Dominance Acquisition During Mammalian Social Development: The "Inheritance" of Maternal Rank 1

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1 AMER. ZOOL., 31: (1991) Dominance Acquisition During Mammalian Social Development: The "Inheritance" of Maternal Rank 1 KAY E. HOLEKAMP Department of Ornithology and Mammalogy, California Academy of Sciences, Golden Gate Park, San Francisco, California AND LAURA SMALE Department of Psychiatry and Behavioral Science, State University of New York, Stonybrook, New York SYNOPSIS. We first review the suite of general problems mammals confront during their social development, and then focus on the specific problem of how group-living mammals acquire their social rank. In particular, we examine maternal rank "inheritance" (MRI) in those mammals for which maternal rank is the primary determinant of female rank. This occurs in many primates and in spotted hyenas. Young primates and spotted hyenas usually attain their adult status in two stages: they first attain ranks correlated with those of their mothers in peer interactions, and subsequently challenge and outrank older conspecifics subordinate to their mothers. Observational learning may be necessary, but is not sufficient, for MRI. In some primates, but not hyenas, youngsters appear to learn their ranks from direct aggression against them by higher-ranking adults. Third-party support appears to promote MRI in all species examined: the probability and style of maternal interventions on behalf of infants often vary with rank, and both kin and nonkin frequently form coalitions that may assist juveniles during rank reversals. INTRODUCTION In order to survive, grow, and eventually reproduce, mammals must solve a suite of problems during their social development. First, the neonate must discriminate animate objects, which tend to be both mobile and labile, from inanimate ones. Second, the young mammal must solve a host of problems related to identification and recognition of the animate objects in its environment. Specifically, it must come to recognize the individuals with whom it might interact, and discern how they relate to each other. Third, the young mammal must develop skills necessary for competition and cooperation with conspecifics. Although mammals are born with at least rudimentary communication skills, these must be elaborated and perfected. Successful competition may involve either acquiring combat skills or developing alternative tactics for resource acquisition. In some species, 1 From the Symposium on Animal Behavior: Past, Present, and Future presented at the Annual Meeting of the American Society of Zoologists, December 1989, at Boston, Massachusetts. 306 youngsters must develop skills necessary for participation in coalitions and alliances, post-aggression reconciliation skills, skills necessary for filling specialized social roles, and even skills necessary to deceive conspecifics (e.g., Byrne and Whiten, 1985). Most importantly, the young mammal must determine which individuals can be overcome by whatever means in competition for resources, which individuals cannot, and how this varies with context. Fourth, if the young animal successfully disperses from its natal area, it must familiarize itself with at least one entirely new group of conspecifics in the immigration area, and establish its own social position with respect to these unfamiliar animals. Fifth, the individual must eventually select or acquire mates, and develop skills necessary for courtship and copulation. Finally, the individual must develop skills necessary for raising its own offspring until they can survive independently. The magnitude of each of these problems, the mechanisms operating in their solution, and the temporal characteristics of their occurrence vary greatly across species. In what follows we examine one aspect

2 ONTOGENY OF DOMINANCE 307 of the problem of how young mammals develop competitive and cooperative relationships with conspecifics. Specifically, based on our own work and that of others, we examine how the individual establishes its own social position. We use the term "social position" interchangeably with "rank," "status," and "dominance," all of which refer to the individual's priority of access to resources necessary for survival and reproduction. We use two behavioral measures to infer an individual's social rank. The first is an individual's ability to displace others from a desired resource, and the second is the occurrence of appeasement or submissive behavior during dyadic encounters. We refer to the displaced individual, or the one exhibiting appeasement behavior, as the subordinate. Both displacement and appeasement may occur with or without any preceeding aggression. Social dominance is a relational concept, and rank relations may vary with the contexts in which they occur (e.g., Rowell, 1974; Bernstein, 1981). Furthermore, rank relations may be extremely unstable, particularly within dyads including young animals that are not yet integrated into adult hierarchies, or dispersers that have recently joined new social groups. Nevertheless, dominance has proven to be a robust concept, useful in describing and predicting outcomes of social interactions in a large number of group-living organisms (e.g., Gauthreaux, 1978). In many species, outcomes of dyadic interactions are sufficiently predictable to permit description of the social order in terms of linear dominance hierarchies which may remain stable for extended periods (Hausfater et al., 1982; Samuels*?/ al, 1987). Each individual must establish its own social rank with respect to several categories of conspecifics. First, in mammals bearing multiple-offspring litters, each individual may establish a dominance relationship with its littermates. This has been described in members of the pig family (Suidae: e.g., Fraser et al., 1979; Byers, 1984) and in various carnivores (Scott and Marston, 1950; BekofF, 1989; Frank and Glickman, 1989). The factors influencing intralitter rank acquisition have not been well studied, but the likeliest causal variables appear to be birthweight, birth order, sex, and early aggressive and displacement interactions among littermates during nursing competition. Second, each individual must establish its own rank with respect to members of the opposite sex. In most mammals, members of one sex become socially dominant to members of the other. Male dominance over females is most common (e.g., many ungulates, most pinnipeds, many primates; Wilson, 1975), but female dominance over males occurs in some mammals (Rails, 1976; Smuts et al, 1989). Sex-biased natal dispersal may have a profound influence on intersexual dominance relations in some species (e.g., Frank etal., 1989). More commonly, adult-like intersexual rank relations are established as members of the dominant sex begin to outcompete others through development of greater size, strength, secondary sex characteristics and aggressiveness (Moyer, 1974; Clutton- Brock et al, 1982; Smuts et al, 1989). Finally, dominance relations are established among members of the same sex. This often occurs as individuals join breeding groups. Intrasexual rank may be acquired gradually by philopatric mammals as they mature in the natal group where they will mate (e.g., Smuts et al, 1989; Frank, 1986i). Among emigrants, intrasexual rank may be initially established after natal dispersal, and/or repeatedly during annual formation of breeding groups in seasonally breeding species (e.g., elephant seals, red deer, ground squirrels). Factors known to affect intrasexual social status are body size and other physical characteristics (Clutton-Brock et al, 1982), age (Goodall, 1986), tenure in the group (Sugiyama, 1976), coalition formation (Bernstein, 1976) and political maneuvering (de Waal, 1982). In some mammals, maternal rank is the most important determinant of social status among females. This phenomenon has been referred to as maternal rank "inheritance" (MRI: e.g., Harcourt and Stewart, 1987) and, although rank is not literally inherited, we adopt that terminology here.

3 308 K. E. HOLEKAMP AND L. SMALE TABLE 1. Species exhibiting maternal rank "inheritance." Species Primates Macaca M. fuscuta M. mulatta M. fascicularis M. arctoides M. nemestrina M. radiata Papio P. cynocephalus ursinus P. cynocephalus cynocephalus P. anubis Cercopithicus C. aethiops sabaeus Carnivores Crocuta C. crocuta Common name Macaques Japanese Rhesus Java Stumptail Pigtail Bonnet Baboons Chacma Yellow Olive Vervets Spotted hyenas MRI has been documented in several species of three genera of Cercopithicine primates {Macaca, Papio and Cercopithecus: Table 1), and in spotted hyenas (Crocuta crocuta: Frank, 1986&). These species are characterized by female philopatry and male dispersal (Smuts et al., 1989; Frank, 1986a; Henschel and Skinner, 1987). All live in permanent social groups containing more than one breeding male. In all of these species, maturing females acquire social ranks adjacent to those of their mothers and, in most, young females come to outrank their older sisters ("youngest ascendency"; Walters and Seyfarth, 1989). MRI appears to be a complex behavioral phenomenon requiring frequent longterm exposure to a particular group of conspecifics, substantial overlap in space and time between members of consecutive generations, some clumping of vital resources in the natural habitat, and a well-developed ability for social learning. Only primates and hyenas have been sufficiently wellstudied to date to reveal this form of rank acquisition. However, further study may reveal an influence of maternal rank on offspring rank in other highly social, longlived mammals with widely divergent ecologies, such as elephants and odontocete cetaceans. In what follows, we describe developmental changes in rank-related References Kawai, 1958, 1965; Koyama, 1967 Sade, 1967, 1972; Missakian, 1972 Angst, 1975 Estrada, 1978 Bernstein, 1969 Silket al., 1981 Cheney, 1977 Hausfater, 1975; Lee and Oliver, 1979; Hausfater et al., 1982 Scott, 1984; Johnson, 1987 Cheney et al., 1981; Horrocksand Hunte, 1983 Frank, 1986i; Smale and Holekamp, 1989 social interactions among young primates, discuss potential mechanisms by which maternal rank influences offspring rank, and then compare primates and hyenas with respect to the development of rank relations. MATERNAL RANK "INHERITANCE' PRIMATES: DESCRIPTION In most of the primate species studied to date, acquisition of maternal rank occurs in two major stages. Young monkeys first establish their own social positions within the peer group, and subsequently work their way into the adult hierarchy. Establishment of rank-relations with peers Rank relations among young primates are strongly influenced by the presence of conspecifics. Kawai (1965) distinguished between "basic rank," expressed during isolated dyadic encounters, and "dependent rank," expressed during encounters occurring in the presence of animals that might support one participant. Among immature vervets and macaques of both sexes, dependent rank is perfectly correlated with maternal rank, but basic rank is determined by age or physical strength (Koyama, 1967; Horrocks and Hunte, 1983). Among young macaques there is eventually a transition in which the mater- IN

4 ONTOGENY OF DOMINANCE 309 nally-determined dependent rank-order becomes the basic rank-order, which is subsequently maintained in the absence of the mothers (Koyama, 1967; Missakian, 1972; de Waal, 1977; Bernstein and Williams, 1989). In juvenile olive and yellow baboons, pronounced sex differences exist in the organization of dominance relations; social rank is highly correlated with maternal rank among young females, but only body size and age are effective predictors of rank among males (Lee and Oliver, 1979; Johnson, 1987). In contrast to these other Papio species, a combination of maternal rank and age predicts 90% of agonistic interactions among immature chacma baboons of both sexes (Cheney, 1977). Establishment of rank-relations with adults Juvenile macaques and baboons are initially subordinate to all adults but, as they mature, they begin to reverse certain of these early dominance relationships (Bernstein and Williams, 1989; de Waal, 1977; Walters, 1980). The adult member of an adult-juvenile dyad undergoing a dominance reversal is referred to as a "targeted" animal (Walters, 1980), and is usually of lower rank than the juvenile's mother. Early in the reversal process, a juvenile Java macaque begins to aggress against a targeted adult, soliciting aid from conspecifics as it proceeds; the targeted animal generally flees, but does not exhibit submissive behaviors to the juvenile until the end of the reversal process (de Waal, 1977). This process appears to be quite similar in female yellow baboons, and four stages of dominance reversals between adolescents and adults have been identified in this species (Walters, 1980). Initially, the adolescent in a given dyad exhibits submissive behavior to the targeted adult, which exhibits aggressive behavior. Second, the adolescent exhibits both aggressive and submissive behavior to the targeted adult. Third, the adolescent ceases to submit to the adult, and both animals exhibit only aggressive behavior. Finally, the adult ceases to behave aggressively, and begins to submit to the adolescent. At this point, the targeted adult appears to accept its new subordinate role vis-d-vis the juvenile. Interestingly, adolescents are often able to non-aggressively displace adults before aggressive-submissive interactions have been reversed (Walters, 1980). In what types of dyadic relationships, then, do reversals occur? Juvenile female macaques and baboons challenge adult females outranked by their mothers, but the period during which reversals occur may extend into adolescence or even adulthood (Koyama, 1967; Walters, 1980; Bernstein and Williams, 1989). The changing patterns of dominance relations are more complicated in young male primates, whose status is influenced by both body size and maternal rank (Koyama, 1967; Koford, 1963; Lee and Oliver, 1979; Johnson, 1987). Juvenile male rhesus initially work their way up the adult hierarchy, as do females (Bernstein and Williams, 1989). Sons of high-ranking rhesus females may eventually assume higher ranks within the adult male hierarchy in their natal troop than would be predicted by their age, whereas sons of low-ranking females drop in rank and become peripheralized (Koford, 1963). Juvenile male olive and yellow baboons can displace adult females ranked below their mothers, but are consistently displaced by adult females that outrank their mothers (Lee and Oliver, 1979; Johnson, 1987). As they reach puberty, however, the influence of maternal rank on young males diminishes, and they come to outrank their own mothers and other, higher-ranking adult females larger than themselves. Young male baboons are never able to displace adult or subadult males larger than themselves (Lee and Oliver, 1979; Johnson, 1987). Dominance reversals are rare in vervets compared to macaques and baboons because, in the earliest interactions observed between juveniles and adults ranked below their mothers, the juvenile threatens the adult, which ignores or defers to the juvenile (Horrocks and Hunte, 1983). Thus, unlike macaques and baboons, young vervets appear to hold dependent ranks adjacent to those of their mothers from the outset (Horrocks and Hunte, 1983).

5 310 K. E. HOLEKAMP AND L. SMALE MATERNAL RANK "INHERITANCE" IN PRIMATES: MECHANISMS The changing interaction patterns described above raise many questions about the mechanisms of rank acquisition. For example, how is dependent rank established among peers and how does this become an animal's basic rank? How are young animals able to reverse rank relations with targeted animals much larger than themselves, and how do they choose animals to target? A variety of hypotheses have been proposed to explain the development of maternally "inherited" dominance structures. Genetic heritability of rank-related traits The first possibility is that genetic inheritance of rank-related behavioral tendencies or physical characteristics accounts for MRI. A variety of data are incompatable with this hypothesis (de Waal, 1977). For example, in many species, when a mother's rank changes so does the rank of her juvenile offspring (Johnson, 1987; Marsden, 1968). Rank relations in some species are characterized by long periods of stability punctuated by brief, turbulent periods of rapid and substantial change (Samuels et al., 1987). In captive situations the social dependence of dominance status can be demonstrated by changing the social environment and observing subsequent rank reversals (Bernstein and Gordon, 1980; Chapais, 1987; Marsden, 1968). The difference between an individual's basic and dependent rank also demonstrates an important influence of other group members on status (de Waal, 1977). All of these patterns are difficult to reconcile with an explanation of MRI based on genetic heritability. Observational learning There is a prolonged period during which the young primate remains in close contact with its mother. Therefore the infant can observe its mother's rank-related social interactions long before the infant begins to engage in agonistic interactions with conspecifics. The infant may perceive its mother's social rank early during development and learn its own position through imitation or identification with the mother (Kawai, 1965). Maternal status influences many facets of an infant's earliest non-agonistic social experience (Gouzoules, 1975; Caine and Mitchell, 1979; Pereira and Altmann, 1985), and thus may indirectly promote the infant's awareness and passive acceptance of its rank (Altmann, 1980; Walters, 1980). The difference between an individual's dependent and basic ranks, however, suggests that young primates do not passively accept their social positions (Horrocks and Hunte, 1983). A large juvenile with a lowranking mother resists and dominates a smaller youngster with a high-ranking mother when the latter's mother is not nearby. Thus, observational learning alone cannot determine basic rank relations among immature primates, but dependent rank may be learned by observation. Careful study of the earliest rank-related interactions among infants is required to establish whether maternal rank determines offspring rank at the outset, or only after an early period of trial and error learning. Walters (1980) suggested that infant female yellow baboons learn their birthranks through early observation and nonagonistic social interactions, and that this early learning determines their subsequent choices of which adults to target for dominance reversals. Although this may be true, early observational learning cannot ensure that such challenges will be successful, particularly if the juvenile's mother later falls in rank (Datta, 1986; Johnson, 1987). Thus observational learning during infancy might be necessary, but is clearly not sufficient, for acquisition of maternal rank. Observational learning might also function importantly in another very different way. As group members come to associate an infant with its mother, they might equate the infant's rank with that of the mother. If this is true, then conspecifics should perceive changes in the rank appropriate for a juvenile when its mother's rank rises or falls, but not if its mother disappears. In so far as they influence patterns of coalition formation (see below), conspecifics' perceptions may be important determinants

6 ONTOGENY OF DOMINANCE 311 of the ranks attained by young primates. This hypothesis is consistent with data from olive baboons, in which a female over three years old can maintain a rank equal to her mother's if the mother dies, but her rank falls if the mother's rank falls (Johnson, 1987). Aggression by adults against infants In some species, aggression by adult females against the offspring of lowerranking females may promote the development of a rank-order among juveniles parallel to that among their mothers. Infant vervets are not involved in agonistic interactions until after they become frequent targets of aggression by adult females. This aggression, which Horrocks and Hunte (1983) call "harassment," is directed most frequently at infants whose mothers are low-ranking, and more frequently towards females than males. Soon after the harassment begins, offspring of high-ranking mothers begin to aggress against those of low-ranking mothers; the latter respond with deference. Although early harassment by adult females may shape the development of dependent rank among juveniles, it does not appear to influence basic rank, which is determined by body size in this species until at least three years of age (Horrocks and Hunte, 1983). Maternal rank influences the degree of harassment by adults against infant rhesus macaques who have not yet established a peer hierarchy (Berman, 1980), and also against young stumptail macaques (Gouzoules, 1975), bonnet macaques (Silk et al., 1979), and yellow baboons (Lee and Oliver, 1979). The temporal relationship between the onset of this aggression and the development of rank-related behaviors is unclear in these latter three species. Maternal interventions, coalitions, and alliances Many rank-related social interactions of young primates involve alliances or coalitions. A juvenile's ally may be its mother, other kin, or unrelated group members. Allies may protect the target of an aggressive act, or they may join an aggressor against its target. In most species, alliances of some sort appear to be important factors in rank acquisition, and a variety of alliance-based models have been developed to account for MRI. Maternal interventions on behalf of offspring. Immature chacma baboons of both sexes often receive protective support from their mothers when they are threatened or attacked by conspecifics, and the frequency and effectiveness of this support are positively correlated with maternal rank (Cheney, 1977). Cheney (1977) concluded that maternal interventions are a major factor promoting acquisition of rank among immature baboons, and suggested that the probability of effective maternal protection influences the frequency with which youngsters counterattack when threatened. Frequent maternal interventions in chacma baboons might account for the greater impact of maternal rank on dominance among immature males in this species than in olive or yellow baboons, in which maternal interventions are very rare (Johnson, 1987; Lee and Oliver, 1979; Walters, 1980). Among vervets the probability of maternal intervention in disputes involvingjuveniles is positively correlated with maternal rank, and mothers never intervene against opponents higher-ranking than themselves. Horrocks and Hunte (1983) suggested that maternal interventions are important for the maintenance but not the acquisition of rank in this species because, in contrast to baboon and macaque mothers, vervet mothers are far more likely to intervene when their offspring initiate aggressive interactions than when they are victims. However, if infants initially aggress against peers irrespective of their targets' maternal ranks, then selective reinforcement of aggression against infants of lower birthrank might reduce the number of peer targets against which aggression is directed. Prior to the emergence of a hierarchy among infant rhesus macaques, the protection received by infants is determined by maternal rank (Berman, 1980). Although the probability of protective intervention by mothers is unrelated to rank, infants of high-ranking mothers have more female relatives, spend more time in

7 312 K. E. HOLEKAMP AND L. SMALE proximity to them, and are more likely to receive protection from them than are infants of low-ranking females. Furthermore, protectors of infants from low-ranking lineages are especially fearful as they intervene. Conspecific support of juveniles during reversals. In many species third party support appears to facilitate MRI by promoting rank reversals in juvenile-adult dyads in which the juvenile's mother outranks the adult (Datta, 1983, 1986; de Waal, 1977; Walters, 1980). Conspecifics may ally themselves with juveniles prior to or during the rank-reversal process. Before reversals begin, protective support to juvenile rhesus threatened by older dominant animals is influenced by the rank of the aggressor relative to that of the juvenile's mother. When the juvenile's mother outranks the aggressor, conspecifics joining in support of the juvenile usually elicit submissive behavior from the aggressor; this is not the case when the aggressor outranks the juvenile's mother (Datta, 1986). The experience of effective protection against an opponent may eventually lead the juvenile to challenge that opponent (Datta, 1986). When they challenge adults outranked by their mothers, juvenile macaques and baboons frequently solicit and receive help from conspecifics (de Waal, 1977; Datta, 1983; Netto and van HoofF, 1986; Walters, 1980). The rate at which immature monkeys receive coalitionary support is correlated with their mother's rank (Cheney, 1977). Interestingly, most of this coalitionary support is provided by non-relatives (de Waal, 1977; Walters, 1980). This third party support almost certainly helps juveniles challenge and outrank adults ranked below their mothers. Juvenile support of conspecifics during reversals. In addition to receiving third party support, juveniles of many macaque and baboon species frequently join in aggressive disputes initiated by others (Cheney, 1977; de Waal, 1977; Walters, 1980). They often join against targeted adults with whom they have unstable rank relations (de Waal, 1977; Walters, 1980), and they tend to join on the side of high-ranking adults or of peers whose mothers are higher-ranking than their own (Cheney, 1977). These coalitions rarely change the outcome of disputes because juveniles always join the winning side (Cheney, 1977; de Waal, 1977). By joining high-ranking animals, a youngster may opportunistically defeat an opponent with which its relationship is unstable, and thereby more directly or rapidly come to outrank that opponent (Chapais, 1988). In addition to attaining these immediate benefits, young primates may form coalitions because of the potential benefits of later reciprocal support from the animals with which they have joined (Cheney, 1977). MATERNAL RANK "INHERITANCE" IN SPOTTED HYENAS Spotted hyenas are large carnivores that live in social groups ("clans," Kruuk, 1972) containing 5 (Mills, 1984; Tilson and Henschel, 1986) to 80 individuals (Frank, 1986a). Adults of each sex can be ranked in a linear dominance hierarchy (Frank, 19866; Tilson and Hamilton, 1984), and all adult females dominate all immigrant adult males (Kruuk, 1972). As in Cercopithecine monkeys, the social ranks of subadult hyenas are highly correlated with their mothers' ranks (Frank, 19866). Youngest ascendency also occurs but, unlike the situation in monkeys, both male and female hyenas come to outrank their older siblings. The "inheritance" of maternal rank in spotted hyenas raises the question of whether the same developmental mechanisms promote rank acquisition in this species as in Cercopithicine primates, despite their strikingly different ecologies. We have been studying social development in spotted hyenas of one large study clan in the Masai Mara National Reserve, Kenya, since June, Except where otherwise stated, the information we discuss here on rank acquisition comes from this ongoing work, conducted in collaboration with L. G. Frank. Unlike primate development (Pereira

8 ONTOGENY OF DOMINANCE 313 J G O H g" u tn B o - 1 A 0 E F B WINNERS M-RANK AGE F F F M M M M F F M M M F SEX S J G Q H M B A O E F B R I D FIG. 1. Cub dominance matrix yielded by outcomes of agonistic interactions over food during an hourlong "bone test" administered at the communal den February 19, and Altmann, 1985), hyena development is clearly partitioned into stages by discrete environmental changes. Hyenas are usually born in an isolated natal den where a single female maintains her offspring for the first few weeks of its life (Kruuk, 1972). Dominance relations between siblings are worked out during this early stage (Frank and Glickman, 1989). At approximately one month of age the young hyena is carried by its mother to the clan's communal den, where offspring of several females reside concurrently until cubs are 5 to 8 months old (Kruuk, 1972). Upon arrival at the communal den the young hyena's social world is suddenly expanded to include unrelated mother-offspring pairs and other clan members who pay frequent visits to the den. Cubs exhibit high rates of submissive behaviors to conspecifics of all agesex classes when they first arrive at the communal den. Initially cubs spend most of their time underground, and emerge mainly to nurse, so most of a cub's time with its peers is spent inside the den. Because the den's interior is inaccessable to adults, unlike primates, hyena cubs cannot depend on their mothers for support in their early interactions with peers. UJ o a. 0- o <r a. n (44) (52) (46) AGE OF AGGRESSOR (MONTHS) FIG. 2. Ontogenetic change in cub aggression against peers at the communal den. Targets were considered to be "appropriate" if their mothers were lower-ranking than the aggressor's, and "inappropriate" if their mothers were higher-ranking than the aggressor's mother. Sample size represents number of targeted animals. Except for rare incidents in which mothers provision their young with meat (Holekamp and Smale, 1990), cubs at the communal den have little to fight over, and levels of aggression among peers are low. Nevertheless, by four months of age a nearlinear hierarchy exists among peers, but dominance status is unrelated to maternal rank, or to the size or sex of cubs (Fig. 1). By six months of age cubs' rank-order has changed such that, even in the absence of adult females, dominance status among peers is perfectly correlated with maternal rank (Smale and Holekamp, 1989). MRI apparently involves a learning process during which the range of conspecifics against whom cubs direct aggression narrows during early development to include only those of lower rank than the aggressor's mother (Fig- 2). When they leave the communal den, cubs begin to participate in the intensely competitive feeding situations characteristic of this species (Kruuk, 1972). Young hyenas are confronted with the task of eating as much as possible amidst an excited, aggres-

9 314 K. E. HOLEKAMP AND L. SMALE TABLE 2. Summary of data relevant to three mechanisms by which maternal rank might be "inherited.' I: Establishment of rank relations with peers: 1) Juvenile acquires dependent rank 2) Dependent rank becomes basic rank II: Establishment of rank relations with adults: 1) Target selection 2) Rank reversals I: Establishment of rank relations with peers: 1) Juvenile acquires dependent rank 2) Dependent rank becomes basic rank II: Establishment of rank relations with adults: 1) Target selection 2) Rank reversals Observation? Macaques? Baboons? Hyenas? Macaques + Baboons? Hyenas Third parly support Harrassment + Macaques? Baboons + Vervets Hyenas? Macaques? Baboons? Hyenas Kin join juvenile Non-kin join juvenile Juvenile joins others + Macaques ± Baboons + Vervets + Hyenas + Macaques ± Baboons + Vervets + Hyenas? Macaques? Baboons? Hyenas + Macaques + Baboons + Hyenas? Macaques? Baboons? Hyenas + Macaques + Baboons + Hyenas * (+) data suggest the mechanism operates. ( ) data suggest the mechanism does not operate. (±) data suggest the mechanism operates in some species but not in others. (?) no data yet available. sive crowd of conspecifics, without suffering serious injury. Maternal rank is an important determinant of how successful cubs are during these group feeding situations (Frank, 19866). After leaving the den, rank-ordering among peers continues to be correlated with maternal rank, and unrelated to sex. During this period young male and female hyenas begin to challenge adult females ranked below their mothers. Most, but not all, of the factors promoting MRI in primates also appear to operate in hyenas (Table 2). Young monkeys and hyenas have myriad opportunities to observe agonistic interactions among conspecifics, including their mothers, and may thereby learn their mother's social rank before they establish their own. However, in both taxa observational learning of social relationships may be necessary but appears not to be sufficient for MRI. Direct aggression by adults against offspring of lowerranking females may teach young primates their social positions, but this apparently does not occur in hyenas. Defensive maternal interventions on behalf of offspring occur frequently in both taxa, and appear to be constrained by maternal rank. These interventions may function to "teach" both the youngster and other conspecifics the youngster's status. Defensive interventions by close female relatives other than the mother are extremely rare in hyenas. Finally, agonistic disputes often involve coalitions in which individuals invariably join the side that ought to win, according to the "rules" of MRI. Coalition formation thus appears to function importantly in rank acquisition and maintenance in hyenas as well as in monkeys. Interestingly, in both taxa, the animals joining or being joined by youngsters during coalition formation are often unrelated to the youngster. Indeed, all members of both primate and hyena societies, not just a youngster's close kin, appear to behave in a manner that promotes and maintains a system in which maternal rank determines offspring rank. As a result of a complex suite of behaviors exhibited by youngsters and other members of the society, young animals are endowed with social ranks equivalent to those of their mothers. The behaviors exhibited by the youngsters themselves appear to be directed toward achievement

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