Kroeber Anthropological Society Papers, Nos. 71-72, 1990

Colobine Socioecology and Female-bonded Models of Primate Social StructureCraig B. Stanford

Ecological models ofprimate social systems have been used extensively to explain the variationsfoundin social organization among living primates and to accountforprimate sociality itself. Recent attemptsto characterize primate social systems as either 'female-bonded" or "non-female-bonded" establish atypology that does notfully consider the variation in patterns ofsex-biased dispersal seen in the Primateorder. This paper uses as its example the Old World monkey subfamily Colobinae to show that ecologi-cal models are basedprimarily onfrugivorous, territorialpinmates. The models are inadequate to explainpatterns ofintergroup competition and should not be usedfor setting general rulesforprimate societies.A preliminary alternative view ofsex-biased dispersal that is based onfrequency dependence is offered.

INTRODUCTION

Trivers (1972) and Emlen and Oring (1977)outlined the hypothesis that females and maleshave been selected to invest their lifetime energiesdifferently: females in maintaining access tomaintenance and growth resources, in order toinvest most in their offspring; and males in areproductive strategy that maximizes access to fe-males, investing relatively little in offspring. Inshort, females should compete for food, andmales should compete for females. Wranghamextended the logic of ranking evolutionary pres-sures on social systems in this way to nonhumanprimate societies, first to explain ape social sys-tems (1979) and later to explain primate societiesin general (1980, 1987). His female-bondedmodel of the evolution of primate social structureobserved that most primate species are found ingroups of related females accompanied by males,and hypothesized that this grouping pattern is theproduct of the competing costs and benefits ofliving and foraging socially rather than singly(Wrangham 1980, 1987).

This paper examines the applicability of thistheory to the Old World monkey subfamily Co-lobinae and argues that ecological models offemale-bonded primate groups fail to explain therange of social adaptation found in this large pri-mate taxon. While acknowledging that a male/female asymmetry in mating strategies should beexpected, I will argue that the evidence suppor-ting both intergroup feeding competition and sex-biased dispersal is weak, and that using field datafrom colobine studies to test the model leads toconclusions quite different from those of thefemale-bonded model. By implication, the modelis held insufficient as a unitary explanation for theevolution of primate societies.

The female-bonded model characterizespiimate societies as either female or non-female

bonded according to each species' typical patternof sex-biased dispersal. Males are assumed tohave a greater lifetime reproductive potential thanfemales, and in most species they invest less inoffspring than do females (Trivers 1972). Sincefood intake for an individual female primate ismaximized by feeding singly, the evolution ofprimate sociality suggests that there is some bene-fit accruing to females who forage as a group.Wrangham (1980) considered this benefit, whichoutweighs the costs of intra-group competition,to be the ability of females in groups to displaceand defend high-quality food patches from othergroups. Because the joint defense of food pat-ches requires females to act in unison forindividual reward, kin selection theory was in-voked to account for the fitness advantages offemale kin cooperation. Other corollaries of themodel are that in female-bonded species, femalesshould take an active role in territorial defenseand are expected to influence the timing and di-rection of group travel (Wrangham 1980).

The model thus depends on certain ecolo-gical conditions, such as discreetly locatedpatches of food which are large enough to accom-modate a group of females and are defensible bythem. In order to explain the evolution of thesocial systems of primate species that cannot beconsidered "female-bonded", one or more ofthese ecological conditions must not be true.Common chimpanzees (Pan troglodytes), moun-tain gorillas (Gorilla gorilla beringei), hamadryasbaboons (Papio hamadryas) and red colobusmonkeys (Procolobus badius) are four specieslabelied "non-female-bonded". They are consid-ered to live predominantly in male kin groupswith female dispersal for the ecological reasongiven above, unlike female-bonded, male-disper-sal species. The rest of this paper considerswhether this dichotomy is warranted.

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NON-FEMALE-BONDED SPECIES

Of the four primate species identified as non-female-bonded or female transfer, the hamadryasbaboon should probably be considered a specialcase in that female transfers occur almost exclu-sively between higher level strata of the socialorganization ("clans") and thus, females may notbe permanently leaving the local breeding pool.In mountain gorillas and common chimpanzees,females do not have affiliative relationships, andfemales of both species may emigrate from theirnatal groups, although in common chimpanzeesthe transfer may be more of a "visit" with a laterreturn to the natal group than a permanent emi-gration for reproductive purposes. The fourthspecies, the red colobus monkey, seems to behighly variable in social structure, and the samepopulation may show quite different interannuallevels of female emigration (Marsh 1979; Smithpers. comm.). The incidence of intensive pre-dation on some red colobus populations bychimpanzees adds to the difficulty in establishingfunctional bases for social structure; the male-bonded kin groups at the core of some redcolobus populations may be the evolutionary re-sult of advantages of male cooperation againstattacking chimps. The relative effectiveness ofpredator mobbing by related males versus single-male anti-predator attacks has not been tested.

COLOBINE SOCIOECOLOGY

The anthropoid subfamily Colobinae con-sists of approximately 35 species of African andAsian monkeys. The range of social and matingsystems found in this group varies from mono-gamy (Presbytis potenziani) to multi-male groupswith female dispersal (some red colobus popu-lations) to territorial one-male groups (mostPresbytis spp.), with some species displayinggreat intraspecific variation (Presbytis entellus).The group is characterized by a specialized gutanatomy that is able to break down plant cell wallmaterials and, using symbiotic gut flora, digestmature leaf material that is typically avoided orindigestible by other primates (Bauchop 1978).This adaptation has led to an unwarranted gen-eralization that the colobines are leaf-eaters.Although clearly adapted to coping with aseasonally poor diet, a diversity of diets fromseed-eating (Presbytis rubicunda, Davies 1984;Colobus satanus, McKey and Waterman 1982) tounripe fruit (Procolobus badius, Struhsaker1975) and even ripe fruit (Presbytis pileata, Stan-ford 1989) have been reported. This probablyindicates that colobines, while able to respond to

local ecologies, tend to subsist on a diet that islow in mature leaves but switch to preferred fruitand leaf flush whenever possible. It also sug-gests that the colobine digestive adaptation mayvary among species in form and function ratherthan be a uniform suite of morphological andphysiological traits that aid in the digestion oflow-quality foods.

Most colobines live in territorial one-malegroups (Table 1). Males disperse from thesegroups at or before sexual maturity, or are drivenoff by the resident male, though exceptions existin which subadults remain in their natal groups tobreed. Females transfer between groups in manyspecies; the earlier view of social units that areessentially closed except for the dispersal ofyoung males and invasions by outside males isalmost certainly simplistic. Little data exist onfemale dominance relationships and where theyhave been documented dominance is most oftensimply labelled "strong" or "weak". Femaledominance relations, or the lack of them in mostcolobines, are important because they may be re-lated to the relatively high rates of femaleemigration observed among colobines (Stanfordin preparation). McKenna (1979) viewed therelationships between female colobines to bestrongly influenced by the uniform distribution oftheir leafy diets, which minimized intragroupcompetition and allowed a weakening of the dom-inance hierarchy. The assumption that colobinesuse leaves as a year-round staple diet has beenquestioned, however, and such a dietary basis fordominance is not clear (Stanford 1989).

As field data accumulate on more colobinespecies, most species living in one-male groupshave been reported to have a regular if unknownrate of female transfer (Stanford 1989; Moore andAli 1984; Davies 1987; Bennett 1983). It istherefore probably incorrect to classify the socialsystems of this subfamily as either "female-bon-ded" or "female-transfer". Although Wrangham(1980) allows for a "restricted" amouni of trans-fer by females in female-bonded groups, there isa continuum of female transfer rates. For exam-ple, some red colobus populations have 100%female dispersal (Kanyawara, Kibale, Uganda;Struhsaker 1975), while others are characterizedby a much lower and perhaps variable frequency(Tana River, Kenya; Marsh 1979; Smith pers.comm.). Despite numerous field studies andthousands of observer hours female transfer hasrarely been reported in Hanuman langurs. Thus,there appears to be wide variation in the patternand frequency of female transfer among membersof the Colobinae. The implications of both thisinter- and intra-specific variation will be dis-cussed below.

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The dietary categories in Table 1 are neces-sarily vague, as a monkey that feeds heavily onleaves during one or two seasons may be highlyfrugivorous or a seed specialist in other parts ofthe year. Since the time span over which pri-mates balance their, diets and energy budgets isunknown, the potential importance of seasonalvariation in diet for analyzing both feeding ecol-ogy and evolutionary and ecological influenceson the social system is presently unmeasurable.Travel leadership is presented for those speciesfor which it has been systematically reported; un-like the literature on baboon behavior, where thedetermination of the timing and direction of groupmovement has been studied (Sigg and Stolba1981; Rhine and Westlund 1981), patterns ofgroup travel in arboreal forest monkeys arepoorly known. The significance of female lead-ership, discussed below, is hard to establishbecause it is often unobservable in dense foliageor rapidly moving groups and sub-groups, andwhen it is observable, fieldworkers have failed torecord it systematically.

The Capped Langur

The capped langur (Presbytis pileata, Figure1) is found in the eastern portion of the Indian

Figure 1. Capped langur monkey (Presbytispileata durga) in Madhupur National Park,Bangladesh.

subcontinent. It lives exclusively in one-malegroups of four to thirteen animals. During 1400hours of observation over 15 months, three adultfemales immigrated into five study groups, andthese immigrations were accompanied by femalesolicitation of and copulation with the residentmale. No male changes were observed, and atleast one resident male maintained his tenure forat least 26 months. Capped langur groupsoccupy widely overlapping home ranges, no partof which were ever observed to be defendedagainst other groups. Food trees were also unde-fended. During the rainy season, capped langursat Madhupur switched their dietary habits frompredominantly mature leaves to ripe and unripefruit. Although feeding competition theory pre-dicts that widely dispersed fruit sources shouldbe competed for more intensely than abundantleaves, capped langur groups showed no greaterrates of aggressive displays during intergroupencounters when they fed heavily on fruit thanwhen they ate mainly leaves. Groups encoun-tered one another an average of about once perday in the Madhupur forest. The response uponmeeting was one of mutual attention and vigi-lance, but tension was rarely observed. Incontrast, encounters between one-male groupsand extra-group males were tense and oftenaggressive.

The behavior of females and males duringintergroup encounters provides additional supportfor the conclusion that intergroup encounters inPresbytis pileata involve mate defense rather thanfood defense. When females attempted to movein the direction of the other group during an en-counter, the resident male rushed to the femaleand coercively moved her back towards thegroup. This behavior, coupled with the observa-tions that females do move between groups andthe apparent lack of successful male takeovers,suggests that the capped langur mating system ischaracterized by mate defense polygyny that ismoderately unsuccessful on the part of the males,as the rate of female transfer appears to be high.Because social groups of most primate species tosome extent defend the borders of an area inwhich both food and mates are located, hypothe-ses that can distinguish between resource defenseand mate defense are difficult to test. Because ofthe absence of food source defense in capped lan-gurs, the function of male and female behaviorduring intergroup encounters was clearly relatedto mating tactics.

If capped langurs are considered to befemale-bonded, then several assumptions can betested with regard to their ecology and matingsystem:

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1) Females should lead groups during thegroup's daily range path, as the relatedness ofadult females is expected to contribute to eachfemale's inclusive fitness benefit in enhancedforaging efficiency and food-getting.

2) If high quality but widely dispersed foodpatches are preferred, they should be contestedfor by different groups sharing the home range.If they are not overtly competed for, then a clearintergoup dominance relationship should be dis-cemable that mediates the frequency and intensityof such encounters over food sources.

3) Females should cooperate in aggression du-ring such intergroup encounters, as they have amutual inclusive fitness stake in defending foodsources from neighboring groups.

4) Females should in general show affiliativebehavior towards one another, in the form ofalliances, grooming relationships and higher fre-quencies of spatial association among themselvesthan between themselves and the group male.

Only the first of these assumptions wasfound to be true for capped langurs (Stanford1989); females determined the timing and direc-ton of virtually all group travel during ranging.Even though during the rainy season ripe fruitswere the most preferred food source, neither thefrequency nor the intensity of intergroup encoun-ters increased significantly in spite of the longerdistances travelled to reach fruit trees. Affiliativelevels among females were relatively low; fe-males spent little time in close proximity (< 1meter) to one another or to the group male (onaverage less than 4% of the active time of eachfemale).

Because capped langur groups have broadlyoverlapping home ranges and do not contest foodsources aggressively, it is likely that intergroupencounters in this species are related primarily tomate defense and female transfer. It would beunwise to speculate on the cognitive processes ormotivation that prompt female emigration, but theprotective/coercive behavior shown towards fe-males by their group males during encounterswith other males suggests that females use inter-group encounters to evaluate conditions in otherone-male groups, or to assess the quality of alone male or the males of an all-male band, as re-ported for mountain gorillas (Harcourt et al.1976).

INTERGROUP COMPETITION

The absence of resource defense by P. pil-eata may be related to at least two measurableeconomic factors: the degree of defensibility of

food sources and the level of food abundance.Mitani and Rodman (1979) attempted to predictwhen a primate group should defend food sour-ces according to the overall home range size inrelation to the group's daily range length. If dayrange is insufficiently long to effectively monitorthe perimeter of the group's range, then foodsources are considered economically indefensi-ble. Following this prediction, capped langurs atMadhupur should be expected to defend fruittrees during the rainy season, when their dayrange increases substantially and all groups feedheavily on ripe fruit witiin their overlapping 20hectare home ranges. During the dry wintermonths, when mature leaves are the staple, dayrange is shorter and the economics of food sourcedefense different; no defense is expected in thisseason. In fact, the animals never defended foodsources, even when they were feeding on highquality clumps of fruit.

The other variable, the abundance of food inthe habitat, is more difficult to measure. Vegeta-tion analysis showed that few of the monkeys'food trees were clumped in distribution, andoverall tree species diversity was quite low -- 28species comprised nearly all of the animals'feeding records. During the dry season, approxi-mately 70% of all Madhupur trees were more orless bare of foliage (Stanford 1989). Patch sizeof the most commonly eaten food, the young andmature leaves of Wrightia tomentosa (Apocyna-ceae), was uniformly small (average trunk dia-meter at-breast-height of individuals in sampletransect = 6 cm). The monkeys fed on the matureand often dessicated leaves of whatever treeswere in leaf and also fed on herbaceous groundcover and tree pith. These food items were avail-able more or less evenly throughout the habitat.When fruit was eaten heavily, the preferred spe-cies of trees were widely scattered and themonkeys travelled further each day and spentmore total time moving to reach them. The treeswere not, however, competed for in an aggres-sive sense; even when two or three groupsattempted to feed at the same tree, they either oc-cupied opposite edges of the tree crown (for largeFicus trees) or waited for one group to finishbefore entering the tree. There was no consistentdominance relationship among the five mainstudy groups.

If females in female-bonded groups shouldbe expected to enhance their reproductive successby competing successfully for patches of high-quality foods, then the food must conform to twopatterns: it must be defensible and there must beenough of it to feed all or most of the group.This raises the question of how to define a high-quality food patch. The concept of "patch" tends

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to be defined by ecological primatologists inwhatever way is best suited to the model at hand,rather than according to energy maximizing pnn-ciples drawn from foraging theory (Stephens andKrebs 1986). Its use by primatologists variesand the concept is often used incorrectly to sup-port assertions about the influence of ecology onsocial structure. Is a species that feeds exten-sively on leaves limited in the same way as is afrugivorous species? In foraging theory, the cru-cial difference is that leaves tend to be eaten onlypartially while fruits are more often consumed en-tirely. While some would argue that the problemis simply one of properly identifying the patchand measuring the energetic costs and benefits ofexploiting it, it is important to note that there areimportant qualitative differences between differ-ent types of food patches. White and Wrangham(1988) point out that although it is tempting to re-late chimpanzee grouping patterns and socialstructure directly to patch size, the size of foodpatches undoubtedly differs widely across therange of chimp habitats and there is no evidencethat chimp social organization varies with it.

The implication of capped langur socioecol-ogy is that this species and other leaf-monkeysbelie the utility of female- or non-female-bondedtaxonomies. This may be true for nonhuman pri-mates in general (Stanford in preparation). Thequestion then is how to explain complex socialsystems in which there are different and variablerates of both male and female dispersal. Femalelions, for instance, emigrate at varying rates indifferent populations but the result is the same:females that transfer breed later and suffer highermortality than those who do not (Pusey andPacker 1987). Specific levels of emigration byfemales in a male-dispersal social system may beselected for, but the ecological or demographicfactors that would mediate dispersal by onlysome rather than by all females are unknown.Possibly a small proportion of females can obtainbenefits in the form of enhanced mating successor nutritional advantages in the form of reducedintra-sexual competition by emigrating, but selec-tion against inbreeding may prevent large scalemigration by females in species characterized bymale dispersal. Small numbers of females mightbenefit by ending up as "novel" females in other,smaller groups while a large influx of femaleswould not be favored. Models of purported in-tragroup cooperation in resource defense are alsonot readily operationalized. This sort of fre-quency dependence could produce the variation indispersal patterns seen without invoking un-wieldy inclusive fitness arguments that rely onsuch models of intragroup cooperation. Whythere are only a few "female-transfer" species

among nonhuman primates is a puzzle.The data on nonhuman primate patterns of

dispersal and intergroup relations, therefore, sug-gest that: 1) the dichotomy drawn by Wranghamand others between "female-bonded" and "non-female-bonded" species is falsified by the rangeof mating systems and dispersal patterns foundamong the colobines; and 2) regardless of the ma-ting system taxonomy used, levels of intergroupfood competition vary widely between speciesand do not necessarily follow the axiom that highquality food sources produce intense intergroupcompetition which would favor individuals toler-ating group life for the sake of access to betterfood.

Female-bonded models are ultimately exten-sions of resource-defense polygyny models ofavian social systems. Among many bird species,males compete for territories rich in food andnest-site resources and females choose males onthis basis (Emlen and Oring 1977). Variation interritory quality leads to differences in the repro-ductive potential of both males and females. Inthe avian model, males distribute themselves inspace and influence the distribution of females onthe basis of the females' choice of male territo-ries. In the primate model, females choose thespatial distribution according to resources andmales attach themselves to single or multiplefemales in order to enhance their chances of suc-cessful mating. Control of females is the key tomating success in both models. For species thatare not female-bonded, males do not defend afixed spatial area (e.g., mountain gorillas). Matedefense polygyny is then inferred from the natureof intergroup encounters. The capped langur datashow that mate defense polygyny and resourcedefense can be easily conflated in a territorialspecies. Capped langurs also teach us that as-sumptions about the costs and benefits ofintergroup resource competition must take intoaccount seasonal differences in the values of dif-ferent resources. Thus, the colobines in generalillustrate the problems of applying unitary expla-nations to an exceedingly diverse set of primatesocial adaptations.

CONCLUSIONS

Vehrencamp and Bradbury (1984) point outthat creating a taxonomy of mating systemsaccording to any hierarchical ranking of thereladve importance of different behavioral optionsis faulty in that by focusing on one component,attention is drawn away from other potentiallyimportant influences. Although it might beargued that this is unavoidable in hypothesis

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formation, the problem can be minimized by al-lowing for a mixture of behavioral strategiesrather than the hierarchy of evolutionary pres-sures proposed by female-bonded taxonomies.Examples drawn here from the colobine monkeysshould be sufficient to show that such a typologyof female-bonded versus female-transfer primatesocieties is simplistic and, in portraying socialsystems as largely built around the single inde-pendent variable of female food competition, itfails to explain the range of social behavior seenin just one primate taxon.

The preliminary alternative scenario presen-ted here for colobine social system evolution canbe no more accurate than the female-bonded mo-del without more field data on the relationshipsbetween dispersal patterns and mating strategiesand between ecology and intergroup relations.Future field studies of Old World monkeys willcontinue to reveal the complexity of socialrelationships within and among groups that con-founds attempts to construct predictive models ofobserved behavior patterns.

I have previously suggested (Stanford 1989)a "frequency-dependent" interpretation of theprimate field data on sex-biased dispersal andpolygyny. The variety of mating systems in thecolobines suggests a spectrum of rates of sex-biased dispersal and perhaps also a range oflevels of aggression faced by immigrating malesand females. Females should be expected totransfer because of the benefits they can receivein other groups (better access to food and mates),but increased transfer would not be favored aslater arrivals fmd themselves in groups alreadyoccupied by previous immigrants. Althoughsome strongly female philopatric primate speciesmay fit the female-bonded and non-female-bonded taxonomy, most groups and even somespecies exhibit a continuum of dispersal, inter-group interactions and mating systems that haveso far been given little attention and have defiedgenuine explanation. Ultimately the evolution ofsex-biased dispersal in primates will have to beexplained as it has been in other mammals. Anevolutionary model of the behavioral options in-fluencing the formation of female-bonded versusnon-female-bonded species is needed to stimulatetestable hypotheses in this area. These effectswould have profound influences on the way inwhich we currently view the evolution of primatereproductive strategies.

ACKNOWLEDGMENTS

For their contributions of ideas that are pre-sented in this paper and their comments on earlier

versions of this material I am grateful to ThelmaRowell, Phyllis Dolhinow, Katharine Milton, JimMoore and Nancy Krusko. Thanks to SusanWagner for preparing Table 1. I also thank thegovernment of Bangladesh and especially AbdulWahab Akonda, M. R. Talukder and Erin Moorefor assistance during periods of fieldwork be-tween 1986 and 1988.

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