- tat. This work provided impor- McGill School of Environment. His current erged between empirical data and tant insights into the variation in pri- research is focused on the ecological determinants of primate behavior and longstanding assumptions about mate behavior and the ecological abundance, emphasizing novel means of food competition in folivores, which conditions associated with various promoting primate conservation. Cur- challenge conventional interpreta- behavioral traits. The research of be- rently, both authors conduct field work in Kibale National Park, Uganda. tions of their competitive regime. In havioral ecologists working on other Departments of Anthropology and Biology, the second part of the paper, we taxa8,9,20–22 provided a strong theo- McGill University, 855 Sherbrooke St. examine how traditional assump- West, Montreal, Canada, H3A 2T7. Phone: retical basis for the development of 514-398-1242, Fax: 514-398-7476, E-mail: tions have led to what has been primate-specific qualitative models [email protected] called the folivore paradox.4,17 We grounded in evolutionary theory. In Department of Anthropology and McGill 14 School of Environment, McGill University, explicitly examine the context within a seminal paper, Wrangham shifted Wildlife Conservation Society, 2300 which this paradox was proposed the focus of primate socioecology in Southern Boulevard, Bronx, NY 10460, and critically examine whether foli- USA. E-mail: [email protected] two ways. First, rather than relying vores experience food competition. on correlational analyses, he used an Throughout the paper, we focus spe- evolutionary approach to generate cifically on ecological variation and hypotheses about the adaptive signif- the consequent expressions of food icance of social organization. Sec- Key words: folivore paradox; group size; social competition. While we recognize the ond, he focused primarily on female organization; socioecology; scramble competition potential importance of predation, relationships as determined by food infanticide, and social factors, no competition. This brought primate VC 2007 Wiley-Liss, Inc. attempt is made to exhaustively socioecological theory in line with DOI 10.1002/evan.20132 Published online in Wiley InterScience review these phenomena or to dis- the basic premise that, for most spe- (www.interscience.wiley.com). cuss their effects on social organiza- cies, female behavior is affected by ARTICLES Folivore Group Size and Socioecology 95

Box 1. Types of Food Competition2,31

Between-group contest (BGC) sity. The effects of BGS are pre- take the form of aggression, dis- occurs when territories or food patches sumed to be independent of group placement, or avoidance. can be cooperatively defended by size and to have little effect on Within-group scramble (WGS) group members. This type of competi- social behavior. occurs due to the limited nature of the tion should favor larger or more aggres- Within-group contest (WGC) food supply, which must be shared sive groups that can supplant or occurs when food is distributed so among group members. Competition exclude smaller groups from feeding that it can be monopolized or increases in intensity with group size sites. defended, resulting in the develop- and smaller groups are favored. Be- Between-group scramble (BGS) ment of dominance hierarchies, dif- cause feeding opportunities are re- results from the common use of ferential access to resources, and duced equally for all group members, food resources by all groups or skewed energy gains. Behavioral WGS is unrelated to the development individuals, and increases in inten- consequences include direct con- of dominance hierarchies and does not sity with increasing population den- tests over access to food and may lead to skewed resource acquisition.

ecological variables and food com- ability to defend a home range of vided conceptual clarity in subse- petition, while males are primarily appropriate size (in territorial spe- quent models. The type and intensity affected by mating competition and cies) will ultimately constrain group of food competition have important the distribution of receptive fe- size. Non-female bonded species implications for group size, social males.8,20,23 Female food competi- were classified into two categories. behavior, dominance relationships, tion, as the ultimate evolutionary One category includes species that and dispersal patterns. Depending on force influencing primate social orga- rely almost exclusively on high-qual- the distribution and abundance of nization, has provided the funda- ity, patchy resources and display food resources, individuals in groups mental starting point for all subse- short-term variation in group size so will experience either contest or quent models. that individuals can respond to fluc- scramble competition, or both. When Wrangham14 proposed an ecologi- tuations in food availability and individuals or groups can exclude cal mechanism for the formation of competition intensity, as do chim- others from resources, contest com- female-bonded primate groups; spe- panzees (Pan troglodytes) and spider petition results in differential access cifically, females will live in groups monkeys (Ateles spp.). The second to food and ultimately leads to when the benefits of cooperative category includes those whose pre- skewed fitness. Scramble competition resource defense outweigh the costs ferred foods occur in low-quality uni- occurs because all individuals must of within-group feeding competition. form patches with a large number of forage from the same limited Females will form bonds with their feeding sites (i.e., leaves, particularly resource base and results in equally relatives to cooperatively defend mature leaves), and thus live in co- reduced feeding opportunities for all access to food resources. Large hesive groups with little or no feed- individuals. Because the cost of groups will out-compete smaller ing competition. Many non-female scramble competition intensifies as groups and obtain greater fitness by bonded folivores were placed in this groups grow larger, within-group excluding neighboring groups from category. scramble competition is expected to food sources. This requires that By highlighting the social conse- impose a limit on group size, while high-quality food is distributed in quences of food competition, Wrang- contest competition between groups discrete, defensible patches, and that ham14 refocused the attention of pri- may favor larger groups.14,31 fallback foods (those eaten when matologists. Empirical work has sup- Various authors built on Wrang- preferred high-quality foods are un- ported the importance of between- ham’s work to make predictions about available), occur in large, uniform group competition, among other fac- the outcome of competition on group patches that minimize within-group tors, in determining group size and size and social relationships.2,15,16,32 competition. When feeding sites social organization among prima- van Schaik2 modified Wrangham’s within food patches are limited or tes,24–26 birds,22 carnivores,27 and model, suggesting that predation risk vary in quality, competition within humans.1 Over the next decade, a was the ultimate factor forcing females groups will lead to the formation clearer understanding of food com- to live in groups despite the costs of female dominance hierarchies. petition was developed, which led to imposed by feeding competition. Build- For these female-bonded species, expanded ecological models of pri- ing on previous work,1,13,14 van Schaik between-group competition will mate social organization. Building argued that the costs of within-group select for group formation and create on the work of population and be- competition far outweigh any advan- a selective advantage for larger havioral ecologists,28–30 Janson and tages resulting from communal groups, while within-group competi- van Schaik2,31 defined four types of resource defense and that resource tion (in nonterritorial species) or the food competition (Box 1) that pro- defense cannot be invoked as the pri- 96 Snaith and Chapman ARTICLES mary selective force for grouping. Rather, the threat of predation puts a Box 2. Behavioral Indicators of Food Competition15 lower limit on group size, while within- group food competition sets the upper limit. If food is uniformly distributed in Type of Competition Behavioral Indicator small patches of even quality that can- Between-group contest Between-group aggression among not be monopolized, or in very large females patches where the whole group can feed, then competition will be by Between-group scramble Positive relationship between home scramble. Female fitness will be range size and group size affected primarily by group size and Within-group contest Strong female dominance individuals will not be able to increase hierarchies food acquisition through overt behav- iors. If food occurs in well-defined, de- Within-group scramble Positive relationship between day fensible patches that vary in quality range (daily travel distance) and and are not large enough for all group group size members, then contest competition will Negative relationship between occur within groups. If high-quality female reproductive rates and food is clumped and patches are large group size enough for all group members, then between-group competition will be im- portant. and ecological cost of dispersal may act tion. Notably, however, Isbell raised van Schaik outlined a series of pre- as a major determinant of social orga- the possibility that ranging and dictions regarding female dispersal nization, proposing that when food is group size may be poor indicators and social relationships under various clumped, both WGS and WGC occur of competition among folivores and competitive regimes. This model was and, when food is dispersed, neither that previous attempts to measure among the first to draw a sharp distinc- occurs. In constructing this model, these variables may have been con- tion between frugivores and folivores Isbell15 provided valuable methodologi- founded by food availability. This in terms of food distribution, competi- cal clarification by explicitly defining foresight is now proving to be very tive regime, and social outcomes. five behavioral indicators of food com- important. Within groups, folivores were classified petition (Box 2), which can be used to Developed alongside these models as scramblers and frugivores as con- assess the competitive regime of a spe- was one that simply proposed to testers, while between-group contests cies. Interestingly, although separate explain variation in group size. The were assumed to occur only among indicators were proposed for contest ecological constraints model, or frugivores. This distinction has been and scramble competition, Isbell15 scramble competition hypothesis, maintained in the literature and has linked them together by presenting suggests that group size is a function been amplified so that applications of data demonstrating that they covary; of travel costs.34–37 Within-group some later models assume that foli- that is, among species having home competition is associated with in- vores experience no feeding competi- ranges that increase in size with group creasing day range because when 15 tion at all. size, females are aggressive between food is patchy, larger groups will 16 Sterck, Watts, and van Schaik groups. Similarly, among species with deplete patches more quickly, indi- expanded van Schaik’s model to ex- strong female dominance hierarchies, viduals will obtain less food per plicitly integrate social variables and day range (daily travel distance) patch, and groups will have to visit to define more clearly the possible increases with group size. In contrast, more patches in a day.38,39 The ener- social outcomes. By incorporating species with weak or no female domi- getic cost of travel between food the effects of male behavior (particu- nance hierarchies demonstrate no rela- patches is the mechanism whereby larly sexual coercion and infanti- tionship between day range and group scramble competition imposes a cost cide), habitat saturation, and the size. This is an important point because on individuals and limits group size. cost of dispersal, along with preda- the model precludes the possibility of The model is well supported by tion and food distribution, this scramble competition without contest empirical data, particularly among model seems to explain more of the competition. The model does not allow frugivorous primates that compete observed variation in primate group- the possibility that foods may be limit- for patchy, high-quality food resour- ing patterns and social organization. ing but not defensible, or patchy but ces.34,35,40–43 Variation in group size With respect to folivores, Sterck, not monopolizable and that competi- is not a simple function of food Watts, and van Schaik16 suggested tion could be by scramble alone, as sug- abundance, however, but is a re- that infanticide in particular may gested in earlier models.2,14 sponse to the interaction of the size, have important social consequences Furthermore, Isbell15 presented density, and distribution of food for some species. empirical data from a wide range of patches as well as individual differ- Isbell15 and Isbell and Young33 studies to demonstrate that many ences in energy budget, travel costs, advanced ideas about how the social folivores experience no food competi- and foraging strategy. Nevertheless, ARTICLES Folivore Group Size and Socioecology 97

Figure 1. Black-and-white colobus monkey, Colobus guereza, from Kibale, Uganda. existing evidence clearly demon- competition within folivore groups is flat relationship between group size strates i) the cost of grouping to indi- inconsequential and that populations and day range, in combination with viduals, ii) the limiting effect of food and groups are not limited by the the longstanding assumption that competition on group size, and iii) availability of food (but see Koenig leaf resources are abundant and the mechanism behind the relation- and colleagues26 and Borries46). This evenly dispersed, has been used to ship between group size and day inference is based primarily on stud- infer that within-group food compe- range. While acknowledging that ies that have found no relationship tition is weak or absent among foli- observed group sizes will be con- between group size and day range vores.4,14–16,33,37 founded by variables such as preda- among folivores. For example, Clut- Given this assumed reduction in tion risk, resource defense, and mat- ton-Brock and Harvey3 found that feeding competition, folivores are ing strategies, the ecological con- feeding group weight was not related theoretically free to form larger straints model proposes that the to day-range length across diurnal, groups. If protection from predation upper limit on group size is set by arboreal folivore genera. Similarly, is a major aggregative force,1,2,10,13 the increasing costs of travel im- Yeager and colleagues47,48 found that then folivores should take advantage posed in larger groups. The applica- across 17 Asian colobine species, day of this reduction in feeding competi- tion of this model to folivores has range did not increase with increas- tion to form large groups. However, rarely been examined, but see Gilles- ing group size. More specifically, many folivores live in surprisingly pie and Chapman44 and Ganas and early data for red colobus (Proco- small groups relative to similarly Robbins.45 lobus rufomitratus tephrosceles)in sized frugivores, which should be Kibale, Uganda, showed no relation- more constrained by the patchy dis- ship between group size and day tribution of fruit.37,51 This apparent range.49 More recently, Fashing50 contradiction has been referred to as THE FOLIVORE PARADOX found no relationship between group the folivore paradox.4,17 In applications of socioecological size and day range across five groups Social factors, such as the risk of models, many authors have implic- of black-and-white colobus (Colobus infanticide, have been invoked to itly or explicitly assumed that food guereza see Fig. 1). In general, the solve the problem. For example, 98 Snaith and Chapman ARTICLES

Crockett and Janson51 found that the interpretations of primate socioecol- space and time, and vary in nutri- rate of infanticide increased with ogy inadequately characterize the tional quality.54,57–60 Thus, they may group size in red howlers (Alouatta competitive regime of folivores, and provide the ecological conditions typ- seniculus), but only until a group that, although social factors are no ically associated with food competi- was large enough to create paternity doubt also important, the folivore tion. It is probably only mature confusion; at that point, WGS be- paradox may be resolved for some leaves that are distributed super- came more costly. These authors species on ecological grounds. abundantly and continuously, and suggested that infanticide avoidance even these vary dramatically in nutri- could constrain group size below the tional quality. level where WGS imposes a cost. Koenig25 and Koenig and col- Steenbeek and van Schaik4 suggested Folivore foods vary in leagues26 have demonstrated that that among Thomas’ langurs (Pres- distribution and quality forest-living hanuman langurs prefer- bytis thomasi),4 group size was lim- entially exploited mature leaves that Folivores have traditionally been ited by the risk of infanticide occurred in low-density clumps that defined as those primate taxa with because larger groups were more at were not large enough for all group morphological adaptations special- risk of male takeover. Although de- members to feed simultaneously, and ized for the efficient digestion of monstrable effects of WGS were were higher in protein and soluble leaves.53 A significant proportion of observed (day range increased with sugar than other available foods. their diet was thought to be com- group size and females in larger Black-and-white colobus (C. guereza groups ate less fruit and more see Fig. 1) in Kibale are among the leaves) the authors concluded that most highly folivorous primates WGS was not limiting group size known, and yet they are selective eat- because dietary switching was mar- Recent evidence ers; they more frequently choose ginal and there was no effect on ac- young than old leaves, select certain tivity budget or birth rate. Koenig suggests the need to tree species, alter their range use to and Borries17 found that both feed- reassess the assumption obtain certain foods, and eat foods ing competition and infanticide risk of varied nutritional content.61–63 constrained group size in hanuman that folivores rely on Similarly, C. guereza and A. palliata langurs (Semnopithecus entellus): As ubiquitous and evenly do not forage continuously as they group size increased, female nutri- move through the canopy, but feed tional condition was compromised, distributed food only in certain trees, often traveling birth rates decreased, and the risk of resources of relatively directly from one source to 59,61 infanticide increased due to immi- low and uniform another. Finally, for many foli- grating males. However, Treves and vores, mature leaves are heavily con- Chapman52 found that infanticide nutritional quality. It is sumed only when other foods are avoidance did not limit group size in now clear that folivores scarce.48 These studies suggest that different populations of hanuman the simple designation ‘‘folivore’’ is langurs, but that increasing group feed selectively and that insufficient for characterizing the size may have been a counter-strat- their food resources vary diet of primate species26,60 or for egy to prevent takeovers and infanti- making behavioral inferences. cide. The available evidence indi- in quality, availability, cates that in some populations in- and spatial distribution. fanticide may constrain group size, but might not provide a complete so- Folivores may deplete patches lution to the folivore paradox. Fur- of food thermore, the data do not rule out the possibility that ecological factors posed of leaf matter. Recent evidence An important assumption underlying also play an important role in limit- suggests the need to reassess the current interpretations of competi- ing folivore group size in some pop- assumption that folivores rely on tion among folivores is that they do ulations. ubiquitous and evenly distributed not deplete food patches. This food resources of relatively low and assumption necessarily underlies the uniform nutritional quality. It is now idea that folivores do not need to Do Folivores Experience Within- clear that folivores feed selectively increase day range to compensate for and that their food resources vary increasing patch depletion rates in Group Scramble Competition? in quality, availability, and spatial larger groups and thus do not experi- Nine lines of evidence suggest that distribution. Many folivores pri- ence scramble competition. However, folivores experience within-group marily select high-quality young a recent study found that red colo- scramble competition and that group leaves, seeds, flowers, and unripe bus monkeys functionally depleted size may be ecologically constrained. fruits.26,48,54–56 These resources are patches of high-quality foods (young This evidence implies that current often patchily distributed in both leaves) and that patch occupancy ARTICLES Folivore Group Size and Socioecology 99 time was related to the size of the large groups of more than 300 indi- lier studies that lacked ecological feeding group and the size of the viduals.72 This has been attributed to controls must be reassessed. patch.64 Similar patch-size effects the almost unrestricted availability of have been demonstrated for howling unusually high-quality mature leaves monkeys.43,65 If patches are depleted that are a source of high protein and Day range may be related to more quickly by larger groups, day low fiber. However, this result must food availability range is expected to increase. How- be interpreted with caution because ever, this relationship may not fiber content was determined using a Several studies have found that foli- always be simple; alternate responses different technique than those used vore groups increase day range during may exist. For example, if larger in other studies. Furthermore, Dun- periods of food scarcity or in areas groups cannot compensate for in- bar73 reported that C. guereza group with lower food availability (G. berin- 45 74 75 creased depletion rates by increasing size was related to territory quality. gei, C. satanas, C. angolensis ), travel distance, they may increase Groups permanently fissioned into presumably due to the need to group spread to maintain fewer indi- smaller groups when group size increase travel between patches. This viduals per patch.43,64–66 Alterna- exceeded 10 trees per individual and can be interpreted as an effect of tively, individuals may deplete territory size could not be increased. scramble competition because, if patches further, possibly by feeding These results suggest that folivore group size is constrained by local eco- on less desirable plant parts. This group size may be ecologically logical conditions, then a given group idea is based on the logic of Char- constrained and that large groups might be expected to respond to tem- nov’s67 marginal value theorem, form only when food conditions poral fluctuations in food availability which proposed that giving-up times mitigate the costs of within-group by increasing its range when food should occur after more depletion (at competition. becomes scarce. However, other stud- a lower intake rate) when the time ies have documented either no rela- 50 required to find another food patch tionship (C. guereza ) or the reverse 76 is high. There has been no examina- pattern (C. satanas ). Careful exami- tion of whether folivores use such Day range may be related to nation of the relationship among food abundance, the distribution of food compensatory measures. However, group size the observations that folivores patches, and ranging behavior is demonstrably deplete patches and As described, evidence for the absence required to clarify these patterns. that patch size is related to feeding of scramble competition among foli- Relationships between food abun- group size are consistent with the vores comes primarily from studies dance and day range are likely to be assumptions of the ecological-con- that have found no relationship confounded by food distribution. For straints model and suggest that WGS between group size and day range, example, some groups may travel long occurs among folivores. and is based on the assumption that distances to reach specific resour- 50,62,77,78 folivores rely on ubiquitous and ces or may change their diet evenly distributed food resources. to rely on more evenly distributed 48 Group size is related to habitat However, using these studies3,47–50 to foods during periods of scarcity. quality infer that there is no within-group competition is problematic because Fission-fusion occurs It has recently been demonstrated they generally lack sufficient controls that folivore group size can be pre- for ecological variation through time, Studies have found that some foli- dicted by habitat variables. For exam- among study groups, or across spe- vore species exhibit fission-fusion ple, across the geographical range of cies. If group size can be adjusted to behavior, with large groups tempo- red colobus, group size tended to be ecological conditions, then scramble rarily dividing into smaller foraging larger in rainforests and moist wood- costs can be avoided, negating the groups that vary in size and compo- lands than in drier seasonal habi- need to increase day range. Ecologi- sition.48,54,70,72,79,80 Studies suggest tats.68,69 Across 10 sites, red colobus cal variation can thus confound cor- that this pattern occurs in response group size ranged from 7 to 83 indi- relational studies, making it difficult to low food availability associated viduals (n ¼ 60) and was affected by to interpret previous comparisons with low tree density, particularly in the tree density, degree of deciduous- across groups, and especially across degraded habitat. Such short-term ness, degree of forest disturbance, species. Several recent studies that variation in group size is a well- and forest block size.70 Similarly, controlled for ecological variation documented response to variable ec- across four study sites in Kibale, found that day range did increase ological conditions among frugi- groups were larger where food-tree with group size for some folivores vores, including chimpanzees,40,42 density was greater.44,71 Furthermore, (Gorilla beringei,45 P. tephrosceles,44 bonobos (P. paniscus),11 orangutans although black-and-white colobus P. thomasi4). If folivore day range (Pongo pygmaeus),12,81 and spider monkeys typically form much smaller has the potential to be affected by monkeys.82,83 This strategy is advan- groups than often-sympatric red colo- group size in the manner suggested tageous for individuals that rely on bus, in Nyungwe, black-and-whites by the ecological constraints model, patchy and unpredictable food re- (C. angolensis) form exceptionally inferences drawn on the basis of ear- sources because the ability to adjust 100 Snaith and Chapman ARTICLES group size allows greater flexibility increasing food intake to compensate apparent absence of a group-size in response to ecological conditions, for increasing energetic costs, which effect. Koenig25,26 documented linear and can mitigate the costs of food may effectively prevent folivores from dominance hierarchies within groups competition. increasing day range as group size of hanuman langurs that fed on high- increases, even if food competition quality clumped resources that were intensifies. This may ultimately result too small for all group members. Reproductive success is related in compromised nutrition, fecundity, Higher-ranking females attained to group size and birth rates. Measures of female higher net energy gain and were in the reproductive success and hormonal best physical condition, indicating There is evidence that female repro- markers of fecundity may provide im- WGC. Furthermore, between-group ductive success may be compromised portant indices of within-group com- differences in condition indicated as group size increases, presumably petition costs when changes in day BGC. Remarkably, the benefits of BGC because increasing food competition range are not observed. were shown to compensate to some leads to nutritional stress. This rea- degree for the demonstrated costs of soning is based on the relationship WGC and WGS, with the result that between female nutritional status ...folivores engage in females in mid-sized groups were in and fecundity, birth rate, and early the best physical conditions. infant survival. There is a very clear contests for food both Some populations of black-and- causative chain linking energy bal- within and between white colobus monkeys rely on fruit ance to fecundity in humans and groups, challenging the for some portion of their diet and apes,84,85 as well as a documented both males and females may partici- relationship between female nutri- longstanding notion that pate in food defense.93 Several tional status (food intake) and both their diet is not worth authors have concluded that in more birth rate and early infant survival in leaf-dependent populations of black- many primates.10,86–89 Although care- fighting over and raising and-white colobus, males competi- ful empirical work is required to sep- further questions about tively defend food resources as an arate the effects of compromised fe- indirect means of defending access to cundity from those of infanticide,51 the apparent lack of females.50,61,62,94 A dominance hierar- there appears to be a group-size dominance relations in chy between groups has been demon- effect on birth rate in folivores. strated for C. guereza at Kibale.62,63 Gorillas in larger groups spent more some species. Although Dominant groups roared more, won time feeding, suggesting a social for- further investigation is more fights, were avoided by subordi- aging cost.90 Struhsaker and cow- nate groups, and maintained core orkers70 found that habitat quality certainly required, the areas with food resources of greater was the most important factor affect- findings reviewed here quantity and quality. This case is par- ing birth rate across 19 groups of red suggest that group size ticularly interesting because this pop- colobus. Koenig17,25 found that as ulation is highly folivorous,61,62,95 group size increased, female nutri- is probably constrained suggesting that leaves are indeed tional condition was compromised by ecological factors for worth fighting over. In general, this among hanuman langurs. Dunbar73 new evidence indicates that folivore documented the same relationship some species of groups may compete to monopolize across four populations of C. guereza folivores... access to food sources even without and suggested that stress and compe- overt fighting or displacements and tition led to reproductive suppression without strict territoriality. As sug- in larger groups. More generally, van Food-related contest competition gested by Wrangham,14 avoidance is a 10 Schaik demonstrated that folivore occurs possible manifestation of contest birth rate (number of infants per competition in primates. Dominant female) decreased with increasing Recent research suggests that food- groups or individuals may maintain group size, and that this relationship related contest competition occurs preferential, if not exclusive, access to was stronger for folivores than frugi- both within and between some groups the best resources simply because vores. However, there is disagree- of folivores. We believe that this find- they are avoided by subordinate ment regarding this use of unad- ing is important for two reasons. First, groups or individuals. justed birth rates.51,87 it challenges previous notions that foli- This effect may be related to the vores generally do not or cannot energetics of a folivorous diet. Due to engage in contests for food. Second, it Population density is related to their dietary specialization for the raises the possibility that the benefits habitat quality or food availability digestion of low-quality foods, foli- of BGC compensate for the costs of vores must devote a large portion of WGS or WGC in some larger folivore Folivore biomass can be predicted by their time to resting and digesting.91,92 groups,14,32 which may lead to the the distribution of mature leaves This may prevent individuals from appearance of no competition and the with a high protein-to-fiber ra- ARTICLES Folivore Group Size and Socioecology 101 tio.72,95–98 Although this does not directly suggest that there will also Box 3. Expanded List of Behavioral Indicators be constraints on group size, it does of Food Competition provide further support that folivores may be limited in important ways by the quality, availability, and distri- Type of Competition Behavioral Indicator bution of food resources, and sug- gests that the potential for food com- Between-group Food-related between-group aggression petition exists. Previous assumptions contest involving females and/or males that folivore food resources are Between-group dominance hierarchy nutritionally uniform and not limit- Between-group displacements or ing have formed the basis for general avoidance inferences about food competition in Between-group Positive relationship between habitat folivores. scramble quality and population density Within-group Female dominance hierarchies DISCUSSION contest Food-related within-group aggression, Folivores have traditionally been avoidance, displacements and/or seen as living without food competi- agonistic alliances tion or social stratification within or Rank-related skew in food acquisition, between groups, but this was largely nutritional status, fecundity, and based on the notion that they reproductive success exploited ubiquitous and invariable Within-group Positive relationship between group size food sources. These assumptions scramble and day range and/or home-range size have been implicitly or explicitly and/or habitat quality incorporated into applications of Negative relationship between habitat socioecological models and have led quality and day range and/or home- to the folivore paradox. However, range size recent empirical data are increas- Fission-fusion related to temporal ingly exposing folivores as competi- variation in resource availability tive and socially variable. Many foli- Positive relationship between patch vore populations exploit high-quality, depletion rate and group size, and/or patchily distributed, temporally vari- negative relationship between depletion able food resources, and display rate and patch size many of the expected responses to Positive relationship between group size food competition. The emerging pic- and normalized group spread, and/or ture is complex. Folivore strategies nonpositive relationship between total vary across populations and species, group size and feeding group size indicating adaptive flexibility in Longer giving-up time in larger groups response to local conditions. Foli- and/or poorer habitat vores appear to be subject to the Negative relationship between group same ecological constraints as frugi- size and female nutritional status, vores and may respond with similar fecundity, and reproductive success competitive regimes when food con- ditions are similar. However, rather than simply increasing day range to compensate for increasing group ings reviewed here suggest that competitive regime of leaf-eating size, folivores may display alternate group size is probably constrained monkeys. responses to the costs imposed by by ecological factors for some spe- In practical terms, we believe there scramble competition or may incur cies of folivores just as has been are two areas where efforts are required fitness costs in larger groups. Per- demonstrated for many frugivores. to provide theoretical clarification and haps most surprisingly, folivores en- Undoubtedly, folivore group size is direction for empirical research. First, gage in contests for food both within also influenced by social factors like the terms used to describe resource and between groups, challenging the infanticide. The interaction of social characteristics and the methods used to longstanding notion that their diet is factors and ecological constraints measure them need to be consistently not worth fighting over and raising requires further investigation. These and explicitly defined,66,99 particularly further questions about the apparent results provide important insights if resource characteristics are used to lack of dominance relations in some into the folivore paradox and may be infer particular competitive regimes. species. Although further investiga- used to refine the assumptions Second, a wider range of indicators of tion is certainly required, the find- behind current interpretations of the food competition, including social, be- 102 Snaith and Chapman ARTICLES

Figure 2. Female aggression during between group encounters as illustrated by female Hanuman langurs (Semnopithecus entellus) from Jodhpur, India. Photo by Carola Borries. havioral, and energetic, needs to be rec- between preferred and fallback tion, and identified measurable be- ognized. foods, but that both may influence havioral indicators by which the The abundance and distribution of social organization. That primates competitive regime of a species can food determines the type, intensity, can modify their feeding strategies in be assessed. It is now becoming and social outcomes of feeding com- response to food availability, exploit- increasingly apparent that primates petition. However, the distribution ing different foods with different possess a suite of responses to food of food varies in a number of inter- nutritional and distributional char- competition and that any single acting dimensions and on many acteristics at different times, may be index may be confounded by a vari- scales. Wrangham14 wrote that BGC a major issue affecting our ability to ety of ecological and social factors. requires that high-quality food is construct realistic models. Here and in Box 3 we propose an distributed in discrete, defensible In the 1980s and 1990s, the work expanded set of behavioral indicators patches, and that fallback food of Wrangham,14 van Schaik,2 of competition. The necessity of occurs in large, uniform patches. Isbell,15 Sterck,16 and others was incorporating multiple indices of This is a complex statement that in- instrumental in defining primate competition into both theory and corporates five separate issues: food competitive regimes and highlighting empirical studies was highlighted by source size, quality, patchiness, de- the ultimate importance of ecological our exploration of the folivore para- fensibility, and variability. Separat- factors in determining the adaptive dox, where failure to document the ing these ideas, clarifying the spatial strategies of individuals and the con- simple expectation of increasing day and temporal scales at which they sequent social organization of range with increasing group size led operate, and standardizing measure- groups. Perhaps most critically, these to premature conclusions about food ment methods will go a long way to- authors emphasized the importance competition. ward clarifying ecological measures of applying clear definitions of the The most commonly used evidence and their competitive outcomes in types of food competition experi- of food-related between-group contest future models. Furthermore, Wrang- enced by individuals in groups, made competition has been female aggres- ham drew attention to the need to predictions regarding the social and sion during between-group encoun- recognize not only the difference behavioral consequences of competi- ters (see Fig. 2)2,14,15,100 and was the ARTICLES Folivore Group Size and Socioecology 103 indicator originally proposed by Isbell or the ability to occupy the best feed- insufficient for describing the com- (see Box 2) to measure this phenom- ing sites). For example, it has been petitive regime of a species. enon. This follows from sexual selec- shown that there may be a demon- Based on the issues addressed in tion theory,23 which suggests that strable WGC effect on food intake this paper, Figure 3 outlines a work- because female reproductive success and reproductive success without the ing-version model of the potential is limited by access to resources, expected agonistic alliances and nep- competitive outcomes of variation in females should compete for and otistic affiliative patterns25 or with- resource characteristics. The logic defend food, while males should com- out clear behavioral contests over and predictions of this model are pete for and defend mates. However, relevant food items.89 Measures of essentially no different from those of a lack of female participation in birth rate and body condition have van Schaik2 or Wrangham.14 We between-group encounters should not the additional advantage of being attempt to build on these models by be used as evidence that BGC is not more direct indicators of fitness and, offering a more detailed tool for related to food. Males may also partic- if they can be related to differences addressing the multidimensional na- ipate in BGC in defense of food in rank, may provide an index of the ture of ecological variation and possi- resources as an indirect means to ultimate effects of food competition ble competitive outcomes. The avail- defend access to females.8 Further- on the reproductive success of indi- ability, distribution, size, quality, and more, overtly aggressive between- viduals.25 contestability of food resources are group interactions are not required; A positive relationship between addressed as separate ecological vari- avoidance behaviors may also indi- day range and group size has long ables that can vary independently of cate BGC.14,100 been used as the primary indicator one another. There are no a priori Between-group scramble competi- of within-group scramble competi- assumptions about the mutual exclu- tion results from the common use of tion. However, the relationship sion of different types of competition. food resources by all groups or indi- between day range and group size For example, WGS may occur alone viduals; it can thus occur only when can be obscured by ecological varia- or along with BGC and/or WGC. groups occupy overlapping ranges. tion. Moreover, increasing day range When the empirical evidence pre- In habitat of constant quality, BGS is not the only possible behavioral sented here regarding the distribu- will increase in intensity with response to scramble competition in tion, quality, and abundance of foli- increasing population density. Ear- groups. Group size itself may be vore foods is applied to this model or lier work15,87 suggested that an constrained by local habitat quality, to previous models, it leads to the pre- increase in home-range size as a so that individuals may avoid the diction that many folivores will com- result of an increase in group size need to increase day range. Further- pete by scramble and/or contest. could be used to indicate BGS. How- more, within groups, individuals Perhaps the most important devel- ever, because between-group scram- may compensate for temporal fluc- opment presented here, from the ble is an effect of population density tuations in competition intensity perspective of understanding ecologi- and is independent of group size, caused by ecological variation by cal constraints on folivores, is the this is not an appropriate measure. adjusting day range through time or distinction between patchy (that is, Rather, a positive relationship by fissioning. Individuals may also depletable) and continuous food dis- between population density (cumula- avoid the travel costs associated tribution at the second level of classi- tive group size) and habitat quality with increasing day range by alter- fication. This allows for the possibil- indicates that BGS competition ing group spread or patch depletion ity of WGS without contest competi- occurs. thresholds and giving-up times. If tion. Scramble can still be important Female dominance hierarchies individuals are unable to compen- when food is neither variable in qual- have traditionally been used as the sate for grouping costs, then fitness ity nor defensible, a likely scenario primary indicator of within-group will decrease in larger groups. Such for many folivores. We provide contest competition. Because contest considerations substantially broaden examples of folivore populations on competition results in skewed energy the list of potentially observable as many branches as possible, in- acquisition,2,9,31 interindividual dif- indicators of within-group scramble cluding branches representing com- ferences in fitness, as indicated by competition. petitive regimes that have tradition- skew in birth rate, body condition, Expanding the list of acceptable ally been reserved for frugivores. and other physiological measures indicators of food competition pro- Further research is required to deter- may also indicate WGC. Such meas- vides measurable, quantifiable varia- mine whether the ideas presented in ures must be used with care because bles for field studies and may provide Figure 1 are a useful and accurate individual differences in fitness will direction for the development of way to depict the ecological pres- be affected by many factors such as hypotheses that will further our sures influencing the evolution of genetic and ontogenetic variation. understanding of primate socioecol- primate social organization. Nevertheless, these measures may ogy. Furthermore, by constructing The evidence presented here sug- prove useful in cases where overt this list we acknowledge that prima- gests several profitable directions for contests and dominance hierarchies tes may employ a variety of possible future field research. First, it is im- are rare or difficult to observe (for responses to food competition and portant to understand individual be- example, subtle avoidance behavior that univariate analyses will often be havioral strategies. Data regarding 104 Snaith and Chapman ARTICLES

Figure 3. Working model of how resource abundance and distribution affect competitive regime in primates. Legend: BGS: Between- group scramble competition; BGC: Between-group contest competition; WGS: Within-group scramble competition; WGC: Within-group contest competition. the activity budgets, nutrient gain, quality within and between patches increasing our understanding of the and reproductive success of recogniz- and through time, patch size relative adaptive significance of particular able individuals in groups of differ- to group size, and patch attributes competitive regimes and the selective ent sizes are required to quantify the such as contestability. Because these forces shaping primate food competi- fitness costs of food competition. factors are presumed to be of pri- tion and social organization. Second, attention should be focused mary importance in determining the on subtle expressions of contest com- nature of within- and between-group ACKNOWLEDGMENTS petition, such as avoidance or the competition, we need to investigate consistent attainment of better feed- their social outcomes in hypothesis- This research was funded by the ing sites by certain individuals or driven field studies. Canadian Research Chairs Program, groups, and whether these have fit- It is unlikely that any model will Wildlife Conservation Society, Natu- ness consequences. Third, to unravel ever capture the entire range of ral Science and Engineering how primate social organization is social variability among primates, Research Council of Canada, shaped by ecological conditions and and we recognize that our focus on National Science Foundation, and whether different species and popu- feeding competition captures only the Tomlinson Fellowship Trust. lations respond in the same manner part of the puzzle. Many other fac- Andre Costopoulos, Anthony DiFiore, to ecological variation, we need tors, including predation, infanticide, Carolyn Hall, Stacey Hodder, Mitch quantitative ecological data based on dispersal costs, and social dynamics Irwin, Andreas Koenig, Cheryl Knott, carefully defined measures for a wide must also be incorporated. But we Don Kramer, Joanna Lambert, Louis range of species. For example, we hope that the issues brought to light Lefebvre, Patrick Omeja, David Pil- need comparable descriptions of the by this ecological examination of the beam, Jessica Rothman, Richard spatial and temporal distribution of folivore paradox will contribute to Wrangham, McGill University’s food resources, variation in food the next generation of models by Behavioural Ecology Discussion ARTICLES Folivore Group Size and Socioecology 105

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