KroeberAnthropological Society Papers, Nos. 71-72, 1990

Colobine Socioecology and Female-bonded Models of Social Structure Craig B. Stanford

Ecological models ofprimate social systems have been used extensively to explain the variationsfound in social organization among living and to accountforprimate sociality itself. Recent attempts to characterize primate social systems as either 'female-bonded" or "non-female-bonded" establish a typology that does notfully consider the variation inpatterns ofsex-biased dispersal seen in the Primate order. Thispaper uses as its example the subfamily to show that ecologi- cal models are basedprimarily onfrugivorous, territorialpinmates. The models are inadequate to explain patterns ofintergroup competition and should not be usedfor setting general rulesforprimate societies. Apreliminary alternative view ofsex-biased dispersal that is basedonfrequency dependence is offered.

INTRODUCTION bonded according to each species' typical pattern Trivers (1972) and Emlen and Oring (1977) of sex-biased dispersal. Males are assumed to outlined the hypothesis that females and males have a greater lifetime reproductive potential than have been selected to invest their lifetime energies females, and in most species they invest less in differently: females in maintaining access to offspring than do females (Trivers 1972). Since maintenance and growth resources, in order to food intake for an individual female primate is invest most in their offspring; and males in a maximized by feeding singly, the evolution of reproductive strategy that maximizes access to fe- primate sociality suggests that there is some bene- males, investing relatively little in offspring. In fit accruing to females who forage as a group. short, females should compete for food, and Wrangham (1980) considered this benefit, which males should compete for females. Wrangham outweighs the costs of intra-group competition, extended the logic of ranking evolutionary pres- to be the ability of females in groups to displace sures on social systems in this way to nonhuman and defend high-quality food patches from other primate societies, first to explain ape social sys- groups. Because the joint defense of food pat- tems (1979) and later to explain primate societies ches requires females to act in unison for in general (1980, 1987). His female-bonded individual reward, kin selection theory was in- model of the evolution ofprimate social structure voked to account for the fitness advantages of observed that most primate species are found in female kin cooperation. Other corollaries of the groups ofrelated females accompanied by males, model are that in female-bonded species, females and hypothesized that this grouping pattern is the should take an active role in territorial defense product of the competing costs and benefits of and are expected to influence the timing and di- living and foraging socially rather than singly rection of group travel (Wrangham 1980). (Wrangham 1980, 1987). The model thus depends on certain ecolo- This paper examines the applicability of this gical conditions, such as discreetly located theory to the Old World monkey subfamily Co- patches of food which are large enough to accom- lobinae and argues that ecological models of modate a group of females and are defensible by female-bonded primate groups fail to explain the them. In order to explain the evolution of the range of social adaptation found in this large pri- social systems of primate species that cannot be mate taxon. While acknowledging that a male/ considered "female-bonded", one or more of female asymmetry in mating strategies should be these ecological conditions must not be true. expected, I will argue that the evidence suppor- Common chimpanzees (Pan troglodytes), moun- ting both intergroup feeding competition and sex- tain gorillas (Gorilla gorilla beringei), hamadryas biased dispersal is weak, and that using field data baboons (Papio hamadryas) and from colobine studies to test the model leads to monkeys (Procolobus badius) are four species conclusions quite different from those of the labelied "non-female-bonded". They are consid- female-bonded model. By implication, the model ered to live predominantly in male kin groups is held insufficient as a unitary explanation for the with female dispersal for the ecological reason evolution ofprimate societies. given above, unlike female-bonded, male-disper- The female-bonded model characterizes sal species. The rest of this paper considers piimate societies as either female or non-female whether this dichotomy is warranted. 22

NON-FEMALE-BONDED SPECIES local ecologies, tend to subsist on a diet that is low in mature leaves but switch to preferred fruit Of the four primate species identified as non- and leaf flush whenever possible. It also sug- female-bonded or female transfer, the hamadryas gests that the colobine digestive adaptation may baboon should probably be considered a special vary among species in form and function rather case in that female transfers occur almost exclu- than be a uniform suite of morphological and sively between higher level strata of the social physiological traits that aid in the digestion of organization ("clans") and thus, females may not low-quality foods. be permanently leaving the local breeding pool. Most colobines live in territorial one-male In mountain gorillas and common chimpanzees, groups (Table 1). Males disperse from these females do not have affiliative relationships, and groups at or before sexual maturity, or are driven females of both species may emigrate from their off by the resident male, though exceptions exist natal groups, although in common chimpanzees in which subadults remain in their natal groups to the transfer may be more of a "visit" with a later breed. Females transfer between groups in many return to the natal group than a permanent emi- species; the earlier view of social units that are gration for reproductive purposes. The fourth essentially closed except for the dispersal of species, the red colobus monkey, seems to be young males and invasions by outside males is highly variable in social structure, and the same almost certainly simplistic. Little data exist on population may show quite different interannual female dominance relationships and where they levels of female emigration (Marsh 1979; Smith have been documented dominance is most often pers. comm.). The incidence of intensive pre- simply labelled "strong" or "weak". Female dation on some red colobus populations by dominance relations, or the lack of them in most chimpanzees adds to the difficulty in establishing colobines, are important because they may be re- functional bases for social structure; the male- lated to the relatively high rates of female bonded kin groups at the core of some red emigration observed among colobines (Stanford colobus populations may be the evolutionary re- in preparation). McKenna (1979) viewed the sult of advantages of male cooperation against relationships between female colobines to be attacking chimps. The relative effectiveness of strongly influenced by the uniform distribution of predator mobbing by related males versus single- their leafy diets, which minimized intragroup male anti-predator attacks has not been tested. competition and allowed a weakening ofthe dom- inance hierarchy. The assumption that colobines use leaves as a year-round staple diet has been COLOBINE SOCIOECOLOGY questioned, however, and such a dietary basis for dominance is not clear (Stanford 1989). The anthropoid subfamily Colobinae con- As field data accumulate on more colobine sists of approximately 35 species of African and species, most species living in one-male groups Asian monkeys. The range of social and mating have been reported to have a regular if unknown systems found in this group varies from mono- rate offemale transfer (Stanford 1989; Moore and gamy (Presbytispotenziani) to multi-male groups Ali 1984; Davies 1987; Bennett 1983). It is with female dispersal (some red colobus popu- therefore probably incorrect to classify the social lations) to territorial one-male groups (most systems of this subfamily as either "female-bon- Presbytis spp.), with some species displaying ded" or "female-transfer". Although Wrangham great intraspecific variation (Presbytis entellus). (1980) allows for a "restricted" amouni of trans- The group is characterized by a specialized gut fer by females in female-bonded groups, there is anatomy that is able to break down plant cell wall a continuum of female transfer rates. For exam- materials and, using symbiotic gut flora, digest ple, some red colobus populations have 100% mature leaf material that is typically avoided or female dispersal (Kanyawara, Kibale, Uganda; indigestible by other primates (Bauchop 1978). Struhsaker 1975), while others are characterized This adaptation has led to an unwarranted gen- by a much lower and perhaps variable frequency eralization that the colobines are leaf-eaters. (Tana River, Kenya; Marsh 1979; Smith pers. Although clearly adapted to coping with a comm.). Despite numerous field studies and seasonally poor diet, a diversity of diets from thousands of observer hours female transfer has seed-eating (Presbytis rubicunda, Davies 1984; rarely been reported in Hanuman langurs. Thus, Colobus satanus, McKey and Waterman 1982) to there appears to be wide variation in the pattern unripe fruit (Procolobus badius, Struhsaker and frequency of female transfer among members 1975) and even ripe fruit (Presbytispileata, Stan- of the Colobinae. The implications of both this ford 1989) have been reported. This probably inter- and intra-specific variation will be dis- indicates that colobines, while able to respond to cussed below. 23

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00 } = ; i i0 A 24 The dietary categories in Table 1 are neces- subcontinent. It lives exclusively in one-male sarily vague, as a monkey that feeds heavily on groups of four to thirteen . During 1400 leaves during one or two seasons may be highly hours of observation over 15 months, three adult frugivorous or a seed specialist in other parts of females immigrated into five study groups, and the year. Since the time span over which pri- these immigrations were accompanied by female mates balance their, diets and energy budgets is solicitation of and copulation with the resident unknown, the potential importance of seasonal male. No male changes were observed, and at variation in diet for analyzing both feeding ecol- least one resident male maintained his tenure for ogy and evolutionary and ecological influences at least 26 months. Capped langur groups on the social system is presently unmeasurable. occupy widely overlapping home ranges, no part Travel leadership is presented for those species of which were ever observed to be defended for which it has been systematically reported; un- against other groups. Food trees were also unde- like the literature on baboon behavior, where the fended. During the rainy season, capped langurs determination of the timing and direction of group at Madhupur switched their dietary habits from movement has been studied (Sigg and Stolba predominantly mature leaves to ripe and unripe 1981; Rhine and Westlund 1981), patterns of fruit. Although feeding competition theory pre- group travel in arboreal forest monkeys are dicts that widely dispersed fruit sources should poorly known. The significance of female lead- be competed for more intensely than abundant ership, discussed below, is hard to establish leaves, capped langur groups showed no greater because it is often unobservable in dense foliage rates of aggressive displays during intergroup or rapidly moving groups and sub-groups, and encounters when they fed heavily on fruit than when it is observable, fieldworkers have failed to when they ate mainly leaves. Groups encoun- record it systematically. tered one another an average of about once per day in the Madhupur forest. The response upon meeting was one of mutual attention and vigi- The Capped Langur lance, but tension was rarely observed. In contrast, encounters between one-male groups The capped langur (Presbytis pileata, Figure and extra-group males were tense and often 1) is found in the eastern portion of the Indian aggressive. The behavior of females and males during intergroup encounters provides additional support for the conclusion that intergroup encounters in Presbytis pileata involve mate defense rather than food defense. When females attempted to move in the direction of the other group during an en- counter, the resident male rushed to the female and coercively moved her back towards the group. This behavior, coupled with the observa- tions that females do move between groups and the apparent lack of successful male takeovers, suggests that the capped langur mating system is characterized by mate defense polygyny that is moderately unsuccessful on the part of the males, as the rate of female transfer appears to be high. Because social groups of most primate species to some extent defend the borders of an area in which both food and mates are located, hypothe- ses that can distinguish between resource defense and mate defense are difficult to test. Because of the absence offood source defense in capped lan- gurs, the function of male and female behavior during intergroup encounters was clearly related to mating tactics. If capped langurs are considered to be female-bonded, then several assumptions can be Figure 1. Capped langur monkey (Presbytis tested with regard to their ecology and mating pileata durga) in Madhupur National Park, system: Bangladesh. 25 1) Females should lead groups during the food sources and the level of food abundance. group's daily range path, as the relatedness of Mitani and Rodman (1979) attempted to predict adult females is expected to contribute to each when a primate group should defend food sour- female's inclusive fitness benefit in enhanced ces according to the overall home range size in foraging efficiency and food-getting. relation to the group's daily range length. If day 2) If high quality but widely dispersed food range is insufficiently long to effectively monitor patches are preferred, they should be contested the perimeter of the group's range, then food for by different groups sharing the home range. sources are considered economically indefensi- If they are not overtly competed for, then a clear ble. Following this prediction, capped langurs at intergoup dominance relationship should be dis- Madhupur should be expected to defend fruit cemable that mediates the frequency and intensity trees during the rainy season, when their day of such encounters over food sources. range increases substantially and all groups feed 3) Females should cooperate in aggression du- heavily on ripe fruit witiin their overlapping 20 ring such intergroup encounters, as they have a hectare home ranges. During the dry winter mutual inclusive fitness stake in defending food months, when mature leaves are the staple, day sources from neighboring groups. range is shorter and the economics offood source 4) Females should in general show affiliative defense different; no defense is expected in this behavior towards one another, in the form of season. In fact, the animals never defended food alliances, grooming relationships and higher fre- sources, even when they were feeding on high quencies of spatial association among themselves quality clumps of fruit. than between themselves and the group male. The other variable, the abundance of food in the habitat, is more difficult to measure. Vegeta- Only the first of these assumptions was tion analysis showed that few of the monkeys' found to be true for capped langurs (Stanford food trees were clumped in distribution, and 1989); females determined the timing and direc- overall tree species diversity was quite low -- 28 ton of virtually all group travel during ranging. species comprised nearly all of the animals' Even though during the rainy season ripe fruits feeding records. During the dry season, approxi- were the most preferred food source, neither the mately 70% of all Madhupur trees were more or frequency nor the intensity ofintergroup encoun- less bare of foliage (Stanford 1989). Patch size ters increased significantly in spite of the longer of the most commonly eaten food, the young and distances travelled to reach fruit trees. Affiliative mature leaves of Wrightia tomentosa (Apocyna- levels among females were relatively low; fe- ceae), was uniformly small (average trunk dia- males spent little time in close proximity (< 1 meter at-breast-height of individuals in sample meter) to one another or to the group male (on transect = 6 cm). The monkeys fed on the mature average less than 4% of the active time of each and often dessicated leaves of whatever trees female). were in leaf and also fed on herbaceous ground Because capped langur groups have broadly cover and tree pith. These food items were avail- overlapping home ranges and do not contest food able more or less evenly throughout the habitat. sources aggressively, it is likely that intergroup When fruit was eaten heavily, the preferred spe- encounters in this species are related primarily to cies of trees were widely scattered and the mate defense and female transfer. It would be monkeys travelled further each day and spent unwise to speculate on the cognitive processes or more total time moving to reach them. The trees motivation that prompt female emigration, but the were not, however, competed for in an aggres- protective/coercive behavior shown towards fe- sive sense; even when two or three groups males by their group males during encounters attempted to feed at the same tree, they either oc- with other males suggests that females use inter- cupied opposite edges ofthe tree crown (for large group encounters to evaluate conditions in other Ficus trees) or waited for one group to finish one-male groups, or to assess the quality of a before entering the tree. There was no consistent lone male or the males of an all-male band, as re- dominance relationship among the five main ported for mountain gorillas (Harcourt et al. study groups. 1976). If females in female-bonded groups should be expected to enhance their reproductive success by competing successfully for patches of high- INTERGROUP COMPETITION quality foods, then the food must conform to two patterns: it must be defensible and there must be The absence of resource defense by P. pil- enough of it to feed all or most of the group. eata may be related to at least two measurable This raises the question of how to define a high- economic factors: the degree of defensibility of quality food patch. The concept of "patch" tends 26 to be defined by ecological primatologists in among nonhuman primates is a puzzle. whatever way is best suited to the model at hand, The data on nonhuman primate patterns of rather than according to energy maximizing pnn- dispersal and intergroup relations, therefore, sug- ciples drawn from foraging theory (Stephens and gest that: 1) the dichotomy drawn by Wrangham Krebs 1986). Its use by primatologists varies and others between "female-bonded" and "non- and the concept is often used incorrectly to sup- female-bonded" species is falsified by the range port assertions about the influence of ecology on of mating systems and dispersal patterns found social structure. Is a species that feeds exten- among the colobines; and 2) regardless of the ma- sively on leaves limited in the same way as is a ting system used, levels of intergroup frugivorous species? In foraging theory, the cru- food competition vary widely between species cial difference is that leaves tend to be eaten only and do not necessarily follow the axiom that high partially while fruits are more often consumed en- quality food sources produce intense intergroup tirely. While some would argue that the problem competition which would favor individuals toler- is simply one of properly identifying the patch ating group life for the sake of access to better and measuring the energetic costs and benefits of food. exploiting it, it is important to note that there are Female-bonded models are ultimately exten- important qualitative differences between differ- sions of resource-defense polygyny models of ent types of food patches. White and Wrangham avian social systems. Among many bird species, (1988) point out that although it is tempting to re- males compete for territories rich in food and late chimpanzee grouping patterns and social nest-site resources and females choose males on structure directly to patch size, the size of food this basis (Emlen and Oring 1977). Variation in patches undoubtedly differs widely across the territory quality leads to differences in the repro- range of chimp habitats and there is no evidence ductive potential of both males and females. In that chimp social organization varies with it. the avian model, males distribute themselves in The implication of capped langur socioecol- space and influence the distribution of females on ogy is that this species and other leaf-monkeys the basis of the females' choice of male territo- belie the utility of female- or non-female-bonded ries. In the primate model, females choose the taxonomies. This may be true for nonhuman pri- spatial distribution according to resources and mates in general (Stanford in preparation). The males attach themselves to single or multiple question then is how to explain complex social females in order to enhance their chances of suc- systems in which there are different and variable cessful mating. Control of females is the key to rates of both male and female dispersal. Female mating success in both models. For species that lions, for instance, emigrate at varying rates in are not female-bonded, males do not defend a different populations but the result is the same: fixed spatial area (e.g., mountain gorillas). Mate females that transfer breed later and suffer higher defense polygyny is then inferred from the nature mortality than those who do not (Pusey and ofintergroup encounters. The capped langur data Packer 1987). Specific levels of emigration by show that mate defense polygyny and resource females in a male-dispersal social system may be defense can be easily conflated in a territorial selected for, but the ecological or demographic species. Capped langurs also teach us that as- factors that would mediate dispersal by only sumptions about the costs and benefits of some rather than by all females are unknown. intergroup resource competition must take into Possibly a small proportion offemales can obtain account seasonal differences in the values ofdif- benefits in the form of enhanced mating success ferent resources. Thus, the colobines in general or nutritional advantages in the form of reduced illustrate the problems of applying unitary expla- intra-sexual competition by emigrating, but selec- nations to an exceedingly diverse set of primate tion against inbreeding may prevent large scale social adaptations. migration by females in species characterized by male dispersal. Small numbers of females might benefit by ending up as "novel" females in other, CONCLUSIONS smaller groups while a large influx of females would not be favored. Models of purported in- Vehrencamp and Bradbury (1984) point out tragroup cooperation in resource defense are also that creating a taxonomy of mating systems not readily operationalized. This sort of fre- according to any hierarchical ranking of the quency dependence could produce the variation in reladve importance ofdifferent behavioral options dispersal patterns seen without invoking un- is faulty in that by focusing on one component, wieldy inclusive fitness arguments that rely on attention is drawn away from other potentially such models of intragroup cooperation. Why important influences. Although it might be there are only a few "female-transfer" species argued that this is unavoidable in hypothesis 27 formation, the problem can be minimized by al- versions of this material I am grateful to Thelma lowing for a mixture of behavioral strategies Rowell, Phyllis Dolhinow, Katharine Milton, Jim rather than the hierarchy of evolutionary pres- Moore and Nancy Krusko. Thanks to Susan sures proposed by female-bonded taxonomies. Wagner for preparing Table 1. I also thank the Examples drawn here from the colobine monkeys government of Bangladesh and especially Abdul should be sufficient to show that such a typology Wahab Akonda, M. R. Talukder and Erin Moore offemale-bonded versus female-transfer primate for assistance during periods of fieldwork be- societies is simplistic and, in portraying social tween 1986 and 1988. systems as largely built around the single inde- pendent variable of female food competition, it fails to explain the range of social behavior seen injust one primate taxon. REFERENCES CITED The preliminary alternative scenario presen- Bauchop, T. (1978) Digestion of leaves in ted here for colobine social system evolution can vertebrate arboreal folivores. In G.G. Mont- be no more accurate than the female-bonded mo- gomery (ed.), The Ecology of Arboreal del without more field data on the relationships Folivores. 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