Richard Sociobiology Primate Field Studies

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Sociobiology: Primate Field Studies

A. F. Richard; S. R. Schulman

Annual Review of Anthropology, Vol. 11. (1982), pp. 231-255.

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Ann Rev. Anthropol. 1982. 11:231-55Copyright O 1982 by Annual Reviews Znc. AN rights reserved

SOCIOBIOLOGY: PRIMATEFIELD STUDIESA. I;: RichardDepartment of Anthropology, Yale University, New Haven, Connecticut 06520S. R. SchulmanSubdepartment of Animal Behaviour, University of Cambridge, Madingley,Cambridge, England

INTRODUCTIONSociobiology is concerned with the evolution and adaptive significance ofsocial behavior. Certain kinds of social behavior, such as aggression, arereadily explained by Darw in's concept of individual selection. In con trast,until recently acts of altruism seemed to be in direct contradiction toDarwinian thinking [see Alexander (2) for a h istory of the subject]. The firstmajor step toward the resolution of this apparent paradox came with thedevelopment of kin selection theory (52, 65, 67). Today, the cornerstonesof sociobiological theory are models explaining the evolution of social be-havior not only by means of individual selection (e.g. 39, 152) and kinselection (15, 25, 28, 67-69,70, 95, 100, 154, 158, 169), bu t also by rec ipro-cal altruism (15, 150) and group selection (14, 15, 57, 94, 102, 151, 153,159-161).Our aims in this review are, first, to survey studies which have tried toapply these models to wild primates and, second, to discuss some of theresulting problems. In the process, we have found it impossible to avoid acertain arbitrariness of organization. To underscore the fact that th is is not,emphatically, a review of sociobiological theory as such [excellent reviewsalready exist (e.g. 15, 89, 97)], but rather an evaluation of the impact of

'Present address: Department of Biology, Princeton University, Princeton, New Jersey08540.


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232 RICHARD & SCHULMANsociobiology upon primate field research, we have chosen to order thereview according to the long-standing concerns of primatologists instead ofthe theoretical preoccupations of sociobiologists. By using traditional subdi-visions within the field, we have had to "force" certa in studies into sectionsin which they do n ot en tirely fit. The num ber of studies we review in detailis low. The past few years have seen an explosion of excellent, problem-oriented primate field studies, but we have limited ourselves primarily tothose which invoke sociobiological explanations explicitly.With these caveats in mind, let us turn to a review of applications ofsociobiological models to three broad classes of relationship, namelyfemales with females, males with males, an d ad ults w ith offspring. Then weshall look a t more general applications of these models to the evolution ofsocial systems.SURVEYRelationships Among FemalesEarly primate field studies generally described social relationships amongage/sex classes rath er than among individuals (e.g. 20). This was particu-larly true of female relationships. The picture began to change during thelate 1950s an d early 1960s with th e em ergence of research in which animalswere individually recognized and followed (60, 85, 88, 131). Consistentpatte rns of interaction am ong individual females were found, and a numberof attem pts have been made recently to provide functional explanations forthese patterns (23, 79, 81, 137).Hrdy & Hrdy (79) were the first to suggest th at relatedness and reproduc-tive value (52) were crucial to an understanding of rank relationships inmany female primates (see also 158). According to them, dominance rela-tions among female members of a langur (Presbytis entellus) social groupare organized into an "age-graded'' system. Older females not only defer toyounger ones, but also expose themselves to greater risks on behalf of thelatter in unreciprocated acts of altruism. This system, the Hrdys argued,reflects underlying changes with age in the reproductive value of females,close genetic relatedness of group members, and the attempt of all con-cerned to max imize their inclusive fitness. Specifically, since reproductivevalue (th e average expectation of futu re offspring of a fem ale of a given agerelative to a new born female's expectation) generally declines with age aftersexual maturity for most primates, the inclusive fitness of an aging femaleis disproportionately enhanced by protecting the kin component of thatfitness, namely her daughters and other closely related kin with high repro-ductive values. In contrast, directing altruism at old females near the endof their reproductive life is poor strategy for the younger generation, who


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PRIMATE FIELD STUDIES 233stand t o gain little in terms of the kin comp onent of their fitness an d to losemuch in terms of individual fitness.Rank relations am ong howler monkey (Alouata palliata ) females showparallels with the langur in that age and rank are inversely related in thisNew World folivore as well (8 1). In con trast with langurs, however, juvenilefemales leave their natal group as they app roach matu rity a nd en ter a newone. There they join the adult hierarchy at th e bottom but quickly rise inrank or leave. In Jones's words, the rule is "up or out." Jones's functionalinterpretation of this pattern invokes not reproductive value and inclusivefitness, but individual selection. Her argument is as follows. Agg ression isstrictly limited among all howler monkeys because they depend heavily onleaves which a re low in extractable energy so tha t animals cannot afford theenergetic costs of frequen t or intense aggression. The inverse relationshipbetween rank and age reflects a difference between (young) imm igrants an d(old) group members, not in the costs but in the potential benefits ofaggression. Membership in a group is impo rtant for survival and reproduc-tion, but only young animals are successful immigrants. They enter thehierarchy with low rank and leave if they do not achieve high rank quickly.Thus, an animal must gain entry to a group and rise in rank when youngif it is to achieve group membership at all (unless it colonizes a new resourcepatch). In short, the benefits of persistence during aggressive episodes aregreat for su ch individuals, whereas group residents do not lose their mem -bership in th e group by submitting to a young immigrant. Indeed, the costof aggression is too high fo r it to be wo rth their while persisting indefinitelyin aggressive bouts. Note tha t Jones does not explain why it is necessary toachieve high rank quickly in a new group in order to stay in it.Th e explanatory value of genetic relatedness and reproductive value hasbeen further explored in the context of macaque society. From data col-lected over 16 years (e.g. 114, 132) on the Cayo Santiago population ofrhesus macaques (Macaca mu latta) has emerged a highly consistent patternof rank relations among females. Daugh ters rank above all females to whomtheir mothe r is dominant, and below all females to w hom their mother issubordinate; daughters do not outrank their mo ther; by the time a femalereaches sexual ma turity she rises in rank above her older sisters. Schulman& Chapais (137) propose an evolutionary model to explain this pa ttern. O nCayo Santiago, the reproductive value of females peaks shortly after theyfirst give bir th an d declines steadily thereafter. Th e auth ors argue th at th eobserved rank order am ong adult sisters may be attributable to continuousma ternal favoritism of daugh ters with the highest reproductive value. Thisdoes not, however, explain the support a mother gives her very youngdaughte rs (with low reproductive value) against their older sisters (some ofwhom may have higher reproductive values). The vulnerability of young


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234 RICHARD & SCHULMANoffspring may be a confounding factor (23, 137, 138; S. B. Hrdy, personalcomm unication); less able to fend for themselves, they benefit dispropor-tionately from a given amount of aid.A sequel to this paper (23) presents a more general theory of femaledominance relations in primates. Using game theory [for a broad discussion,of its application in sociobiology see (62, 101-108)] and simulations basedon prevailing demographic values on Cayo San tiago, the authors found th ata simple sociobiological model of individuals acting in the ir own self interestwas consonant with th e structural characteristics of the observed hierarchy.From this they concluded that dominance hierarchies, maintained from dayto day by specific patterns of aiding and attraction, are actually an epi-phenomenon of the interplay of individual efforts to maximize inclusivefitness.A crucial element in Chapais and Schulman's model is the selectivesupport females give their offspring during internecine agonistic interac-tions as well as during interactions between daughters and other groupmembers. This class of behavior, known generally as fight interferencestrategies, has been explored by a number of primatologists in recent years.Findings from studies of who aids whom during fights in three differentmacaque species agree on the basic dynamics of fight intervention (83, 84,92,99). Macaques aid relatives against nonrelatives in fights. Furtherm ore,individuals tend to aid close relatives against distant relatives. (Althoughthe topic is not, in principle, relevant only to females, in p ractice, migrationof males out of their natal group m eans tha t most of the a ttention has beenfocused on females.) Genetic relatedness is not, however, the only factoraffecting patterns of aid. Differences in age and sex of contestants explainmuch of the residual variation, suggesting that reproductive value andvulnerability are important components as well (46, 92, 99, 138, 157).We note here, parenthetically, that the first significant contribution ofprimate field studies to sociobiological theory m ay be in this area. Implicitin all the studies of fight interference among primates is the idea that analtruist should dispense altruism comm ensurate w ith the degree of related-ness of recipients. Lewontin (96; see also 135) emphasized that this isactually an erroneous assumption and, citing explicitly the macaque studies,Altmann (7) pointed out that the idea of proportional investment is acomm on gambler's fallacy. Other things being equal, investment should beconcentrated on the most closely related relative. However, as Altmannnoted, additional factors such as diminishing returns on investments anddifferences in reproductive value and vulnerability will complicate the issue(23, 27, 157). For example, a monkey may reach a point when it hasgroomed away all, or nearly all, of the ectoparasites from its closest kin.Weigel(157) has recently explored a model of diminishing returns to al tru -


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PRIMATE FIELD STUDIES 235ism using a simulation approach. An investment strategy analogous toproportional dispensation of altru ism can arise under a diminishing returnsmodel, but the conditions under which it will do so probably occur rarely.Be this as it may, the striking empirical findings from studies of fightinterference behavior in three different macaque species seem to agree w itha proportional deployment regime. This suggests that current models areneglecting other imp ortant considerations such as, for example, the advan-tage derived from laying one's eggs in several baskets, or risk-spread ing (64,129, 139).A central assumption of most of the models discussed so far is that highsocial rank confers a reproductive advantage on females. This assumptionis largely untested. A study of gelada baboons (Th eropithecusgelada) in thewild showed that low-ranking females experienced more infertile cyclesthan did high-ranking females, perhaps because when the former were inestrus they were often harassed by the latter (48). Hence, there may be acorrelation between dominance and reproductive success in this species(46). Supporting evidence was also reported from provisioned island colo-nies of rhesus macaques some years ago (44, 134), but with th e accumula-tion of more d ata on provisioned macaques it now seems that the associationbetween female rank and reproductive success is much less clearcut (H.Gouzoules, personal communication). Furthermore, over a 4 year periodthere was no correlation between the two among wild rhesus monkeys inthe Himalayas (A. F. Richard, in preparation). Research on vervet monkeys(Cercopithecus aethiops) at Amboseli suggested that during a 3% yearperiod, morta lity in low-ranking females due to illness and restricted accessto resources was offset by greater predation upon high-ranking fem ales (29).The sample sizes are very small in all three studies of wild populations,however, and fu rther data are needed for a definitive test of the assumption.

The last study to be reviewed in this section represents a rather differentapproach from those considered above. Instead of constructing a model toexplain data already in hand, Kurland's (92) goal from the outset was totest the hypothesis that altruistic acts increase and selfish acts decrease asthe degree of relatedness between individuals increases. To this end, he an dhis wife studied Japanese macaques (Macaca fuscata) for nine months,collecting data on ac ts specified as altruistic or selfish. Like the Cayo San-tiago rhesus, the Japanese macaques living in forests adjacent to th e Japa-nese Prima te Research Center have been monitored for many years (85,86,88), and genealogical relationships through the maternal line were welldocum ented for all but six individuals included in the s tudy . Since paternitywas not known, coefficients of relatedness between dyads were calculatedassuming a probability of relatedness through the paternal line of 0.5.Kurland classed a number of activities as selfish or altruistic but here we


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236 RICHARD & SCHULMANshall consider only two, agonism and allogrooming, respectively designatedselfish and altruistic. The costs and benefits associated with these acts werenot m easured directly, and instead the a utho r explicitly assumed that thecost or benefit of a particular act is more or less constant. In accordancewith his initial hypothesis, he then used six classes of matrilineal relation-ship to predict the distribution of selfish and a ltruistic acts among animalsassigned to each class. Results showed a clear, positive relationship betweendegree of relatedness and frequency of allogrooming, but also a directional-ity not predicted by kinship theory. Kurland suggested that some of thisbias might be related to an interaction between reproductive value andinclusive fitness, and the rest to reciprocal altruism. In contrast with allog-rooming, agonistic behavior was not a linear function of relatedness, forhigh rates of aggression were found between mothers and offspring as wellas between individuals from different matrilines.Relationships Among MalesIn most primate societies males leave their natal group as they approachma turity while females spend their lives in the g roup into which they w ereborn. In general, then, females tend to be surrounded by female kin whilemales do so only to the extent that they migrate into groups already contain-ing male kin. The frequency with which this occurs is poorly documented.In a recent study of migrating males in the free-ranging rhesus colony atLu Cueva, Puerto Rico, Meikle & Vessey (1 12) found t ha t males were morelikely to transfer into social groups in which an older brother alreadyresided. The brothers spent more time near each other than near othermales, formed alliances more often, and disrup ted consorts involving broth-ers less often than those involving other males. In the wild, however, it isoften difficult to observe the fate of natal males once they have migratedfrom a focal study group, and genealogical relationships are rarely known.Perhaps partly because of the practical problem, kin selection theory hasbeen little used in explanations of the evolution of male-male relationshipswhich have focused instead on individual selection models.A striking feature of some primate societies is the rank ordering of adu ltmales. Although the importance of social dominance has been questionedrepeatedly (12, 54, 72, 127, 142), its explication nonetheless remains centralto many studies. In m ost instances, the general framework of research is anindividual selection model which assumes that high social rank increases amale's fitness by providing priority of access to limited resources such asfood and reproductively active females, and it asserts that individuals com-pete for high social rank and the benefits it confers (122). Evaluation of theassumption that high social rank increases a male's fitness has been the goalof a number of recent field studies as well as several more controlledlaboratory studies (e.g. 49, 121)


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PRIMATE FIELD STUDIES 237Hau sfater (73) investigated the relationship between dominance rank andreproductive success among the Amboseli baboons (Papio cynocephalus).Using data on adult male rank relations an d m ating behavior, he tested amodified version of Altmann's (5) priority-of-access model. The modelpredicted the frequency with which sexually matu re males of various rankswould copulate with an estrous female. If it is assumed that an estrousfemale will mate with the higher ranking of any two potential m ale partners,and that all other males are excluded from participation, then a m ale ofdominance rank r should mate with an estrous female only when thenumber of females simultaneously in estrus is greater than or equal to r.The field data did not fit the model's predictions. High ranking malescopulated at a low frequency but concentrated their efforts on those daysin the estrous cycle when conception was most likely to occur. Lowerranking males appeared to m ate as often as possible over a greater span oftime during a female's estrus even if they were aggressively excluded byhigh-ranking males during optimal conception days.In place of the linear priority-of-access model, Hausfater suggested sub-stituting a more complex model involving alternative, rank-dependent re-productive strategies (cf 147). Systems of this kind are not uncommonamong social species (128). Variations in reproductive success depend onvariations in the length of time males spend at different ranks. While it isconceivable tha t in their lifetime all males spend a similar amoun t of timeat different ranks, this has not been found to be the case in othe r polygynousmammals [e.g. elephant seals (93), red deer(56)l. Furthe rmore, in expand-ing populations males achieving high rank earlier in life will have greatergenetic representation in subsequent generations than males breeding later,even if both are high ranking for equal lengths of time. Hausfater concludedtha t the rank held by an animal over a period of a year or two was a poorpredictor of reproductive success and that data on the life histories ofindividual males would be needed to understand the biological and evolu-tionary implications of male-male relations as manifested in the baboondominance hierarchy.Post (123, 124) looked in detail at dietary differences among the A mboselibaboons, including in his sample individuals differing by rank and by sex.Like Hausfater, he was interested in th e costs and benefits associated withdifferences in social rank but used access to food instead of females as ameasure. Post did not uncover obvious, rank-related dietary differences.In marked contrast to the models discussed so far, Bygott's (19) modelexplaining the functional significance of relationships among adult malechimpanzees (Pan troglodytes) implies no selective advantage in high socialrank per se but rather suggests that all participants benefit from the stabilityto which a dom inance hierarchy gives rise. Th e chimpanzee males he stud-ied at G ombe Stream, Tanzania, live in stable, mutually exclusive commu-


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238 RICHARD & SCHULMANnities with little exchange of individuals between them. Agonistic behaviorwas quite frequent among community m embers, much of it occuring duringreunions between males that had been foraging apart. Bygott divided the15 adu lt males in his study into four categories according to the num ber ofindividuals to whom they were dom inant or subordinate: alpha male, an dhigh-, middle-, and low-ranking males. His evidence suggested that thesecategories correspond roughly with age differences. Highest rank wasachieved in middle age, but once the physical deterioration associated withold age set in, an individual's rank declined. Within this general patternthere was considerable variation in the age particular animals reached agiven rank class, probably because of individual differences in such factorsas health, ability to form coalitions, etc. Discussing the significance ofmale-male relationships, Bygott argued that competition for food was toorare for priority-of-access to be a significant advantage of high social rankand, furthermore, reproductive success as measured by copulation fre-quency showed no correlation w ith ran k (109).Rather, he postulated, thechimpanzee social system in its entirety provides the key to understandingmale relationships. The need to defend the community range against othercomm unities strongly favors males who attack strangers, especially males,on sight. Although border patrols are som etimes cooperative efforts, malesdo not spend all their time together, so that reunions are frequent. Giventhe chimpanzee male's tendency to attack or flee from strangers, thesereunions are tense affairs for there is always the possibility of nonrecogni-tion. This m ay partly account for the frequency of agonistic interactions atreunions, in which postures, calls, and orientation emphasize individualcharacteristics. Individuals differ natu rally in strength and aggressiveness,and it may be in the interests of all to develop hierarchical relationshipswhich will minimize the risk of fighting. Subordinate an imals avoid beinghu rt in a fight, and dom inant animals avoid hurting animals who are likelyto be relatives.The idea that males may benefit equally from a relationship with oneanother has been pursued in a different context by Packer (120).He col-lected data on coalitions formed by pairs of adult male baboons (Papioanubis). Coalitions occurred when one individual successfully enlisted thesupport of a second individual against a third, the opponent. In 1100 hoursof observations, Packer saw 140 solicitations resulting in 97 coalitions. On20 occasions the opponent was consorting with an estrous female; in fact,males were more w illing to join a coalition under tho se circumstances. Sixout of these 20 coalitions resulted in th e opponen t losing his consort to theenlisting male while the solicited male continued to fight the opponent.There was a strong correlation between the frequency with which adultmales joined coalitions and the frequency with which they successfullyenlisted coalition partners, a nd some suggestion tha t preferences for partic-


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PRIMATE FIELD STUDIES 239ular partners may have been partly based on reciprocation. Although thegenealogical relationships of the males included in the study were notknown, circumstantial evidence suggested that they were unlikely to beclose relatives, and that the data fulfilled the criteria fo r reciprocal altruismas specified by Trivers (150).Paren t-O fspring RelationshipsLactation sharply constrains the alternative reproductive strategies avail-able to mammalian females. A female cannot desert her milk-dependentoffspring and leave them in the care of her mate. Female investment inindividual offspring is thus high. Most primates produce only a singlealtricial young at birth who is dependent on its mother for nutrition andprotection. During long-distance movements, primate infants are carried.Materna l dependency in many species develops into a lifelong associationof maternally related female kin, In studies of macaque social groups ofknown matrilineal relatedness, social groups were found to have a spatialsubstructure of clusters of maternal kin groups (92, 136, 156).Adult males may either remain with their mate and help rear theiroffspring, or they may desert and attempt to mate with other females,investing less in individual offspring. This latter strategy, termed the "duck"strategy by M aynard Sm ith (104), is that of most male primates. Althoughpolygynous males do not contribu te directly to the rearing of offspring, theymay contrib ute indirectly in several ways. Conceivably, the alarm calls ofadult males serve to protect offspring from p redato rs. However, Cheney &Seyfarth (30) found puzzling evidence tha t vervet monkeys ala rm call pri-marily for predators to which their own age/sex class is most susceptible.More likely, indirect male investment arises from contributions to the de-fense of core areas or territories.In monogamous primates, the ratio of neonate weight to m aternal weightis high (93), and it may be tha t m ale investment in th e rearing of offspringis required for offspring survival. In the majority of monogamous primates,males help by carrying offspring. There is even some evidence of Callitrichidmales providing or sharing food as in many monogamous birds (17).In several colobines (24, 75, 77, 78, 115, 130, 164) and in chimpanzees(18, 60, 11 9 , males occasionally kill infants. In a general review of infanti-cide, Hrdy (78) describes four adaptive explanations of the phenomenonand one nonadaptive explanation. Adaptive explanations include exploita-tion of the infant as a resource. This may take the form of using the infantsas a food resource, or infant deaths may occur incidentally when infants a reexploited to buffer aggression (40; see 143) or are "aunted to death" (76).Infanticide may also result as a consequence of adults seeking to reducelocal resource competition. A third selective advantage of infanticide maybe that parents kill infants to concentrate investment in existing older


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240 RICHARD & SCHULMANoffspring, or to conserve resources during ecologically depressed periods.Afourth functional interpretation is tha t infanticide is a consequence of sexualselection, e.g. males kill offspring sired by their rivals. A nonfunctionalexplanation is that infanticide is simply nonadaptive social "pathology."Each of these explanations would be expected to be appropriate underdifferent environmental conditions and would entail somewhat differentdynamics. Fo r th e colobine primate examples, the sexual selection hypothe-sis seems to be the most plausible and parsimonious explanation of infanti-cide; however, it occurs so infrequently that it would be premature todismiss alternative hypotheses. In the Presbytus entellus examples of infan-ticide which have received the most attention (75, 77, 79, 146), the eventssurrounding infanticide are consonant with what we would expect if compe-tition among males for mates was intense. Supporting evidence for thesexual selection hypothesis is tha t 1. infants are killed only by adult males;2. the infants tha t a re killed are unlikely to have been offspring of the m alecommitting the act; 3, infanticide occurs during harem takeovers by rivalmales; 4, infanticide accelerates a female's return to estrus, and conse-quently, females begin producing offspring sired by the new male sooner;and 5. male takeovers tend to increase with density, hence males will havea shorter expectation of reproductive tenure and thus acceleration of returnto estrus would be desirable.Th e Evolution of Social SystemsWhy are stable patterns of interaction maintained among the members ofa social group? This is the question which m ost of th e studies reviewed sofar have tried, in various ways, to answer. A different, more synthetic setof studies has broached a larger question to which we now turn : what is theevolutionary explanation for the diversity of extan t primate social systems?Traditionally, these studies were less concerned with the mode of selec-tion tha n with identifying the selective agents. Thus, although they focusedupon evolution, their em phasis was not sociobiological as we have beenusing that term. With the emergence of sociobiology, interest broadened toinclude the mechanisms whereby particular social systems arise.Before embarking upon a survey of this literature, a point of clarificationis needed. This review does not contain a section on male-female relation-ships, an d the omission is no t a n oversight. The study of these relationshipshas usually been integral to research on the evolution of mating systems [butsee (144)], and it is difficult to consider the evolution of a mating systemseparately from the evolution of the social system in its entirety. In thissection, therefore, we include studies of male-female relationships in thecontext of the mating system and, more generally, the social system.The first modern attempt to explain the evolution of primate socialsystems invoked sex as a fundamental bond causing primates to cohere in


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PRIMATE FIELD STUDIES 241permanent social groups (170). Zuckerman 's (170) proposition was quicklyshot down (21) and replaced by a growing conviction that primate socialsystems are to be understood as adaptations to the environmental condi-tions under which particular species live (e.g. 22, 42, 66, 80). The associa-tion of a particular form of social organization with a particularenvironment is the result of long-term pressures exerted by that environ-ment which favor a form of social life adapted to that particular set ofconditions. The selective regime under which these adaptive systemsevolved was rarely made clear, and the emphasis was upon extrinsic, ecolog-ical agents of selection with little a ttention paid to the possible relevanceof male and female reproductive strategies.Th e first general exposition of traditional socioecology was by Crook &Gartlan (36). Their work inspired great interest and many papers whichimplied or pointed o ut some of its empirical and theoretical weaknesses andtried to correc t them (1, 6, 31-34, 41, 50, 55, 74, 82, 113, 125). [For adetailed review of this work, see (126)l. Clutton-Brock & Harvey's (33)paper illustrates the contemporary version of this research tradition. In-stead of making a broad, qualitative classification as Crook and G artla n ha ddone, they sought statistically significant correlations between pairs from awhole spectrum of behavioral and ecological variables to which numericalvalues could be assigned. They concluded that while their results providedsome support for the idea that general types of social organization can beusefully assigned to broad ecological categories, the functional significanceof different forms of social organization is better studied by looking at thedistribution of single variables rather than at whole sets of variables asCrook and Gartlan had done.Attention was drawn by G oss-Custard et a1 (61) to the possible impor-tance of reproductive strategies in shaping social systems. They suggested,for example, tha t the permanent presence of a single adult male in a socialgroup may not enhance adult survival or the success with which young areraised, but rather may result from male-male competition for access tofemales.Th e interaction between ecological pressures and m ale and female repro-ductive strategies has been explored more intensively since then (16, 35, 51,119, 166). Wittenberger (162) has a developed a formal model along theselines. The logic of the model is as follows. Since parental investment inindividual offspring is typically high in mamm als, an d is usually greater infemales than in males, it is to be expected that natura l selection will favoran optimal distribution of females with respect to crucial environmentalresources. In other words, female distribution and, more specifically, groupsize are ecologically determined. The distribution of males, in contrast,depends on their ability to defend female groups against competing males.In short, the selection pressures promoting gregariousness are different for


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242 RICHARD & SCHULMANmales and females. A corollary of the m odel is tha t male and fem ale patternsof dispersal differ. This is indeed true for m any mam mals as well as for birds(63).Wrangham (166) has elaborated these ideas with reference to primates.Most primates follow the typical mam malian pattern of philopatric femaleswho spend their lives in their natal group and males who migrate at or justbefore reaching sexual maturity. As noted earlier, this means that a maledoes no t have many kin around him after dispersal unless he joins a groupalready containing male kin. A female, in contrast, tends to be surroundedby kin, and Wrangham argues tha t kin selection among females can thu soperate under app ropriate conditions, favoring those who form tightly kn itcooperative social networks with close kin. What conditions are appropri-ate? Wrangham suggests tha t a key factor prom oting large, stable aggrega-tions of fem ale primates is the benefit they derive from defending jointlyexploited resources distributed in large, scattered patches. If resources a redistributed in small packages tha t w ill support only a few females, smallerand more strictly territorial social groups a re formed. In this case, femalesexclude more than a single male from the te rritory, giving rise to a single-male harem form of social organization rather tha n to the m ultimale socialgroup associated with larger aggregations.What empirical evidence is there to support this argument? In mostprimate species there are philopatric females who live, as predicted, inhighly developed cooperative networks; but consider those polygynous spe-cies in which females do leave their natal group: Gorilla gorilla (71),Pantroglodytes (1 18, 165), Colobus badius (98, 141), an d Papio ham adryas (90).In keeping with the model's predictions, in the two species with multimalesocial groups (Pan and Colobus), social networks seem to be more devel-oped among m ales. In both, for example, grooming is more common amongmales than among females (58, 59, 141).Although the evolution of polygynous mating systems and, more gener-ally, the social organization of the terrestrial old w orld monkeys and Afri-can apes has received the most atten tion, the evolution of monogamy amongnonhuman primates is generating more interest as the num ber of monoga-mous species becomes appa rent. Of approximately 85 extant species of oldworld monkeys, only two, both with extremely limited distributions, areknown to be m onogamous (Presbytispotenziani an d Nasalis concolor) (149,163), but when the Callitrichids, Cebids, and Hylobatids are taken intoaccount, the total number of monogam ous primate species rises to 22, andthere are probably more to be added to the list (148).Th e type of monogam y tha t occurs in primates has been termed ob ligate,meaning that these species are monogamous throughout their range regard-less of local conditions. Facultatively monogam ous species, in c ontrast, tend


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PRIMATE FIELD STUDIES 243toward polygyny at higher densities (87). However, at least for the Callitri-chids, the largest family of monogamous primates, a third category may beneeded since recent research suggests tha t m embers of this family may tendtoward polyandry under certain ecological conditions (J. Terborgh, per-sonal communication).No cogent explanation for the evolution of monogamy is yet available.Clutton-Brock & Harvey (32, 33) discuss several possible explanations butadm it themselves unable to find one t ha t is com pletely satisfactory. Proba-bly several of the selective pressures they discuss are important, with differ-ent pressures operating simultaneously or for different species. Theinvariable association among primates of monogamy with territoriality mayrepresent a clue, but its meaning is still not understood. Since theoreticalconsiderations suggest that territoriality is most likely to occur when re-sources are distributed in small, renewable pockets, we might expect thedistribution of monogamy in primates to have a pronounced ecologicalcorrelate. Unfortunately, there are not enough da ta for a broad assessmentof this proposition. However, in a comparative study of five sympatricprimates in Peru , where the distribution and phenology of resources weremonitored in some detail, the two territorial and monogamous species inthe community, Sanguinus uscicollis and S. mperator, differed from othe rspecies in that they did indeed exploit resources with a distribution closelyapproximating that predicted on theoretical grounds (148).DISCUSSIONMany problems are evident in the applications of sociobiological models toprimate data reviewed here, problems which several of the authors them-selves discuss. We shall consider briefly eight of them, some with obvioussolutions, others to which the solution is less clear. In several instances, thedifficulty is not unique to studies of prim ate sociobiology or even to sociobi-ological studies in general, but rather is common to the broad spectrum ofresearch in evolutionary biology. This point tends to be overlooked, webelieve, by some of the more vehement critics of sociobiology. The eightissues we shall discuss are as follows: 1. the lack of long-term data on thedemography and social behavior of large samples of individually knownanimals; 2. the lack of long-term, fine-grained data on the distribution ofresources in time and space; 3. the absence of information on relatednessthrough the paternal line; 4. the difficulty of assigning costs and benefits toparticular behaviors; 5 , the degree of perceptual resolution needed by ani-mals to m ake the fine discriminations apparen tly required by many of themodels; 6 . the equilibria1 assumptions made by most models; 7. our almost


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244 RICHARD & SCHULMANtotal ignorance of the genetics of nonhum an prim ate social behavior; 8. theuntestable nature, even under the best of circumstances, of many sociobio-logical models.1. Th e lack of long-term data on primate life histories and social behavioris an obvious problem to which a t least in principle there is a ready solution.Fo r the time being, however, it means tha t it is rarely possible even to beginto evaluate the appropriateness of a pa rticular model. C ertainly, not one ofthe studies reviewed here presents values for all the social and demographicparameters needed to test fully the explanatory hypotheses put forward.Hrdy & Hrdy (79), for example, propose a model in which social rankdecreases with increasing age, but they lack firm evidence of the ages of thelangur subjects fo r which the model was formulated. E xplanations of male-male an d female-female relationships usually assume that high social rankenhances reproductive success, but, as already noted, the few studies whichhave attempted to evaluate the assumption have produced conflicting re-sults and suggest that, in any case, correlations between reproductive per-formance an d rank over a year or two may have little bearing upon variancein reproductive success over a lifetime. Curtin & Dolhinow (38) have high-lighted the inadequacy of available data for testing the assumptions ofadaptive models of langur infanticide. More generally, Sade (133) has ar-gued th at the construction of fitness indices for primates may quite simplybe impossible.The data sets from Cayo Santiago and Japan come closest to adequacyin this regard and are thus uniquely valuable, but the generality of conclu-sions drawn about these provisioned populations must remain an openquestion at least until com parative da ta are available for wild populations.As a footnote here, we would add th at the failure of Chapais & Schulman's(23) model to incorporate estimates of the variance in reproductive valuewithin a given age cohort of rhesus females on Cayo represents a shortcom -ing of the model itself and not of the Cayo data-set: that information isavailable.In short, we know enough to be su re that primates, like other long-livedsocial species such as elephants (168), have complex and highly variable lifehistories which may be shaped by social factors (43) as well as by individualdifferences in physiology and environmental cons traints. We do n ot knowenough, in most cases, to estimate with confidence the actual values of manyof the parameters fundamental to almost all sociobiological models. Acorollary of this, pointed out by Hausfater among others, is that as moredata accumulate it is likely that many of the simplifying assumptions ofcurrent models will be shown to be inapplicable to long-lived social speciessuch as primates (see also 168).


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PRIMATE FIELD STUDIES 2452. The lack of long-term, fine-grained data on the distribution of re-

sources in time and space becomes a major handicap in form ulating modelssuch as Wrangham's (166), which com bines both ecological parameters an dindividual reproductive strategies into a g rand explanation of the evolutionof whole social systems. There is, for example, a de arth of rigorous ecologi-cal data documenting the distinction between resources distributed in"large, scattered patches" and those distributed in "small, evenly spacedpockets."3. Firm , observationally based evidence of paternity among wild pri-mates is extremely difficult to collect, and in species dispersed in socialgroups containing more tha n one adult m ale or in which there is frequentmovement of males among groups, tests of biological paternity are th e soleconvincing form of evidence. I t is not surprising, therefore, tha t there is nostrong evidence concerning relatedness through the paternal line for anyprimate population in the wild, and the absence of this information repre-sents one of the major gaps in th e Cayo and Japanese data sets. Failure totake paternal relatedness into account may have far-reaching implications.Altman n (3) has pointed ou t that given typical demographic trends and th edynamics of adult male dominance hierarchies in primates which formmultimale social groups, age coho rts may actually be as closely related asmaternal siblings. If this is so, models based on relatedness only throughthe m aterna l line, like those of Kurland , Chapais, an d Schulm an, will needto be reexamined. As it is, these models in their current form fit the dataalmost too well, suggesting that paternal relatedness may parallel closelyma ternal relatedness, or that the effects of paternal relatedness are somehowswamped by a mother's manipulation of her offspring, or possibly that themodels themselves are tautologous.4. With the possible exception of fitness indices, gaps in the data basediscussed in 1,2, and 3 can be filled, given enough time, money, a nd energy.The assignment of costs and benefits to particu lar behaviors is more prob-lematic, and continues to bedevil all areas of sociobiology (105). While itis reasonable to assume that there is a cost to aggression and a benefit togrooming, attaching precise values to discrete acts in order to generatecost-benefit ratios is difficult if no t impossible. Jones's (8 1) model illustratesthe difficulty, hinging as it does upon equality in th e costs and differencesin the benefits of aggression to young imm igrants and old gro up members.Specifically, the model assumes that the young benefit more from aggres-siveness tha n d o the old. I n the absence of real m easures, however, it couldequally well be assumed that the potential cost of aggression to younganimals with high reproductive value is much higher than to old animalswhose reproductive value is low (cf 79). In short, there seems to be a certain


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246 RICHARD & SCHULMANpost hoc quality to the assignment of values. Yet it is difficult to see how,in practice, a set of more or less aggressive acts could be analytically isolatedfrom the rest of an individual's biology and behavior, and related to itslifetime reproductive success. In other words, attem pts to go beyond intui-tion run rapidly into problems with confounding variables.5. Th e fifth issue concerns the importance to sociobiological research ofcareful studies of proximate behavioral mechanisms. Biomedical research-ers have traditionally dismissed field research for its lack of control andinevitable biases, and have paid little attention to hypotheses about theevolution of behavior. Conversely, field researchers have often ignoredthe findings of laboratory workers because the lab situation seemed toofar removed from the real world. Today, however, it is increasingly ap-parent that while the study of proximate mechanisms of behavior cannotprove or disprove an evolutionary hypothesis, an understanding ofthe degree to which animals are capable of making fine discriminationscan help in both the formulation and evaluation of sociobiologicalmodels.Models explaining the evolution of behavioral traits by kin selectionprovide a good example of the feedback which is beginning to occur. Thesemodels differ widely in their assumptions about the ability of altruists torecognize degrees of relatedness of kin (15), the reproductive value of kin(27), and whether kin are carriers of the trait in question (25). Some modelswork even without recognition of kin, so long as it is assumed that thepopulation is viscous-and tha t potential altruis ts follow a set of simple rulessuch as discriminating neighbors from strangers (135). Still, the effect ofbuilding into such models greater refinement of phenotypic recognitionusually has the effect of accelerating the spread of a kin-selected trait.Indeed, in some models an altru ist allele which is initially rare will actuallybe extinguished in a population if altruism is dispensed according to averagedegree of relatedness rather than relatedness at the locus in question (25).What is important in all these models is that the assumptions concerningphenotypic recognition abilities are stated explicitly and are amenable totesting.What evidence is there for th e ability of animals to make fine discrimina-tions of this kind? Recent work on two species of amphibian suggests thatthey have the ability to recognize siblings, and also tha t this ability has astrong underlying genetic component (13, 155). Bateson's (9-1 1) studies ofJapanese quail have revealed a finely tuned phenotypic recognition systemin these birds. Among primates, field evidence has long suggested thatindividuals respond differently to m aternal kin relations, but since materna lkin are usually close neighbors, it is difficult without experimental manipu-


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PRIMATE FIELD STUDIES 247lation to e liminate the possibility that animals respond differently to famil-iar individuals rather than to kin as such. Ironically, recognition of paternalkin, about which little or nothing is known in the wild, has been betterstudied in the laboratory. It has been shown that recognition of paternalrelatedness is not only possible (167) but indeed exerts an important influ-ence on social behavior (140).6. In the absence of demographic data and in keeping with the preceptsof r and k theory, there has been a tendency to assume that primatepopulations maintain themselves at o r close to equilibrium. Both empiricalevidence and models simulating populations processes increasingly suggestthat this assumption is incorrect (8, 45, 47, 126). The Altmanns (8) havestressed the profound effects upon an individual's social environment whicheven random demographic fluctuations may have, and they note the impli-cations of this variation for the selective regime to which an individual isexposed. Chapman & Hausfater (24) used a simulation model to investigatethe length of male tenure in a g roup w hich would favor infanticidal males.For the most part, however, sociobiological models tend to assume staticequilibrium and to ignore the possibility that different modes of selectionmay operate serially on the same behaviors under different demographicconditions. This is an area of research in which there is an urgent need forempirical evidence and also for further theoretical exploration of the effectsof change in demographic parameters.7. A m ajor weakness underlying all research on primate sociobiology isthe virtual absence of work on the genetics of nonhuman primate socialbehavior. The long generation time and behavioral complexity of mostprimates pose real problems for experimental approaches to behavioralgenetics, and current understanding of Mendelian inheritance of particularbehavioral traits is more advanced for humans than for nonhuman primatesbecause of the obvious medical and health-related applications of suchresearch (1 10, 11 1). Even if we agree th at some genetic basis exists for thecomplex social behaviors incorporated into sociobiological models, both themode of inheritance of this substrate and the constraints it imposes areunknown. It is unlikely th at these behaviors are controlled by a single geneor indeed that they are simple products of a set of genes, yet single locusmodels still prevail in theoretical approaches to the issue (e.g. 15). Exten-sion to a multilocus model is straightforward only if it is assumed thateffects are essentially additive across loci and are in o r near linkage equilib-rium (26, 37).

While there is little or no firm evidence on the genetic substrate ofnonhum an primate behavior, data collected on baboons living in the AwashValley of Ethiopia suggest, at the very least, that the issue merits explora-


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248 RICHARD & SCHULMANtion (53, 116, 117, 145). Along the Awash, the geographical ranges of oliveand hamadryas baboons (Papio anubis and I? hamadryas) overlap forminga hybrid zone, and the biology and behavior of the hybrids have beensubjected to detailed study. Members of hybrid social groups show a pro-nounced tendency to form harems, a characteristic of hamadryas socialorganization, but most of the harems are smaller and/or less stable incomposition than those typical of hamadryas. These differences seem to bedue to the females, who "disobey" their harem leaders more often thanhamadryas females. Kummer et a1 (91) have shown that females of bothspecies rapidly modify their behavior in response to different males; femalehamadryas soon stop following a particular male when in the companyof olive males who do not herd them, and, conversely, anubis femalesquickly learn to follow one male when released into a hamadryasband. It thus appears to be the hybrid males' behavior which facilitatesthe disobedience of females (1 17), and there is in fact some evidencethat they are less effective herders than their hamadryas counter-parts. Olive baboons living in a range of habitats at the species bordershow several behavioral adaptations to local conditions, but the gen-eral features of their social system remain the same. In contrast, thesocial system of five hybrid groups living in similar habitat differed inaccordance with their genetic makeup, as indicated by their externalappearance.Taken together, these observations provide some support for the proposi-tion that differences between the social systems of olive and hamadryasbaboons are determined largely by the genetic substrate controlling thebehavior of males of the two species. However, conclusions about theimmediate ancestry of males made according to their external appearancehave yet to be confirmed by serological analysis. I t is still not possible, then ,to reject the hypothesis that an appropriate social environment may promptsome individuals to fix their interest persistently on others and that thesocial possessiveness of hamadryas males and , to a lesser extent, of hybridmales, may be a learned behavior.8. The last issue concerns the general way in which models are used inprimate research. Like many hypotheses in evolutionary biology, several ofthose discussed earlier are not amenable to test as hypotheses in the physicalsciences can be tested. Rather, models must be evaluated and judged moreor less plausible on a variety of grounds. With this procedure we have noquarrel, although th e kinds of evidence brought to bear in these evaluationsin many cases needs expanding; for example, exceptions to the rule deservecloser attention, as do the proximate behavioral mechanisms which permitthe system to function in the way the model proposes. Rather, our concern


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PRIMATE FIELD STUDIES 249is with the failure of most researchers to consider alternative explanationsfor the phenomenon in hand. This represents more than just a nicety ofscientific procedure. Alternative, mutually exclusive explanations may fitthe sam e data set (e.g. 4), with further research needed to eliminate one ofthe two. Of more theoretical importance, alternative but not mutuallyexclusive explanations may fit the same data set because more than onemode of selection is operating simultaneously in a particular context (15,161). In this review we have followed current practice in treating the modelsrepresenting the cornerstones of sociobiology as though they were mutuallyexclusive. In so doing, we are almost certainly underestimating the com-plexity of the selective regime to which primates are exposed and barringourselves from more profound theoretical insights in to the way in whichsocial behaviors evolve.Having enumerated so many problems, what, in conclusion, can we sayhas been the contribution of sociobiology to primate field studies? Has itcontributed at all? We believe the answer is an em phatic "yes." First,sociobiology has filled a theoretical vacuum in primate field studies. Thecorrectness of the many hypotheses subsumed under its rubric is less impor-tant than the fact that we now have something to argue about. From theearly days of sociobiology when polemic shed more heat than light, we havereached a poin t where a concensus is emerging about the problems besettingmodels of behavioral evolution. It is important to realize not only that theseproblems have been identified but also that they now represent intellec tualchallenges, pointers toward directions in which at least some primate re-search could fruitfully move. Second, we believe that, the problems not-withstanding, sociobiological theory has already shed fresh light on tra-ditional areas of interest as well as inspired research in entirely newareas. In particular, the importance of genetic relatedness as an organiz-ing principle of primate societies, long recognized by the Japanese (e.g.85), only became a central concern of Western field researchers after thedevelopment of kin selection theory. In short, whatever its failings, so-ciobiology deserves full c red it' for eradicating the list-making approach(6) in primate field studies and for that alone we should be profoundlythankful.

We are grateful to the following people for their com ments and suggestionsabout m any of the ideas in this article: Sarah Blaffer Hrdy, Robert Dew ar,Glenn H ausfater, Daniel Rubenstein, and John Terborgh.


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