Kroeber Anthropological Society Papers, Nos. 71-72, 1990 Colobine Socioecology and Female-bonded Models of Primate Social Structure Craig B. Stanford Ecological models of primate social systems have been used extensively to explain the variations found in social organization among living primates and to accountfor primate 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 in patterns of sex-biased dispersal seen in the Primate order. 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 explain patterns of intergroup competition and should not be usedfor setting general rulesfor primate societies. A preliminary alternative view of sex-biased dispersal that is based onfrequency dependence is offered. INTRODUCTION Trivers (1972) and Emlen and Oring (1977) outlined the hypothesis that females and males have been selected to invest their lifetime energies differently: females in maintaining access to maintenance and growth resources, in order to invest most in their offspring; and males in a reproductive strategy that maximizes access to fe- males, investing relatively little in offspring. In short, females should compete for food, and males should compete for females. Wrangham extended the logic of ranking evolutionary pres- sures on social systems in this way to nonhuman primate societies, first to explain ape social sys- tems (1979) and later to explain primate societies in general (1980, 1987). His female-bonded model of the evolution of primate social structure observed that most primate species are found in groups of related females accompanied by males, and hypothesized that this grouping pattern is the product of the competing costs and benefits of living and foraging socially rather than singly (Wrangham 1980, 1987). This paper examines the applicability of this theory to the Old World monkey subfamily Co- lobinae and argues that ecological models of female-bonded primate groups fail to explain the range of social adaptation found in this large pri- mate taxon. While acknowledging that a male/ female asymmetry in mating strategies should be expected, I will argue that the evidence suppor- ting both intergroup feeding competition and sex- biased dispersal is weak, and that using field data from colobine studies to test the model leads to conclusions quite different from those of the female-bonded model. By implication, the model is held insufficient as a unitary explanation for the evolution of primate societies. The female-bonded model characterizes piimate societies as either female or non-female bonded according to each species' typical pattern of sex-biased dispersal. Males are assumed to have a greater lifetime reproductive potential than females, and in most species they invest less in offspring than do females (Trivers 1972). Since food intake for an individual female primate is maximized by feeding singly, the evolution of primate sociality suggests that there is some bene- fit accruing to females who forage as a group. Wrangham (1980) considered this benefit, which outweighs the costs of intra-group competition, to be the ability of females in groups to displace and defend high-quality food patches from other groups. Because the joint defense of food pat- ches requires females to act in unison for individual reward, kin selection theory was in- voked to account for the fitness advantages of female kin cooperation. Other corollaries of the model are that in female-bonded species, females should take an active role in territorial defense and 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 located patches of food which are large enough to accom- modate a group of females and are defensible by them. In order to explain the evolution of the social systems of primate species that cannot be considered "female-bonded", one or more of these ecological conditions must not be true. Common chimpanzees (Pan troglodytes), moun- tain gorillas (Gorilla gorilla beringei), hamadryas baboons (Papio hamadryas) and red colobus monkeys (Procolobus badius) are four species labelied "non-female-bonded". They are consid- ered to live predominantly in male kin groups with female dispersal for the ecological reason given above, unlike female-bonded, male-disper- sal species. The rest of this paper considers whether this dichotomy is warranted. 22 NON-FEMALE-BONDED SPECIES Of the four primate species identified as non- female-bonded or female transfer, the hamadryas baboon should probably be considered a special case in that female transfers occur almost exclu- sively between higher level strata of the social organization ("clans") and thus, females may not be permanently leaving the local breeding pool. In mountain gorillas and common chimpanzees, females do not have affiliative relationships, and females of both species may emigrate from their natal groups, although in common chimpanzees the transfer may be more of a "visit" with a later return to the natal group than a permanent emi- gration for reproductive purposes. The fourth species, the red colobus monkey, seems to be highly variable in social structure, and the same population may show quite different interannual levels of female emigration (Marsh 1979; Smith pers. comm.). The incidence of intensive pre- dation on some red colobus populations by chimpanzees adds to the difficulty in establishing functional bases for social structure; the male- bonded kin groups at the core of some red colobus populations may be the evolutionary re- sult of advantages of male cooperation against attacking chimps. The relative effectiveness of predator 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 and Asian monkeys. The range of social and mating systems found in this group varies from mono- gamy (Presbytis potenziani) to multi-male groups with female dispersal (some red colobus popu- lations) to territorial one-male groups (most Presbytis spp.), with some species displaying great intraspecific variation (Presbytis entellus). The group is characterized by a specialized gut anatomy that is able to break down plant cell wall materials and, using symbiotic gut flora, digest mature leaf material that is typically avoided or indigestible 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 a seasonally poor diet, a diversity of diets from seed-eating (Presbytis rubicunda, Davies 1984; Colobus satanus, McKey and Waterman 1982) to unripe fruit (Procolobus badius, Struhsaker 1975) and even ripe fruit (Presbytis pileata, Stan- ford 1989) have been reported. This probably indicates that colobines, while able to respond to local ecologies, tend to subsist on a diet that is low in mature leaves but switch to preferred fruit and leaf flush whenever possible. It also sug- gests that the colobine digestive adaptation may vary among species in form and function rather than be a uniform suite of morphological and physiological traits that aid in the digestion of low-quality foods. Most colobines live in territorial one-male groups (Table 1). Males disperse from these groups at or before sexual maturity, or are driven off by the resident male, though exceptions exist in which subadults remain in their natal groups to breed. Females transfer between groups in many species; the earlier view of social units that are essentially closed except for the dispersal of young males and invasions by outside males is almost certainly simplistic. Little data exist on female dominance relationships and where they have been documented dominance is most often simply labelled "strong" or "weak". Female dominance relations, or the lack of them in most colobines, are important because they may be re- lated to the relatively high rates of female emigration observed among colobines (Stanford in preparation). McKenna (1979) viewed the relationships between female colobines to be strongly influenced by the uniform distribution of their leafy diets, which minimized intragroup competition and allowed a weakening of the dom- inance hierarchy. The assumption that colobines use leaves as a year-round staple diet has been questioned, however, and such a dietary basis for dominance is not clear (Stanford 1989). As field data accumulate on more colobine species, most species living in one-male groups have been reported to have a regular if unknown rate of female transfer (Stanford 1989; Moore and Ali 1984; Davies 1987; Bennett 1983). It is therefore probably incorrect to classify the social systems 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 is a continuum of female transfer rates. For exam- ple, some red colobus populations have 100% female dispersal (Kanyawara, Kibale, Uganda; Struhsaker 1975), while others are characterized by a much lower and perhaps variable frequency (Tana River, Kenya; Marsh 1979; Smith pers. comm.). Despite numerous field studies and thousands of observer hours female transfer has rarely been reported in Hanuman langurs. Thus, there appears to be wide variation in the pattern and frequency of female transfer among members of the Colobinae. The implications of both this inter- and intra-specific variation will be dis- cussed below. 23 Q% 00~ ~ ~ ~ ~ ~ ~~~~~~~~~~~~~~~~~~~0 ~~~~ 0 _ _ _ 0% I0 ON %oo en o 00' ~ 00 00 W-4~~b~ 00 3 ?O 4) 44 4 )~4), )(q44 44 r ~ ~ ~ 4 C-.0 cl - - C- -- 4)~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~~4 cl. o CA2 > 00 00 } = ; i i0 A 24 The dietary categories in Table 1 are neces- sarily vague, as a monkey that feeds heavily on leaves during one or two seasons may be highly frugivorous or a seed specialist in other parts of the year. Since the time span over which pri- mates balance their, diets and energy budgets is unknown, the potential importance of seasonal variation in diet for analyzing both feeding ecol- ogy and evolutionary and ecological influences on the social system is presently unmeasurable. Travel leadership is presented for those species for which it has been systematically reported; un- like the literature on baboon behavior, where the determination of the timing and direction of group movement has been studied (Sigg and Stolba 1981; Rhine and Westlund 1981), patterns of group travel in arboreal forest monkeys are poorly known. The significance of female lead- ership, discussed below, is hard to establish because it is often unobservable in dense foliage or rapidly moving groups and sub-groups, and when it is observable, fieldworkers have failed to record it systematically. The Capped Langur The capped langur (Presbytis pileata, Figure 1) is found in the eastern portion of the Indian Figure 1. Capped langur monkey (Presbytis pileata durga) in Madhupur National Park, Bangladesh. subcontinent. It lives exclusively in one-male groups of four to thirteen animals. During 1400 hours of observation over 15 months, three adult females immigrated into five study groups, and these immigrations were accompanied by female solicitation of and copulation with the resident male. No male changes were observed, and at least one resident male maintained his tenure for at least 26 months. Capped langur groups occupy widely overlapping home ranges, no part of which were ever observed to be defended against other groups. Food trees were also unde- fended. During the rainy season, capped langurs at Madhupur switched their dietary habits from predominantly mature leaves to ripe and unripe fruit. Although feeding competition theory pre- dicts that widely dispersed fruit sources should be competed for more intensely than abundant leaves, capped langur groups showed no greater rates of aggressive displays during intergroup encounters when they fed heavily on fruit than when they ate mainly leaves. Groups encoun- 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- lance, but tension was rarely observed. In contrast, encounters between one-male groups and extra-group males were tense and often 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 of food 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 tested with regard to their ecology and mating system: 25 1) Females should lead groups during the group's daily range path, as the relatedness of adult females is expected to contribute to each female's inclusive fitness benefit in enhanced foraging efficiency and food-getting. 2) If high quality but widely dispersed food patches are preferred, they should be contested for by different groups sharing the home range. If they are not overtly competed for, then a clear intergoup dominance relationship should be dis- cemable that mediates the frequency and intensity of such encounters over food sources. 3) Females should cooperate in aggression du- ring such intergroup encounters, as they have a mutual inclusive fitness stake in defending food sources from neighboring groups. 4) Females should in general show affiliative behavior towards one another, in the form of alliances, grooming relationships and higher fre- quencies of spatial association among themselves than between themselves and the group male. Only the first of these assumptions was found to be true for capped langurs (Stanford 1989); females determined the timing and direc- ton of virtually all group travel during ranging. Even though during the rainy season ripe fruits were the most preferred food source, neither the frequency nor the intensity of intergroup encoun- ters increased significantly in spite of the longer distances travelled to reach fruit trees. Affiliative levels among females were relatively low; fe- males spent little time in close proximity (< 1 meter) to one another or to the group male (on average less than 4% of the active time of each female). Because capped langur groups have broadly overlapping home ranges and do not contest food sources aggressively, it is likely that intergroup encounters in this species are related primarily to mate defense and female transfer. It would be unwise to speculate on the cognitive processes or motivation that prompt female emigration, but the protective/coercive behavior shown towards fe- males by their group males during encounters with other males suggests that females use inter- group encounters to evaluate conditions in other one-male groups, or to assess the quality of a lone 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 measurable economic factors: the degree of defensibility of food sources and the level of food abundance. Mitani and Rodman (1979) attempted to predict when a primate group should defend food sour- ces according to the overall home range size in relation to the group's daily range length. If day range is insufficiently long to effectively monitor the perimeter of the group's range, then food sources are considered economically indefensi- ble. Following this prediction, capped langurs at Madhupur should be expected to defend fruit trees during the rainy season, when their day range increases substantially and all groups feed heavily on ripe fruit witiin their overlapping 20 hectare home ranges. During the dry winter months, when mature leaves are the staple, day range is shorter and the economics of food source defense different; no defense is expected in this season. In fact, the animals never defended food sources, even when they were feeding on high quality clumps of fruit. The other variable, the abundance of food in the habitat, is more difficult to measure. Vegeta- tion analysis showed that few of the monkeys' food trees were clumped in distribution, and overall tree species diversity was quite low -- 28 species comprised nearly all of the animals' feeding records. During the dry season, approxi- mately 70% of all Madhupur trees were more or less bare of foliage (Stanford 1989). Patch size of the most commonly eaten food, the young and mature leaves of Wrightia tomentosa (Apocyna- ceae), was uniformly small (average trunk dia- meter at-breast-height of individuals in sample transect = 6 cm). The monkeys fed on the mature and often dessicated leaves of whatever trees were in leaf and also fed on herbaceous ground cover 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 the monkeys travelled further each day and spent more total time moving to reach them. The trees were not, however, competed for in an aggres- sive sense; even when two or three groups attempted to feed at the same tree, they either oc- cupied opposite edges of the tree crown (for large Ficus trees) or waited for one group to finish before entering the tree. There was no consistent dominance relationship among the five main study groups. If females in female-bonded groups should be expected to enhance their reproductive success by competing successfully for patches of high- quality foods, then the food must conform to two patterns: it must be defensible and there must be enough 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 26 to be defined by ecological primatologists in whatever way is best suited to the model at hand, rather than according to energy maximizing pnn- ciples drawn from foraging theory (Stephens and Krebs 1986). Its use by primatologists varies and the concept is often used incorrectly to sup- port assertions about the influence of ecology on social structure. Is a species that feeds exten- sively on leaves limited in the same way as is a frugivorous species? In foraging theory, the cru- cial difference is that leaves tend to be eaten only partially while fruits are more often consumed en- tirely. While some would argue that the problem is simply one of properly identifying the patch and measuring the energetic costs and benefits of exploiting it, it is important to note that there are important 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 social structure directly to patch size, the size of food patches undoubtedly differs widely across the range of chimp habitats and there is no evidence that chimp social organization varies with it. The implication of capped langur socioecol- ogy is that this species and other leaf-monkeys belie the utility of female- or non-female-bonded taxonomies. This may be true for nonhuman pri- mates in general (Stanford in preparation). The question then is how to explain complex social systems in which there are different and variable rates of both male and female dispersal. Female lions, for instance, emigrate at varying rates in different populations but the result is the same: females that transfer breed later and suffer higher mortality than those who do not (Pusey and Packer 1987). Specific levels of emigration by females in a male-dispersal social system may be selected for, but the ecological or demographic factors that would mediate dispersal by only some rather than by all females are unknown. Possibly a small proportion of females can obtain benefits in the form of enhanced mating success or nutritional advantages in the form of reduced intra-sexual competition by emigrating, but selec- tion against inbreeding may prevent large scale migration by females in species characterized by male dispersal. Small numbers of females might benefit by ending up as "novel" females in other, smaller groups while a large influx of females would not be favored. Models of purported in- tragroup cooperation in resource defense are also not readily operationalized. This sort of fre- quency dependence could produce the variation in dispersal patterns seen without invoking un- wieldy inclusive fitness arguments that rely on such models of intragroup cooperation. Why there 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 Wrangham and others between "female-bonded" and "non- female-bonded" species is falsified by the range of mating systems and dispersal patterns found among the colobines; and 2) regardless of the ma- ting system taxonomy used, levels of intergroup food competition vary widely between species and do not necessarily follow the axiom that high quality food sources produce intense intergroup competition which would favor individuals toler- ating group life for the sake of access to better food. Female-bonded models are ultimately exten- sions of resource-defense polygyny models of avian social systems. Among many bird species, males compete for territories rich in food and nest-site resources and females choose males on this basis (Emlen and Oring 1977). Variation in territory quality leads to differences in the repro- ductive potential of both males and females. In the avian model, males distribute themselves in space and influence the distribution of females on the basis of the females' choice of male territo- ries. In the primate model, females choose the spatial distribution according to resources and males attach themselves to single or multiple females in order to enhance their chances of suc- cessful mating. Control of females is the key to mating success in both models. For species that are not female-bonded, males do not defend a fixed spatial area (e.g., mountain gorillas). Mate defense polygyny is then inferred from the nature of intergroup encounters. The capped langur data show that mate defense polygyny and resource defense can be easily conflated in a territorial species. Capped langurs also teach us that as- sumptions about the costs and benefits of intergroup resource competition must take into account seasonal differences in the values of dif- ferent resources. Thus, the colobines in general illustrate the problems of applying unitary expla- nations to an exceedingly diverse set of primate social adaptations. CONCLUSIONS Vehrencamp and Bradbury (1984) point out that creating a taxonomy of mating systems according to any hierarchical ranking of the reladve importance of different behavioral options is faulty in that by focusing on one component, attention is drawn away from other potentially important influences. Although it might be argued that this is unavoidable in hypothesis 27 formation, the problem can be minimized by al- lowing for a mixture of behavioral strategies rather than the hierarchy of evolutionary pres- sures proposed by female-bonded taxonomies. Examples drawn here from the colobine monkeys should be sufficient to show that such a typology of female-bonded versus female-transfer primate societies is simplistic and, in portraying social systems as largely built around the single inde- pendent variable of female food competition, it fails to explain the range of social behavior seen in just one primate taxon. The preliminary alternative scenario presen- ted here for colobine social system evolution can be no more accurate than the female-bonded mo- del without more field data on the relationships between dispersal patterns and mating strategies and between ecology and intergroup relations. Future field studies of Old World monkeys will continue to reveal the complexity of social relationships within and among groups that con- founds attempts to construct predictive models of observed behavior patterns. I have previously suggested (Stanford 1989) a "frequency-dependent" interpretation of the primate field data on sex-biased dispersal and polygyny. The variety of mating systems in the colobines suggests a spectrum of rates of sex- biased dispersal and perhaps also a range of levels of aggression faced by immigrating males and females. Females should be expected to transfer because of the benefits they can receive in other groups (better access to food and mates), but increased transfer would not be favored as later arrivals fmd themselves in groups already occupied by previous immigrants. Although some strongly female philopatric primate species may fit the female-bonded and non-female- bonded taxonomy, most groups and even some species exhibit a continuum of dispersal, inter- group interactions and mating systems that have so far been given little attention and have defied genuine explanation. Ultimately the evolution of sex-biased dispersal in primates will have to be explained as it has been in other mammals. An evolutionary model of the behavioral options in- fluencing the formation of female-bonded versus non-female-bonded species is needed to stimulate testable hypotheses in this area. These effects would have profound influences on the way in which we currently view the evolution of primate reproductive 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 Thelma Rowell, Phyllis Dolhinow, Katharine Milton, Jim Moore and Nancy Krusko. Thanks to Susan Wagner for preparing Table 1. I also thank the government of Bangladesh and especially Abdul Wahab Akonda, M. R. Talukder and Erin Moore for assistance during periods of fieldwork be- tween 1986 and 1988. REFERENCES CITED Bauchop, T. (1978) Digestion of leaves in vertebrate arboreal folivores. In G.G. 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