YEARBOOK OF PHYSICAL ANTHROPOLOGY 37:233-271 (1994)
Myth of the Typical Primate
KAREN B. STRIER
Department of Anthropology, University of Wisconsin-Madison,
Madison, Wisconsin 53706
KEY WORDS Cercopithecines,“Typical” primates, Kinship, Dispersal, Aggression, Dominance, Sex, Reproduction
ABSTRACT
Anthropological interest in nonhuman primates as models
for human behavioral evolution has tended to focus on a relatively small
number of species. This emphasis, coupled with a search for unifying principles that explain behavior, has led to a widespread perception of the semiterrestrial cercopithecines as “typical,” and therefore characteristic of most
other primates. The prevalence of male-biased dispersal and female philopatry, the use of aggression to establish and maintain hierarchical relationships, and the occurrence of sex for exclusively reproductive purposes have
been challenged repeatedly, but the cercopithecine model of primate behavior has nonetheless persisted in much of the anthropological literature. This
review incorporates accumulating data on a diversity of primates to examine the myth of the typical primate. The roles of kinship, aggression, and
sex in mediating primate social relationships are far less uniform across
primates than the myth has implied, raising questions about the generality
of models of primate social systems derived from “typical” primates. Acknowledging existing diversity and encompassing it in more accurate portrayals of primate behavioral ecology requires consideration of the interacting effects of phylogenetic, demographic, ontogenetic, and physiological
variables. o 1994 Wiley-Liss, Inc.
In the last two decades, a growing number of anthropologists have begun to
follow nonhuman primates out of the Old World savannas and woodlands into what
remains of the world’s tropical forests. Data on species that were once considered
peripheral to questions about human behavioral evolution are now challenging
many long-standing perceptions of comparative primate behavioral ecology. Yet,
mainstream anthropology has been slow to incorporate behavioral findings from
these newly studied species into its models. The anthropocentric currents of primatology run deep, and appear to have been resistant to change.
Part of this resistance may be rooted in biases dating back to the first primate
field studies in the 1930s, when psychologist Robert Yerkes sent his students to
investigate the naturalistic behavior of nonhuman primates (Carpenter, 1934). By
the mid 1950s, Japanese primatologists, influenced in part by Carpenter’s work,
and in part by Kinji Imanishi’s belief that monkeys “resemble human beings more
than they resemble other animals” (Asquith, 1991:91), initiated field studies on
macaques (see Fedigan and Asquith, 1991). Soon afterward, American anthropologists began t o focus on other Old World semi-terrestrial monkeys in an effort t o
understand the social correlates of adaptations to life on the ground (Washburn
and DeVore, 1961; Dolhinow, 19721, and paleontologist Louis Leakey promoted
field studies on the great apes because of their phylogenetic relatedness to humans.
Unlike many anthropologists, primatologists from disciplines such as psychol0 1994 Wiley-Liss, Inc.
YEARBOOK OF PHYSICAL ANTHROPOLOGY
[Vol. 37, 1994
Descriptive,
Fig. 1. Waves of primate field studies.
ogy and zoology have never limited their research to particular species or geographic areas that were obvious candidates for inferences about human behavioral
evolution. For psychologists such as Carpenter, whose pioneering field study was
on arboreal, New World howler monkeys, and a number of zoologists, who subsequently developed long-term field studies on arboreal New World and Old World
monkeys alike, understanding primate adaptations has been more important than
a particular species’ phylogenetic position or ecological parallel with humans. But,
despite the broad interdisciplinary appeal of primates, anthropologists have
tended to treat primates as species apart from other animals (Richard, 1981). Only
recently, as disciplinary boundaries have blurred, have anthropologists begun to
focus on primates as subjects for addressing questions in comparative behavioral
ecology rather than as human or hominid analogs (Kinzey, 1986).
How accurate are contemporary depictions of primate behavior in the anthropological literature? How do these depictions reflect the shifting perspectives behind primate field studies? What are the consequences of expanding our views of
primate behavior by incorporating new data from diverse species into our models?
In cultural anthropology, recognition of such diversity has led to relativistic approaches that emphasize the uniqueness of different human societies (Boas, 1973).
How can anthropologists retain their search for unifying principles about primate
behavior while simultaneously acknowledging the diverse social systems in their
study subjects? These fundamental questions have strongly influenced anthropological perspectives of the typical primate, and will be considered in the final
section of this review. First, however, i t is appropriate to examine the myth of the
typical primate within the context of evolving research paradigms. Evidence for
much greater variability in primate societies than the myth implies is provided by
comparative data on primate social relationships, including kinship, aggression,
and sex, and by a brief evaluation of some ecological models of primate social
systems.
ORIGIN OF THE MYTH
Methods and standards, as well as the questions asked in primate field studies,
have changed over the years, reflecting a succession of distinct but overlapping
waves as disciplinary perspectives have converged (Fig. 1). The first of these
waves, from the late 1950s through the 1960s, was basically descriptive, adhering
to the anthropological tradition of ethnographic reports and to the zoological tradition of natural histories. These studies were rich in contextual details, but it was
difficult to compare descriptions from different studies because there were few
common denominators. Many observations from this period (e.g., the importance of
coalitions; the prominence of affiliative relationships) clearly anticipated later,
more quantitative findings, but their impact was limited by the lack of a uniform
methodology and comparative and theoretical framework.
In the 1960s and early 1970s, primatologists from all disciplinary backgrounds
began to employ systematic methods of behavioral sampling that could facilitate
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MYTH OF THE TYPICAL PRIMATE
235
quantitative comparisons both among primates and between primates and other
animals (e.g., Hinde, 1973; Altmann, 1974; Dunbar, 1976). The coincidental incorporation and application of evolutionary and ecological theories, including sociobiology and optimality models, further standardized the types of quantitative data
that were collected (Richard, 1981). Consequently, by the mid 1970s, the second
wave of primate field studies had become increasingly focused on specific questions
pertaining to the functional, or evolutionary, significance of behavior.
By the early 1980s, the availability of comparative data from enough different
species permitted the development of general explanatory models relating ecological variables, such a s food distribution and predation pressure, to social variables,
such a s group size and mating systems (e.g., Wrangham, 1980; van Schaik and van
Hooff, 1983; Terborgh and Janson, 1986). The antecedents of these models were
based on early correlations between ecological, morphological, and behavioral
traits in primates (e.g., Hall and DeVore, 1965; Crook and Gartlan, 1966; Eisenberg et al., 1972; Clutton-Brock and Harvey, 1977) and comparative behavioral
ecological analyses of bats (Bradbury and Verhencamp, 19771, birds (Emlen and
Oring, 1977), and mammals (Crook et al., 1976). Primatologists of the 1980s took
the predictions generated by these evolutionary ecological models into what became the third wave of field studies. Predictions could be tested through diachronic
analyses on a few well-studied species, such as macaques, baboons, and chimpanzees, and through synchronic analyses on species that had not been studied previously, or had been studied only cursorily and were included in the general models
incorrectly. At the same time, research on diverse species was facilitated by changing global politics that made many primate habitat countries, and the diverse
primates in them, more accessible to foreign researchers.
The results of third wave efforts to test synthetic models of primate behavioral
ecology have been mixed. Some ecological generalizations, such a s that predicting
a relationship between food patch size and feeding group size, have been supported
in various studies of Atelines and apes, which exhibit more flexible grouping
patterns than most other primates (e.g., Leighton and Leighton, 1982; Chapman,
1988; Symington, 1988a; White and Wrangham, 1988; Strier, 1989). Others, such
as that between body size and diet, have not fared so well against comparative data
from New World monkeys (Ford and Davis, 1992; Strier, 1992a) and lemurs (Richard and Dewar, 1991). A number of other behavioral generalizations, particularly those pertaining to dispersal and kinship, dominance relations and aggression, and sex and reproduction, were also challenged. Today, generalizations in
these fundamental areas of primate sociality are confounded by exceptions, meriting a closer look at the contradictory observations permeating the field.
The 1990s signal the beginning of a fourth wave of primate field studies. Methodologically, the fourth wave is already distinguished by the development of noninvasive tools including DNA analyses from hair follicles and buccal cells obtained
from discarded food wadges (Higuchi et al., 1988; Li et al., 1988; Takasaki and
Takenaka, 1991; Morin et al., 1993; Takenaka et al., 1993) and fecal steroid assays
(Wasser e t al., 1988; Strier and Ziegler, 1994). These methods not only permit a n
integration of what have become standardized methods of behavioral sampling
with new insights into genetic and physiological processes, but they have also
followed the lead of captive primate studies in extending the interdisciplinary
nature of field primatology beyond the behavioral sciences. Theoretically, contemporary studies have also begun to explore some of the inconsistencies that emerged
from third wave models by focusing on distinctions between intra- and intergroup
dynamics (e.g., van Schaik, 1989; Isbell, 1991; Cheney, 1992; van Hooff and van
Schaik, 1992; Strier, 1994), and on a revived interest in ontogenetic, demographic,
and phylogenetic variables (e.g., Altmann and Altmann, 1979; Dunbar, 1979;
Snowdon, 1990a; Fleagle, 1992; DiFiore and Rendall, 1993). It is not yet clear,
however, whether more comprehensive comparative models will be robust enough
to encompass these new perspectives and escape from established perceptions of
the “typical primate.”
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YEARBOOK OF PHYSICAL ANTHROPOLOGY
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The “typical” primate?
It is only natural that three of the longest and best-studied primate taxa, the
baboons, macaques, and chimpanzees, figure prominently in portrayals of primate
social behavior. But i t is also the case that underlying assumptions about the
relevance of these primates to human behavioral evolution have contributed to
their prominence in the anthropological literature. While such simplification may
be acceptable in a n introductory curriculum, it is disturbing to discover how frequently it is carried over into more technical articles and books that review existing knowledge. The fact that baboons, macaques, and chimpanzees differ in many
fundamental respects both from one another, and from within the genera, further
illustrates the arbitrary processes behind such conservative referential approaches
(Fedigan, 1982; Tooby and DeVore, 1987).
Savanna-dwelling baboons, like rhesus and Japanese macaques, live in multimale, multifemale polygamous troops. The troops are cohesive, and comprise related matrilines with male-biased dispersal. Males and females are highly dimorphic in both body and canine size; larger males equipped with more elaborate
weaponry are individually dominant over females. Dominance hierarchies are relatively stable among females because young females inherit the ranks of their
mothers. Among males, however, dominance relationships are routinely challenged and reigning alpha males are regularly overthrown by successors. Dominance hierarchies, and the aggressive interactions that reflect and lead to hierarchical relationships, together with affiliative interactions, such as grooming and
coalitions among kin, form the basis of baboon society. Relationships among related females are more stable than those among unrelated males, and savanna
baboons have come to represent the “typical,” female-bonded primates (Wrangham, 1980).
Chimpanzees superficially resemble savanna baboons in their multimale, multifemale polygamous societies and in the highly visible sexual swellings that signal female reproductive condition, but they are markedly different in nearly every
other respect. Chimpanzee parties are fluid, with heterosexual aggregations occurring only when large patches of preferred fruits are available. In contrast to
baboons, chimpanzee communities comprise related males with female-biased dispersal (Morin, 1993). The strongest associations, beyond those between mothers
and their offspring, exist among males. Males compete amongst themselves for
dominance status, but males also cooperate with one another in intercommunity
aggression. Females appear to have weak dominance relations, although the degree to which they associate with one another is highly variable between populations.
The pronounced differences between the multimale, multifemale polygamous
societies of savanna baboons and chimpanzees also demonstrate the limitations of
relying on superficial characteristics such a s group composition to generalize about
social dynamics. Indeed, these differences have been used to justify distinctions
between chimpanzees, as exceptional primates, and savanna baboons and other
well-studied, female-bonded cercopithecines, a s more “typical” primates. Yet, even
among the ecologically similar semiterrestrial cercopithecines, such as baboons,
vervet monkeys, patas monkeys, and macaque species, social relationships differ
markedly (e.g., Cheney and Seyfarth, 1983; Harding and Olson, 1986; Rowel1 and
Chism, 1986; de Waal and Luttrell, 1989). Similarly, there are significant differences in the societies of common chimpanzees and the closely related bonobos
(Furuichi, 1989; Ihobe, 1992). When data from a n even wider variety of species,
particularly the Malagasy lemurs and the New World monkeys, are considered, it
becomes apparent that many behavioral traits shared among the cercopithecines
are actually unique to them. The diversity of social systems now known to exist
across primates leaves the status of baboons and macaques as “typical” primates in
a highly dubious state.
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MYTH OF THE TYPICAL PRIMATE
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Deconstructing a myth
The myth of the cercopithecine model of a “typical primate” is based on a t least
three erroneous but persistent assumptions. First, male dispersal and female
philopatry continue to be described as the pattern that characterizes the primates
as well as other mammals (Greenwood, 1980; Pusey, 1987). Chimpanzees and
bonobos, along with a few other species (red colobus, hamadryas baboons, and
howler monkeys), have long been regarded as exceptions to this pattern, but the
number of exceptional cases has increased in recent years, challenging the assumptions that a “typical” primate dispersal pattern exists (see Moore, 1984,
1992).
Second, early emphasis on the use of aggressive competition to mediate primate
social relationships has prevailed despite repeated efforts to demonstrate the limitations of such arguments (Rowell, 1974; de Waal, 1989a,b; Silverberg and Gray,
1992). Is the absence of strong dominance hierarchies and overt aggressive interactions in many “atypical” primates due to the failure of observers to detect their
occurrence, or is it the case that these behavioral systems are less uniformly
prevalent across primates than among the cercopithecines? When other variables,
such a s the relationship between male-male competition and female mate choice
and distinctions between intra- and intergroup aggression and affiliation, are examined, the primacy of aggressive competition even among cercopithecines becomes less obvious. Simultaneously, greater attention has been paid to the importance of coalitions and reconciliations (de Waal, 1986, 1989a) and other more
subtle, nonaggressive forms of competition including sperm competition in male
chimpanzees (Harcourt et al., 19811, muriquis (Milton, 1985a; Strier, 1992b,c), and
savanna baboons and rhesus macaques (Bercovitch, 1992), and ovulatory inhibition (Wasser and Barash, 1983) in female talapoin monkeys (Bowman et al., 1978),
gelada baboons (Dunbar, 1980, 19841, and callitrichids (Abbott, 1989). When
viewed collectively, these alternatives suggest that a “typical primate” competitive strategy does not occur.
Finally, the link between sex and reproduction in nonhuman primates has endured despite the fact that it was effectively debated more than a decade ago (Hrdy,
1981). Clarification of the relationship between sex and reproduction has been
elusive because of the difficulties inherent in inferring reproductive success from
mating success (reviewed by Gray, 1985); it is a n important relationship to clarify,
nonetheless, because one of the purported benefits of sociality is the opportunity to
enhance reproductive success and inclusive fitness. Yet, if reproduction is only one
of the functions of sex in nonhuman as well a s human primates, then by extension
we must reconsider the suggestion that “social structures and mating systems are
not the same things” (Cords, 1987:107; see also Melnick et al., 1984; Richard,
1985a; and review in Moore, 1992). The prevalence of female matings with extragroup males in Barbary and Japanese macaques (Mehlman, 1986; Small, 1990;
Sprague, 1992) as well as several other primates (e.g., lemurs: Richard, 1985a;
Richard and Dewar, 1991; Sussman, 1992; patas monkeys: Harding and Olson,
1986; Rowell and Chism, 1986; forest guenons: Cords, 1987; muriquis: Strier et al.,
1993; Strier, 1994) may have profound consequences for the ways in which the
function of primate social systems have traditionally been modeled from ecological
and evolutionary principles.
Questions about the generality of female philopatry, aggression, and sex for
exclusively reproductive purposes were raised years ago and in some cases, repeatedly, in both empirical and theoretical publications. But, the strength of the “typical primate” model has overpowered the impact that many of these original challenges have had on the field (e.g., Glezer and Kinzey, 1993; Janson, 1993;
Snowdon, 1993). With more abundant data on newly studied species, on species
that have long been in the literature but are only now beginning to yield longitudinal data, and the ongoing accumulation of data from well-studied species, it is no
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YEARBOOK OF PHYSICAL ANTHROPOLOGY
[Vol. 37, 1994
longer possible to accept the myth of the “typical primate” uncritically, or to generalize from baboons and macaques, which are themselves highly variable (de
Waal and Luttrell, 19891, to most other primates.
SOCIAL RELATIONSHIPS
Dispersal and kinship
Theoretical obsessions
Kinship has occupied a central position in efforts to understand primate social
relations and social systems during the methodological and theoretical waves that
have swept primatology. Part of this tenacity may be attributed to the tradition in
social anthropology in which kinship, whether biologically or culturally defined,
has been viewed a s a ubiquitous organizing principle in human societies (Sade,
1991; Quiatt and Reynolds, 1993). With the adoption and application of evolutionary theory in primatology, the importance of biological kinship was further elevated. Kin selection and inclusive fitness theory were invoked to explain seemingly altruistic acts that ran contrary to what “selfish” individuals should be
selected to do (Hamilton, 1964). Consequently, knowledge of the genetic relatedness between individuals has become critical to interpretations of primate social
relations, In many cases, however, such knowledge remains largely inferential.
Evolutionary theory permits the formulation of predictions about how different
individuals should behave toward one another and about why interindividual relationships may vary. Because individuals share a greater proportion of their
genes with kin than with nonkin, selection pressures should favor beneficent behavior toward kin as long as the genetic benefits through inclusive fitness outweigh the costs to individual fitness. Armed with this theoretical model, primatologists could both describe and explain the occurrence of nepotistic behavior
among their study subjects.
Efforts to discriminate between beneficent and selfish behavior have produced
many detailed analyses of social relations that confirmed and advanced the theoretical predictions. For example, Kurland (1977) found that female Japanese
macaques spent more time in proximity, grooming, and in agonistic interactions
with kin than with nonkin, and that among kin, the degree of relatedness was
positively correlated with higher frequencies of interaction among close relatives.
Yet, while proximity and grooming were expected to be stronger among kin than
nonkin, agonistic interactions were expected to be less frequent. These incongruent results were reconciled with kin selection theory in a second level of analysis:
when the frequency of agonistic interactions was calculated relative to the frequency of proximity between dyads, aggression between kin was proportionately
less frequent than expected from the time they spent in proximity. Similarly,
Seyfarth and Cheney (1984) observed that vervet monkeys were more likely to
assist kin than nonkin, unless nonkin had recently groomed one another. These
findings were interpreted by combining the predictions of both kin selection and
reciprocal altruism, another powerful sociobiological principle (“rivers, 1971).
Such conclusions, and the analyses that predicated them, could not have been
reached prior to the adoption of systematic, quantitative methods of behavioral
observation. Similarly, biological relatedness among primates could not have been
determined without the accumulated data from long-term studies in which identified mothers could be associated with identified offspring. As successive offspring
matured, maternal relatedness among siblings and ultimately, adults, could be
calculated. However, kinship through the paternal lineage, particularly but not
exclusively in polygamous primates, continues to elude the most exacting observational regimes. Indeed, despite some claims that the increased focus on female
primates was introduced by feminist primatologists in the 1970s (Haraway, 1989),
the importance of female kin groups had already been recognized in the long-term
studies of the Arashiyama Japanese macaques (Fedigan and Asquith, 1991). It is
possible that these renewed emphases on female primates were a consequence of
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MYTH OF THE TYPICAL PRIMATE
239
the coincidental emergence of kin selection theory and its requisite documentation
of genetic relatedness, which could only be accurate for females.
Female-bonded primates: A cercopithecine phenomenon?
Accumulating knowledge of female kinship relations among the Old World cercopithecines permitted primatologists to understand some of the complexities of
these primates’ societies. Hierarchically ranked females in matrilines interact
with hierarchically ranked females in other matrilines; troops fission along matrilines; and members of matrilines ally themselves against other matrilines and
against unrelated males (Kawai, 1965; Samuels e t al., 1987; Cheney, 1992; reviewed in Quiatt and Reynolds, 1993). Thus, the influence of females in their own
groups, in intergroup dynamics, and in terms of male group membership and
mating success has been widely documented (Hrdy, 1981; Smuts, 1987). Furthermore, the primacy of the mother-daughter bond came to represent more than a
descriptive element of primate socialization practices because it was embedded in
a larger social and kinship network involving other mother-daughter bonds (Nicolson, 1991).
If one sex is philopatric, then, according to traditional views pertaining to inbreeding avoidance, the other sex presumably must disperse (Packer, l975,1979a,
1985; Greenwood, 1980). Knowledge of dispersal patterns was thus thought to
provide indirect insights into the kinship structure of a group. And, because determining kinship lineages remains impractical in short-term studies of slowmaturing species such a s primates, documenting sex-biased dispersal has become
a widely employed shortcut for inferring sex-biased philopatry and kinship within
groups. However, as Moore (1984, 1992) has repeatedly argued, coupling malebiased dispersal and female-biased kinship is misguided for two essential reasons.
First, although routine dispersal by both sexes is limited to a relatively small
number of primates, there are numerous reports of occasional dispersal by females
in primates with male-biased dispersal systems, and by males in primates with
female-biased dispersal. Even a low proportion of dispersal events can have profound implications for relatedness among group members because of the relatively
small size of most primate groups and because of the relatively long lifespan of
most primates (Chepko-Sade et al., 1987). Second, there is debate over whether
inbreeding avoidance is, in fact, the primary force for sex-biased dispersal systems
in primates (Moore, 1984; Moore and Ali, 1984; but see Pusey and Packer, 1987).
Without a thorough understanding of what constitutes negligible levels of sexbiased dispersal and why dispersal occurs at all, the behavioral significance of
philopatry remains obscure.
Inferences about nepotistic behavior based on the male-biased dispersal and
female philopatry found in many cercopithecine primates are further confounded
when accumulating data from a more diverse set of species are considered (Fig. 2).
Among the cercopithecoids, dispersal tends to be less biased toward males among
the colobines than among the cercopithecines (McKenna, 1979; Moore, 19841, and
even among congeneric cercopithecines, such as the macaques, there is extensive
variability in the degree of male-biased dispersal (Moore, 1984, 1992). When the
comparison is extended to include other anthropoids, it is evident that none of the
hominoids exhibit this pattern, and among the New World monkeys, only some
capuchin monkeys adhere to it.
Male-biased dispersal and female philopatry is not a “typical” primate pattern;
at most it is a pattern among the prosimians (Richard and Dewar, 1991; Kappeler
and Ganzhorn, 1993) and the cercopithecines. Yet, i t has persisted in being the
“default expectation” (Moore, 1992:369) in primates, despite the fact that examples
in which females disperse and males remain in their natal groups are found across
all haplorhine families except cercopithecines. These include chimpanzees (Goodall,
1986; Nishida et al., 1990), red colobus (Struhsaker, 1975; Marsh, 19791, spider
monkeys (Symington, 1988b), woolly monkeys (Nishimura, 1990), muriquis
(Strier, 1991a), and Costa Rican (but not Peruvian) squirrel monkeys (Boinski,
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[Vol. 37, 1994
Dispersal Patterns in Anthropoid Primates
6
Male-biased
Both
5
Female-biased
2
al
4
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0
3
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a,
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Cercopithecines
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Papio
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Colobus
Nasalis
Presbytis
Pygathrix
Pan
Gorilla
Pongo
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New World Monkeys
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Fig. 2. Dispersal patterns in anthropoid primates. Sources from Moore (1984, 19921, Pusey and Packer
(19871, and Strier (1990).
1987; Mitchell e t al., 1991). These examples do not refute the claim that kinship
can be a powerful organizing principle of social relations in some primates. Rather,
they imply that in a number of primates, kin-biased behavior may be evident
among males rather than females.
More compelling, however, is the growing number of examples in which both
sexes disperse from their natal groups. These include members from all haplorhine
taxa representing a diverse array of social systems, such as, but not limited to,
gibbons (Leighton, 19871, mountain gorillas (Harcourt, 1978; Stewart and Harcourt, 1987), hamadryas baboons (Abegglen, 1984; Phillips-Conroy et al., 1992),
proboscis monkeys (Bennett and Sebastian, 19881, howler monkeys (Glander,
1980, 1992; Crockett and Eisenberg, 1987; Crockett and Pope, 19931, and marmosets and tamarins (Sussman and Garber, 1987). Even when comparisons are restricted to just the polygynous or polygamous genera, fully 50% exhibit dispersal
by both sexes (Fig. 2). This widespread phenomenon severely challenges the assumption that kinship is a n ubiquitous organizing principle in all primate societies.
Implications for understanding primate societies
Why is there such variation in dispersal patterns across haplorhine primates,
and what are the implications for interpretations of social behavior when dispersal
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YEARBOOK OF PHYSICAL ANTHROPOLOGY
240
MYTH OF THE TYPICAL PRIMATE
241
by both sexes might preclude the occurrence of strong kinship among members of
some primate groups? Efforts to decipher why any primate disperses from its natal
group remain highly speculative due to difficulties in distinguishing between alternative mechanisms such a s inbreeding avoidance, expulsion due to resource
competition by same-sexed group members, avoidance of resource competition with
kin, and the search for greater reproductive opportunities elsewhere (Greenwood,
1980; Moore, 1984; Moore and Ali, 1984; Packer, 1985; Pusey and Packer, 1987).
The preponderance of similar dispersal patterns within taxonomic groups, such as
male-biased dispersal in the prosimians and cercopithecines, female-biased dispersal in the New World atelins, and dispersal by both sexes in most apes and other
ceboids, has led to the proposition that dispersal systems may have phylogenetic,
as well as ecological or reproductive, components that correspond to primate evolutionary histories (Strier, 1990; Kappeler and Ganzhorn, 1993).
In the absence of obvious and robust explanations for why sex-biased dispersal
occurs in some primates, it may be useful to rephrase the question from why a
primate might disperse to why primates might benefit by staying with their kin.
Ecological models have suggested that female philopatry should only occur when
food resources are distributed in such a way that females benefit by having related
allies available to cooperate in defending food from other groups of related females
(Wrangham, 1980; van Schaik, 1989) or in avoiding predators (van Schaik and van
Hooff, 1983). According to these models, females should disperse only when the
costs of competing with female kin for food or reproductive opportunities outweigh
the benefits derived from cooperative resource or predator defense (Wrangham,
1982).
Social models have also postulated that female philopatry should be favored
when females require reliable allies to protect themselves from aggression from
larger, more individually dominant males (Dunbar, 1984; Smuts, 1987; Strier,
1990; Smuts and Smuts, 19931, just as male philopatry is thought to facilitate
cooperation among male chimpanzees and spider monkeys in defending community females from other groups of related males (Goodall, 1986; Symington, 1990).
Comparative models developed in birds (Emlen and Vehrencamp, 1983) and bats
(Bradbury and Verhencamp, 1977) support the hypothesis that the occurrence and
patterning of sex-biased dispersal and philopatry in nonhuman primates is a n
outcome of the compromise between intra- versus intergroup competition, whether
it is for food resources or protection in the case of females or for female resources
in the case of males (Wrangham, 1980,1982; Moore, 1984; van Schaik, 1989; Isbell,
1991; Cheney, 1992; van Hooff and van Schaik, 1992).
The evidence for greater diversity in patterns of dispersal and philopatry across
the primates has not diminished interest in the importance of kinship. Rather, i t
has led to increasing efforts to understand the determinants and behavioral and
genetic consequences of sex-biased philopatry when i t occurs. From the perspective
of population genetics, sex-biased dispersal should lead to greater homogeneity
within the philopatric sex than within the dispersing sex, and groups in which one
sex is philopatric should be more genetically homogeneous than groups in which
both sexes disperse (Gouzoules, 1984; Chepko-Sade, et al., 1987). Until recently,
however, there has been little concern for the fate of emigrants (but see Glander,
1992; Crockett and Pope, 1993), in part because many long-term field studies have
focused on single study groups instead of local populations. Indeed, the tendency to
assume that disappearances from a study group represented dispersal, without
confirmation that missing individuals had, in fact, immigrated into other groups,
has had a significant impact on how quantitative and anecdotal dispersal data
have been interpreted (Moore, 1984).
In the few studies in which local populations, rather than single study groups,
have been monitored, a number of confounding findings have begun to emerge.
First, many individuals which leave their natal groups, whether male or female,
experience a long delay before they succeed in immigrating into other groups. In
marked Costa Rican mantled howler monkeys, where 79% of males and 96% of
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YEARBOOK O F PHYSICAL ANTHROPOLOGY
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females dispersed from their natal groups, males maintained solitary lives for up
to 4 years and females for up to 1year (Glander, 1992). In Venezuelan red howler
monkeys, extratroop individuals accounted for 6-9% of approximately 500 censused animals (Crockett and Pope, 1993).
Second, if dispersing individuals leave their natal groups together, and subsequently join the same group, or establish their own group, then the average relatedness in the new groups may be comparable to or greater than the relatedness in
groups comprising philopatric individuals (Moore, 1992). Male vervet monkeys
often transfer to the same groups as those that males from their natal groups have
previously joined, presumably for allies (Cheney and Seyfarth, 1983). Male ringtailed lemurs generally disperse in cohorts, possibly for protection against predators, but may respond to unfavorable sex ratios in their new groups by subsequent
emigrations (Sussman, 1992). Related red howler monkey males that emigrate
together achieve longer tenures than unrelated males in multimale troops, although mating opportunities may differ depending on their relative ages (Crockett
and Pope, 1993).
Finally, the absence of genetic paternity data from most field studies means that
estimates of relatedness are limited to matrilines. Genetic relatedness within
groups and within populations will be higher if some males father a disproportionate number of offspring (e.g., Pope, 19901, if dispersal is strongly sex-biased and
males tend to migrate to the natal groups of their fathers (Kuester et al., 1992), or
if stochastic demographic processes result in skewed infant sex ratios that ultimately affect dispersal patterns and adult sex ratios of groups (Dunbar, 1979,
1984).
Variation in the degree of relatedness within primate groups necessitates a
reevaluation of the consequences of kinship for predicting social relations. While
kinship may facilitate cooperation between individuals, it is not a necessary condition for the formation of cooperative alliances (Kummer, 1978; Wrangham,
1982). Even among “typical” cercopithecine primates, long-term coalitions have
been observed between unrelated individuals that benefit from cooperation either
immediately due to mutualism, or over the long-term due to reciprocity (e.g.,
Packer, 197913; Smuts and Watanabe, 1990). It is likely that familiarity and reliability are the mechanisms by which primates evaluate potential allies; familiarity with kin, or long-term coresidence with unrelated individuals, may be similarly
effective in promoting reciprocal alliances (Kummer, 1978; Gouzoules, 1984;
Small, 1993).
Kinship does not always lead to the expression of cooperation among related
individuals. Among the three atelin genera, for example, there are pronounced
differences in the degree of cooperation between philopatric males. In both spider
monkeys and muriquis, male kin cooperate in intergroup contests over access to
females (Fedigan and Baxter, 1984; Symington, 1990; Strier, 1992c; Strier et al.,
1993). In woolly monkeys, by contrast, there is no evidence of cooperation among
male kin (Nishimura, 19901, probably because greater cohesion among females
and more parous adult sex ratios reduce intergroup competition among males €or
mates (Strier, 1994; see below). Similarly, there is no evidence of cooperation
among philopatric female lemurs (Kappeler and Ganzhorn, 1993).
It is equally difficult to make broad inferences about social relationships, even
among primates exhibiting similar patterns of dispersal and philopatry. Kinship
may be associated with stable hierarchical relationships among female baboons
and macaques, unstable hierarchical relationships among male chimpanzees, or
egalitarian relationships among male muriquis and bonobos. Variability in these
features of primate societies deviate from expectations based on “typical primates.”
Thus, just as there is evidently a need to reassess the assumptions inherent in
traditional perceptions of kinship and dispersal systems in primates, there is also
a need to reassess the assumption that primate social relationships are organized
around hierarchies mediated by aggressive competition.
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242
MYTH OF THE TYPICAL PRIMATE
243
Dominance, aggression, and competition
Theoretical origins
The widely held premise t h a t aggressive competition is a central component of
primate social relationships owes its origins to the visible drama of displays of
aggression and to a preoccupation with the origins of human warfare and aggression during the years following World War I1 when primate field studies were
gaining momentum (de Waal, 1992; Silverberg and Gray, 1992). Early field primatologists devoted considerable efforts to developing ethograms for aggressive
and submissive behaviors, and to constructing dominance hierarchies based on
consistent aggressive interactions between winners and losers.
The “typical” primate society was characterized as one in which group members
could be linearly ranked, both individually, based on the outcome of dyadic interactions, and dependently, based on the outcome of interactions involving coalition
partners (De Vore, 1963). In these “typical primates,” adult males are larger t h a n
females in both body size and canine size, and are individually dominant over
them. Males and females each vie aggressively amongst themselves for status
within their respective hierarchies, although aggression among females was considered more subtle and less likely to escalate into canine-flashing fights that
might injure themselves or their infants (Smuts, 1987). The more egalitarian societies and lower levels of sexual dimorphism in chimpanzees and bonobos set them
closer to the egalitarian nature of human hunter-gatherers than to the hierarchical “typical primates,” further justifying the distinction of these apes as exceptional among nonhuman primates. Yet, aggressive competition among related
males is even rarer in bonobos than in common chimps (Ihobe, 1992), suggesting
that even exceptions to the “typical” primate patten are themselves deviant. The
discovery of a striking degree of variability in dominance styles among different
macaque species further illustrates how comparative data have undermined the
assumption of a “typical” cercopithecine primate from within (de Waal and Luttrell, 1989).
Functional explanations for aggressive competition have focused on the importance of obtaining priority of access to limited resources that affect reproductive
success (Bernstein, 1981). These critical resources should differ for males and
females because of fundamental biological sex differences (Clutton-Brock and
Harvey, 1978; Wrangham, 1979, 1982). In primates, as in other mammals, female
reproductive success is constrained by the time and energetic demands of gestation
and lactation, which are affected by nutritional condition. Data from captive and
field studies alike indicate that better-fed females begin reproducing at a n earlier
age, produce healthier offspring, have shorter interbirth intervals, and live longer
to reproduce (Dittus, 1979; Mori, 1979; Small, 1981; Whitten, 1984). Thus, the
most pervasive resource limiting female reproductive success is food, particularly
high quality, high energy food, and females should compete with one another for
access to the best food and feeding sites. Male reproductive success, by contrast, is
constrained primarily by access to fertile females, whose inherently greater investment in reproduction via gestation and lactation is limiting to males (Rivers,
1972). Consequently, males should compete with one another for access to mates.
The frequency and intensity of aggressive competition should vary both interand intraspecifically according to diet and to seasonal and annual fluctuations in
food availability for females (McKenna, 1979) and to the number of receptive
females and the degree of female reproductive synchrony for males (see below).
Frugivorous female primates should compete more than folivores for access to their
higher quality, more sparsely distributed fruits, and in general, females should be
more competitive when preferred foods are scarce. In many species, however, female behavior may not be entirely consonant with these generalized predictions.
In the frugivorous spider monkeys and chimpanzees, for example, females rarely
compete overtly with one another for access to food, and females avoid feeding
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YEARBOOK OF PHYSICAL ANTHROPOLOGY
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Competition by avoiding one another unless large patches of fruit are available.
Thus, rather than leading to aggressive relations among females, the high costs
associated with direct competition apparently favor fluid, fission-fusion patterns of
association that minimize opportunities for direct contests in these frugivores
(Klein and Klein, 1977; Wrangham and Smuts, 1980; Chapman, 1988; Symington,
1990; but see Chapman and LeFebvre, 1990).Conversely, although leaves and other
herbaceous vegetation may be more widely available than fruit, there are differences in the quality of these abundant foods (Glander, 1978). These qualitative
differences should lead to competition between females for access to the highest
quality items (Watts, 1985). Yet, aggressive contests for these foods may be inhibited by the energetic limitations associated with a low-energy diet (Milton, 1984).
Polygynous males should compete more than monogamous males due to a
greater variance in reproductive opportunities, and among polygynous primates,
competition between males should be greater when female reproduction is asynchronous rather than synchronous. However, efforts to identify a positive relationship between male dominance rank and reproductive success have met with only
limited success for a t least three interrelated reasons. First, it has become increasingly evident that inferring male reproductive success from observed mating success or copulatory frequency is inappropriate (Hausfater, 1975). Data from studies
on a diversity of primates reveal that a substantial proportion of matings occur a t
times in a female’s cycle when she is not ovulating, and therefore not likely to
conceive (reviewed in Martin, 1992). Differences in sperm quantity and quality
may also lead to variation in male fertilization success (Smith, 1984; Parker et al.,
1990; Curtsinger, 19911, further confounding the accuracy of inferences about male
reproductive success from mating success. Paternity tests are ultimately necessary
to establish how male mating behavior corresponds to male reproductive success
because all copulations are not equally responsible for conceptions. Similarly, more
detailed knowledge of female reproductive biology is necessary to evaluate the
diverse relationships between sex and reproduction (see below).
Closer scrutiny of male dominance relationships has also revealed that hierarchies constructed from the cumulative outcomes of dyadic interactions do not necessarily reflect dominance relationships among males in particular contexts. A
male may routinely submit to others a t feeding or resting sites, but nonetheless
consistently win contests over access to sexually receptive females (Popp and DeVore, 1979). Even when the outcomes of aggressive interactions between males are
differentiated by the contexts in which they occur, a male’s position in the hierarchy changes repeatedly throughout his lifetime in response to shifts in his competitive ability, opportunities for establishing reliable coalitions with other males,
and demographic factors that may alter the competitive pressures he faces (Hausfater, 1975). Accurate measures of male lifetime reproductive success are essential
to evaluating the effects of male rank, yet such measures are difficult to calculate
even with paternity tests because primate lifespans may exceed researchers’ careers.
A final confounding factor involves the growing recognition that in many species, males may employ subtle, nonaggressive forms of competition to secure fertilizations. The effectiveness of these alternative strategies, which include winning
female mate choice (Strum, 1982; Smuts, 19851, manipulation of coalitions and
alliances with females and other males (Packer, 1979331, and sperm competition
(Harcourt et al., 1981; Smith, 19841, may be independent of or inversely related to
a male’s ability to compete aggressively (Popp and DeVore, 1979). Females also
engage in subtle forms of competition, including their preference for mating with
particular males that may provide resources or protection for themselves and their
infants (Smuts, 1985, 1987), the manipulation of coalitions and alliances with
other females as well as males (Kummer, 1967; Hrdy, 1981), and in some species,
through pheromonal and/or behavioral inhibition of ovulation in other females
(Wasser and Barash, 1983; Dunbar, 1984; Abbott, 1989).
The use of nonaggressive competitive strategies may reflect the high costs of
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244
MYTH OF THE TYPICAL PRIMATE
245
direct contests between individuals, particularly when the benefits of cooperation
in between-group competition inhibit the expression of aggression among members
of the same groups (Vehrencamp, 1983; Wrangham, 1980; van Schaik, 1989; van
Hooff and van Schaik, 1992; Strier, 1992b, 1994). Thus, most primate social dynamics can be interpreted as a set of compromises between divisive intragroup
competition and the benefits of cooperation among group members during intergroup competition, whether among females over food or among males over mates,
and in terms of the value of social partners (Kummer, 1978; de Waal, 198913).
Consequently, the relative importance of aggressive and nonaggressive tactics is
expected to vary both intra- and interspecifically with ecological and demographic
variables (Wrangham, 1982; van Schaik, 1989; van Hooff and van Schaik, 1992).
The costs of aggressive tactics may also vary among species and among individuals. For example, the risks of fighting may be greater for large bodied primates in
arboreal habitats than in the terrestrial ones occupied by most “typical primates”
(Strier, 1992b). Similarly, while males in their reproductive prime may be more
able, and therefore more willing, participants in aggressive competition (Popp and
DeVore, 1979), females may be more willing to risk injury toward the end of their
reproductive careers (Hrdy, 1981). Thus, habitat and individual life histories, a s
well as population density and diet, affect the expression of aggression and alternatives to aggression across primates.
Because nonaggressive competitive strategies are often quite subtle, they were
not as obvious to early primatologists. Recent data from longitudinal studies of
both typical and atypical primates demonstrate that broad generalizations about
the importance of dominance and aggression are as species- and context-specific a s
those between dispersal and nepotism. Aggressive competition, like kinship, continues to be one of the ways in which the social relations of some primates can be
understood. However, social skills and the ability to manipulate the behavior and
in some instances, the physiology, of competitors may be equally important to
characterizing primate social relationships. In their social interactions and social
relationships, primates are proving to be more diverse both within and between
species than implied by the myth of the “typical primate.”
Female-female dynamics
Nearly all cercopithecine primates living in matrilineal societies associate in
cohesive groups. Females form the core of these groups, whether they are multimale or single-male. Female membership in these groups is stable, and female
hierarchical relationships are usually, but not always, influenced by inherited
rank reinforced by coalition support (Walters, 1980; Altmann et al., 1985; Chapais,
1985; Hausfater et al., 1987; Mori et al., 1989; also in female-bonded capuchins:
O’Brien and Robinson, 1993). Wrangham (1980) linked female cohesive kin groups,
stable affiliative relationships, and relatively stable (compared to males’) hierarchical relationships to the advantages of cooperation in intragroup feeding competition (Fig. 3). According to this model of female-bonded primates, females benefit by stable, kin-mediated relations when the advantages of cooperation in
intergroup feeding competition outweigh the costs of intragroup feeding competition. If competition among group members is greater than that between groups,
females should avoid competing with their kin by dispersing (Wrangham, 1982).
Extreme examples of avoiding such high intragroup interference competition may
result in the female dispersal and fluid grouping patterns found in common chimpanzees and spider monkeys. Female dispersal in muriquis, however, cannot be
explained by high intragroup feeding competition because muriquis feed at large
patches of preferred fruit, consume substantial quantities of abundant leaves when
fruit is scarce, and do not compete directly for food or feeding sites (Strier, 1989,
1991b). The proximate or phylogenetic causes of female dispersal remain undocumented in each of these species.
van Schaik (1989) further extended the distinctions between intra- and intergroup competition for categorizing female primates by distinguishing between
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[Vol. 37, 1994
WRANGHAM’S (19801 MODEL OF FEMALE-BONDED PRIMATE GROUPS
FOOD DISTRIBUTION
,
Preferred foods
not patchy or defendable
OR occur in small patches
Preferred foods
occur in large, defendable
patches U a b u n d a n t
subsistence foods eaten
when preferred foods are
scarce
I
NOT FEMALE-BONDED
Females can
be herded
Females disperse
FEMALE-BONDED
Territorial
Nonterritorial
I
I
,
SINGLE-MALE
MULTI-MALE
SINGLE-MALE MULTI-MALE
(males cooperate)
(males compete)
Fig. 3. Schematization of Wrangham’s (1980) model of female-bonded primates.
contest and scramble types of competition. He predicted that female bonding
should occur when the costs of within group contest competition are offset by the
benefits of cooperating with female kin in between group contest competition.
Among such female-bonded groups, however, patterns of affiliative interactions
suggest that although matrilines may cooperate with one another in intergroup
competition, they otherwise remain strongly differentiated (Cheney, 1992).
When within group contest competition is stronger than between group competition, as is assumed to be the case in specialized frugivores, females should split
up, thereby avoiding direct competition with female kin and precluding the formation of strong afiliations and stable, long-term relationships with one another,
as Wrangham (1980) proposed. Alternatively, within or between group feeding
competition may be of the scramble type due to a dietary reliance on abundant and
evenly distributed foods such a s leaves, grass, and herbaceous vegetation. In these
cases, there should be few benefits to cooperative strategies and the pressures
favoring female bonding should be relaxed.
Gelada and hamadryas baboons are the principal cercopithecine exceptions to
this model for strikingly different reasons (Dunbar, 1986). The diet exploited in the
arid habitat occupied by hamadryas baboons is believed to preclude the formation
of female-bonded groups. Instead, hamadryas baboons have a multilevel society
(Abegglen, 19841, unusual among nonhuman primates (Rodseth et al., 1991; but
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YEARBOOK OF PHYSICAL ANTHROPOLOGY
246
MYTH OF THE TYPICAL PRIMATE
247
see also Robinson et al., 19871, i n which male-male competition determines female
patterns of association. Gelada females, by contrast, conform to the social criteria
of female-bonded primates despite their dietary reliance on abundant, herbaceous
vegetation. Female bonding in gelada baboons may be a secondary strategy employed for social rather than dietary purposes: by bonding together, gelada females
can increase group size in response to high predator pressure (Dunbar, 1986; see
below).
I n primates in which either females or both females and males routinely disperse, hierarchical relationships tend to be based on demographic factors such a s
length of residency in the group, female age, or female reproductive condition
(Hanuman langurs: Hrdy, 1977; mantled howler monkeys: Jones, 1980) rather
than kinship. Furthermore, in some nonfemale-bonded species such as hamadryas
baboons and mountain gorillas, females may associate, a t least in part, as a result
of male efforts a t herding them together (Wrangham, 1980). When males are
experimentally removed or die of natural causes, female associations may disintegrate (but see Stammbach, 1978). In other species, female relations are egalitarian rather than hierarchical (e.g., muriquis: Strier, 1990; squirrel monkeys:
Baldwin, 1992). Resources for these females are either not limited, or else the
benefits of establishing and maintaining priority of access to resources are offset by
high energetic or other constraints (Milton, 1984; Strier, 1992b,c).
Competition for access to preferred foods is only one way in which females can
maximize their reproductive opportunities. Unrelated females form alliances to
prevent new females, and thus potential food and reproductive competitors, from
immigrating into their group (howler monkeys: Sekulic, 1982; Crockett, 1984;
Glander, 1992; Peruvian squirrel monkeys: Mitchell et al., 1991; muriquis: Strier,
1 9 9 2 ~ )Furthermore,
.
females may compete directly for access to preferred mates
which will invest in them or their infants (Smuts, 1985) or for infant care by
inhibiting ovulation in subordinates (Abbott, 1989). Such helpers have been considered to be essential to relieve the high energetic costs on mothers, particularly
among callithrichids which routinely give birth to twins (Goldizen, 1987, 1990).
However, there is evidence t h a t males may provide more infant care than nonreproductive females (reviewed in Snowdon, 1990a).
Inhibiting their own reproduction while helping their mothers to rear siblings
could be perceived a s a n extreme example of cooperation among female primates,
although i t is more likely that it is a case of making the best of a bad situation. If
opportunities for dispersing and founding their own reproductive groups are limited, daughters may benefit their inclusive fitness by remaining in their natal
groups and assisting their mothers in the rearing of siblings (Emlen and Vehrencamp, 1983; Goldizen, 1987; Snowdon, 1990a; see below). Less ambiguous forms of
cooperation among reproductively active females have, however, been documented
in many other primates. These cooperative alliances tend to be strongest among
the female-bonded primates, where females routinely intervene on behalf of their
kin against unrelated females and against males (Waiters, 1980; Smuts, 1987).
However, in both matrilineal and nonmatrilineal societies, female alliances are
effective a t influencing male residence or associations with female groups in single-male polygynous (e.g., langurs: Hrdy, 1977) and multimale polygamous societies (e.g., Japanese macaques: Packer and Pusey, 1979; capuchins: O’Brien, 1991;
muriquis: Strier, 1992c; bonobos: Furuichi, 1989; Ihobe, 1992) and a t defending
food resources during encounters with other groups of females (e.g., vervet monkeys: Cheney, 1987; Peruvian squirrel monkeys: Mitchell et al., 1991; muriquis:
Strier, 1 9 9 2 ~ ) .
Strong female social bonds may also occur when females are unrelated and
exhibit weak dominance relationships. In bonobos, for example, females engage in
frequent genital-genital, or g-g, rubbing, a behavior that has been attributed to
regulating tension under potentially stressful situations (de Waal, 1987). The expression of conciliatory interactions, like that of aggression, is highly variable both
between distant taxa and across closely related species (de Waal, 1989a).
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YEARBOOK OF PHYSICAL ANTHROPOLOGY
[Val. 37, 1994
The occurrence of strong female affliative relationships, cooperation, and reconciliation among both female-bonded and nonfemale-bonded primates does not
imply that females are more passive or less aggressive than their male counterparts. Females may be more likely than males to avoid direct confrontations that
increase the risk of injury to themselves or their infants (Smuts, 1987), particularly in species where males are larger and more equipped to inflict such injuries.
Forming alliances with other females may be an effective strategy for protecting
themselves from male aggression when males are individually dominant (Smuts,
1987; but see Packer and Pusey, 1979), but the risk of male aggression, and consequently the advantages of such alliances, are minimal in species in which females are dominant over, or codominant with, males (Strier, 1990; Kappeler and
Ganzhorn, 1993).
Male-male dynamics
Female mate choice can have profound consequences for the outcome of malemale competition over access to females, but identifying what traits females favor
in males has remained elusive (Small, 1989). Both female choice and male-male
competition directly affect male reproductive success, but they are interrelated
processes that cannot be easily distinguished. In a captive study, female hamadryas baboon preferences for particular males were perceived and respected by
other males, although the bases for these mate choices were unclear (Bachmann
and Kummer, 1982). Similarly, although dominant male olive baboons and chimpanzees may be able to aggressively interfere with copulations by subordinates,
females are nonetheless highly successful at maneuvering themselves into mating
consorts with preferred male associates (Tutin, 1979; Strum, 1982; Smuts, 1985).
Males may solicit favoritism by maintaining proximity with a female, grooming
her regularly, and providing protection and defense for both her and her infant.
Establishing these associations appears to be a strategy employed both by new
immigrant males as a means of achieving acceptance into a group (Strum, 1982)
and by mature males which possess the sophisticated social skills required to gain
a female’s trust (Smuts, 1985). Yet, despite the importance of such affliative
competitive strategies, less than 60% of male “friends” were possible fathers of
infants born during one study of olive baboons (Smuts, 1985). The fact that high
ranking males may be able to achieve substantial mating success without investing in friendships suggests that aggression may be a more effective strategy for
males that are able to outcompete their opponents in direct contests. Because their
competitive abilities fluctuate over their lifetimes, males may shift between aggressive and nonaggressive strategies as they mature and their relationships to
both females and male competitors change. Aggressively competing with other
males and establishing affliative relationships with females to obtain female
choice need not be mutually exclusive strategies. Indeed, switching tactics in response to changing demographic and social conditions is common in many animals
(Milinski and Parker, 1991).
The ability to win overt contests-and all that winning implies about a male’s
ability to defend the resources females need or females themselves-may also be
one of the criteria that some females use in choosing their mates. In brown capuchin monkeys, for example, females preferentially solicit copulations with the
alpha male in their group, presumably because of the greater protection alpha
males can provide females and their infants (Janson, 1984). In Costa Rican squirrel monkeys, males exhibit low levels of aggression except during the brief period
when females are sexually receptive (Baldwin, 1992), and during one breeding
season, the largest male accounted for 70% of all copulations observed (Boinski,
1987). Male-male aggression outside of the breeding season is also rare in black
and white ruffed lemurs, where females appear to mate preferentially with familiar rather than unfamiliar males (Morland, 1993). Thus, whether females mate
with male associates or dominant males at times when they are most likely to
conceive appears to be highly variable both within and between species.
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248
MYTH OF THE TYPICAL PRIMATE
249
As in females, the frequency and intensity of male-male aggression within multimale societies varies across species, ranging from the hostility displayed by many
cercopithecines, to the mixed aggressive and affiliative interactions observed in
chimpanzees and spider monkeys, to the seasonally restricted aggressive interactions in squirrel monkeys and lemurs, to the high levels of tolerance exhibited by
bonobos and muriquis. This spectrum of male-male relationships is related to the
reproductive pay-offs of aggression, which are related, in turn, to how easily females can be monopolized.
Male strategies appear to reflect a compromise between competition for access to
groups of females, or between group competition, and competition for access to
individual females, or within group competition. Several variables have been invoked to differentiate the strength of between group competition, including dispersal patterns, group size, female grouping patterns, and the ratio of reproductive-aged females to males, or the socionomic sex ratio (van Hooff and van Schaik,
1992; Strier, 1994). If males disperse from their natal groups, they must first gain
entrance to a group containing females, which often requires a combination of
rebuffing antagonism from resident males and insinuating themselves into the
group by establishing friendships with group residents. Once tolerated in a group,
they must then begin to work their way up the male hierarchy through aggressive
interactions or develop female support, as is the case in olive baboons (Strum,
1982, 1983; Smuts, 1985), or by transferring and maintaining coalition support
with male kin in some macaques (Melnick and Pearl, 1987). In Hanuman langurs,
males may cooperate with one another in ousting a resident male, and only afterward do they begin fighting amongst themselves for exclusive access to the female
group. Once a single male has succeeded in monopolizing a group of females, he
must still defend his position in between group competition. The killing of infants
sired by the previous male following a take-over to bring females into estrus a s
early as possible during a new male’s own tenure in the group may be a final
extension of within group competition (Hrdy, 1977; but see Bartlett et al., 1993),
but apart from this, obtaining access to a group of females may be close to the
equivalent of obtaining access to individual females.
In species where males generally remain in their natal groups, such a s chimpanzees, spider monkeys, and muriquis, defending access to fluid groups of females
from other groups of males may require extensive cooperation because it is difficult
for males to track females that do not always associate together. This cooperation
may be facilitated by kinship among philopatric males, but kinship does not necessarily imply that male kin will always cooperate with one another. Male philopatry occurs in both bonobos and woolly monkeys, yet, for different reasons, between group competition does not appear to be strong enough to promote male
cooperative alliances in either case (Furuichi, 1989; Nishimura, 1990). van Hooff
and van Schaik (1992) have suggested that group size and female grouping patterns are important determinants of male-male cooperation in between group competition. However, among the patrilineal New World atelin monkeys, female
grouping patterns and the socionomic sex ratio appear to be more important t h a n
group size in determining how easily groups of females can be monopolized (Strier,
1994). Cohesive groups with relatively low female-to-male sex ratios in woolly
monkeys may be more easily monopolized in between group competition, reducing
the benefits of cooperative male alliances, than fluid groups with high female-tomale sex ratios in spider monkeys and muriquis, which are more difficult to defend
without cooperation.
The importance of between group competition to male relationships and reproductive opportunities is based on the assumption that primate social groups are the
equivalent of closed breeding groups (Melnick et al., 1984; Richard, 1985a; Cords,
1987; Moore, 1992). In fact, although most copulations occur within groups, many
female primates also copulate, and may conceive, with extragroup males (ringtailed lemurs: Sussman, 1992; sifaka: Richard, 1985a; patas monkeys: Rowell and
Chism, 1986; Harding and Olson, 1986; forest guenons: Rowell and Chism, 1986;
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Cords, 1987; Barbary macaques: Mehlman, 1986; Small, 1990; Japanese
macaques: Sprague, 1992; muriquis: Strier, 1994). Sexual access to females may
still be the primary reason why males associate in heterosexual groups, but such
associations may not be as effective at monopolizing access to female groups as is
generally thought (Moore, 1992).
The importance of sexual access to particular females within groups is more
clear-cut, because while a male that does not belong to a heterosexual group may
still have opportunities to fertilize females, a male that is unable to mate will not.
The degree of competition among males for sexual access to ovulating females may
be most strongly affected by the ratio of estrous females to males at any particular
time, or by the degree of female reproductive synchrony (Andelman, 1986; Caldecott, 19861, and the degree to which males can dominate females (Budnitz and
Dainis, 1975; Strier, 1990, 1994). It should be more difficult for a single male to
monopolize copulations as the number of females ovulating at any time increases
(Berenstain and Wade, 1983; Cowlishaw and Dunbar, 1991). Thus, aggressive
competition throughout the year may be less pronounced in species with tightly
synchronized breeding seasons than in those in which female receptivity is asynchronous. Males may compete for access to dominant females, older females that
have already demonstrated their success at motherhood, or young females that
have not yet conceived (Stephenson, 1975; Lindburg, 1983) but the potential variance in male reproductive success, and consequently, the degree of within group
competition, should be lower when there are too many estrous females for a single
male to monopolize. In strongly seasonal breeders, such as lemurs and squirrel
monkeys, males rarely engage in aggressive interactions when females are not
receptive (Richard, 1974; Richard and Dewar, 1991; Boinski, 1987; Baldwin, 1992).
Similarly, the tolerant social relationships among male bonobos, which contrast
with the aggressively mediated hierarchical relationships of common chimpanzees, have been attributed to the more prolonged period of sexual receptivity of
female bonobos (Furuichi, 1989). Ecological factors that affect female reproductive
cycles, and physiological factors that affect female receptivity, play important roles
in the degree of male-male aggressive competition.
Monopolizing receptive females requires that females accept the outcome of
male-male competitive efforts. In “typical primates,” in which males are dominant
over females, females may associate and mate with preferred subordinate males,
but dominant males can still interfere with female efforts to exercise choice. Not
all primates are “typical,” however. Muriquis provide a n extreme example of the
consequences that female codominance with males may have on male social relationships and reproductive competition (Strier, 1990, 1994). Codominance may
provide female muriquis with greater opportunities to express their mate choices,
effectively overriding any benefits of male-male aggressive competition. If males
cannot harass females into copulating, and females do not favor aggressive males,
a male muriqui’s best strategy may be to tolerate male allies for their support in
competition with other groups of male kin, and compete for fertilizations through
more subtle means, such as sperm (Milton, 1985a; Strier, 199213)or ejaculate plugs
(Strier, 1 9 9 2 ~ ) .
Sperm competition is just one of many alternatives to aggressive competition
exhibited by male primates, and it may be a form of competition that females
exploit or incorporate into their own reproductive strategies (Small, 1988). I t is
thought to occur in those species where the benefits of male-male aggression are
offset by the necessity of cooperative alliances (Harcourt et al., 1981) or by female
codominance (Strier, 1990, 1992b). Paradoxically, there is little evidence among
lemurs for sperm competition, a t least as measured by testes size, despite female
dominance over males (Kappeler and Ganzhorn, 1993).
Among some primates, such as yellow baboons and Barbary macaques, males
may use infant care to establish affiliative relationships with females (Stein, 1984;
Small, 1990). Among howler monkeys, Hanuman langurs, yellow baboons, and
mountain gorillas, by contrast, males may commit or threaten to commit infanti-
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MYTH OF THE TYPICAL PRIMATE
251
cide to secure access to estrous females (Hrdy, 1979; Smuts and Smuts, 1993; but
see Bartlett et al., 1993). In any species in which social relationships are hierarchical and males are dominant over females, females are vulnerable to attacks
directed by other females or males toward them and their infants (Smuts and
Smuts, 1993).Protection from such aggression may a resource that males in these
species can offer females in exchange for mating opportunities.
Female-male dynamics
The assumption that male aggression toward females and their young is a n
important dynamic in heterosexual relationships is based on the fact t h a t the
“typical” male primate is larger in body size and canine size than the female.
Traditional sexual selection theory has explained the widespread occurrence of
sexual dimorphism in terms of the advantages of size and weaponry in male-male
competition for mates (Alexander et al., 1979). Although sexual dimorphism is
prevalent among anthropoids, the degree of dimorphism tends to vary with the
degree of male-male aggressive competition and other ecological constraints such
as seasonally and spatially limited food and female availability (e.g., Popp, 1983;
Rodman, 1984). In the lemurs, by contrast, males and females are more closely
monomorphic despite radical differences in their social systems (Richard and
Dewar, 1991).
Greater similarity in body and canine size appears to be associated with greater
equity between the sexes. Females are dominant over, or codominant with, males
in the relatively monomorphic callitrichids (Sussman and Garber, 1987), and
muriquis (Milton, 1985b; Rosenberger and Strier, 1989), a s well as the lemurs
(Kappeler and Ganzhorn, 1993). Energetic costs of gestation and lactation may
limit how large females can become (Demment, 1983), and females may have to
rely on alternatives to brute force to assert themselves. It is possible, for example,
that the formation of cooperative female kin groups is a strategy to counteract the
effects of sexual asymmetry in size, weaponry, and dominance (Packer and Pusey,
1979; Smuts, 1987; Strier, 1990) as well as for intragroup competition over access
to food resources (Wrangham, 1982). Despite numerous efforts to identify consistent relationships between levels of sexual dimorphism and intrasexual competition (e.g., Kay et al., 1988; Rosenberger and Strier, 1989; Plavcan and van Schaik,
19921, explanations for the interacting effects of phylogeny, ecology, morphology,
and behavior remain controversial.
Persisting questions
Discussions of primate aggression have traditionally revolved around the effects
of aggressive competition on reproductive success. The accumulation of examples
of alternatives to aggression has led to a better understanding of how primates
compete, but they have not yet resolved outstanding questions about why primates
compete. Captive and field studies have demonstrated that female reproductive
success varies with nutritional condition, but we still lack detailed data on how
nutrition of female primates varies in the wild (Strum and Western, 1982; Moore,
1984). How frequent are droughts and food shortages in nature? Can unpredictable
ecological crises exert strong enough pressures to select for the long-term maintenance of complex social relationships? Conversely, the assumption that male reproductive success is highly variable i n all but monogamous primates dates back
to early considerations of sexual selection theory (Trivers, 1972). Yet, how much do
most males really vary in their lifetime reproductive success (Hausfater, 1975)?
How does variation in male ability to compete aggressively or form affiliative
alliances ultimately affect which males females chose to father their offspring? We
will be unable to answer these questions, or interpret the significance of the answers, until newly developed, noninvasive methods of paternity testing are more
widely applied (Morin et al., 1993; Takenaka et al., 1993). It is important to note,
however, that such data will be limited unless they are obtained a t the level of
local populations rather than just within single study groups, particularly if there
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YEARBOOK OF PHYSICAL ANTHROPOLOGY
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is any indication that extragroup males copulate with estrous females (Melnick et
al., 1984).
Behavioral responses to demographic fluctuations in primate groups and populations are as important to understanding aggression and competition as are fluctuations in ecological and life history variables. Long-term data from different
primates reveal divergent responses to increases in population density, ranging
from increased aggression and the splitting up of established groups to the formation of larger, more tolerant aggregations (Samuels et al., 1987; Strier et al., 1993).
We know even less about the effects of shifts in adult sex ratios on inter- versus
intragroup aggressive competition (Altmann and Altmann, 1979; Dunbar, 1979;
Strier, 1994).
Lastly, it is evident that competition among female and male primates may be
mediated by their reproductive physiology. Whether through sperm competition or
ejaculate plugs among males, or ovulatory inhibition among females, we still know
very little about the proximate mechanisms by which reproductive physiology can
be manipulated. Understanding primate reproductive physiology is essential to
interpreting primate sexual behavior, especially in those cases in which a substantial amount of primate sexual activity occurs a t times other than ovulation.
Sex and reproduction
Historical perspectives
Interest in the relationship between sex and reproduction in nonhuman primates grew out of efforts to understand human sexual behavior from a comparative and evolutionary perspective. Early models focused on the social implications
of concealed ovulation and continuous female receptivity, traits that were thought
to be uniquely human (e.g., Morris, 1967; Alexander and Noonan, 1979; Ember and
Ember, 1984). Scenarios differed in their emphases, which included among others
the role of sex in securing male provisioning to enhance the survival of altricial
young, and the importance of sex to maintaining a long-term pair bond. In many
primates, however, ovulation is not advertised through visual cues and females
copulate at times in their cycles when conception is unlikely, or, in the case of
post-fertilization matings, when additional conceptions are impossible. In addition,
females in a number of polygamous taxa copulate with many more partners than
are necessary for conception (Hrdy, 1981; Small, 1988). These comparative findings clearly indicate that sex and reproduction are decoupled in many nonhuman
primates, and that the human difference is therefore quantitative, not qualitative
(Wolfe, 1991; Martin, 1992). This raises questions about the function of nonreproductive or extrareproductive sexual behavior and the origins of “situation-dependent” female receptivity (Hrdy, 1981).
Hypotheses pertaining to nonreproductive sexual behavior can be grouped into
three broad categories: 1)female strategies to confuse male confidence of paternity
and thus increase male investment andlor reduce male interference in potential
offspring (Hrdy, 1981; Harcourt, 1981; Hamilton, 1984; Wallis and EnglanderGolder, 1992); 2) female strategies to regulate tension and thus decrease the risk
of male aggression (de Waal, 1987; reviewed in Smuts and Smuts, 1993); and 3)
female strategies to acquire a range of partners, permitting them to assess male
quality and, in the case of primates with sexual swellings, to incite male-male
competition (Clutton-Brock and Harvey, 1976). These hypotheses are not necessarily mutually exclusive (Small, 1988; Wallis and Englander-Golder, 1992). For
example, confusing paternity has been invoked as one possible explanation for
promiscuous mating behavior by female baboons, which exhibit visual signs of
ovulation (Hausfater, 19751, as well as to account for nonreproductive matings
with new immigrant males in species such as Hanuman langurs, in which ovulation is concealed and new males are potentially infanticidal (Hrdy, 1979). Examples of female sexual behavior to regulate tension include females soliciting sex
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252
MYTH OF THE TYPICAL PRIMATE
253
with males that may direct or redirect aggression toward them (reviewed by Smuts
and Smuts, 19931, particularly in contexts of elevated excitement (de Waal, 1987).
Indeed, extended sexual swellings and prolonged female receptivity in bonobos
have been linked to the low levels of aggressive competition displayed by males
(Mori, 1984; Furuichi, 1989; Ihobe, 1992). Nonetheless, in all three sets of hypotheses, the implicit assumption is that nonreproductive sex has evolved as one of the
counterstrategies females employ to offset the significant risks male aggression
may pose for female reproductive success and to exert choice over males that are
individually dominant to them (Hrdy, 1981; Smuts and Smuts, 1993).
Evaluating these hypotheses about the function of nonreproductive sexual activity has been difficult due to the coincidental occurrence in many “typical” primates of a suite of interrelated and interacting traits: 1)agonistically established
hierarchical relations among males; 2) male dominance over females due to sexual
dimorphism in body and/or canine size; and 3) the predominance of male-biased
dispersal systems. The absence of visible sexual swellings signaling female ovulatory state in the majority of primates (Dixson, 1983)further confounds observers’
efforts to correlate sexual behavior with female hormonal and reproductive condition. Visual concealment may not, however, confound male detection of female
ovulatory condition, particularly when olfactory communication is employed (Ziegler et al., 1993; Converse et al., 1994).
Promiscuous or opportunistic females?
Species differences in sexual behavior are believed to correspond to differences in
social systems. Promiscuity, or mating with numerous males, is a widespread
occurrence across taxonomic groups whether females live in single-male and multimale groups, exhibit sexual swellings or concealed ovulation, or experience seasonal or aseasonal breeding. But, in most cases, even promiscuous behavior results
in an uneven distribution of copulations by males. Females in single-male groups
copulate with extragroup males during attempted take-over attempts (e.g., langurs), and females in both single-male and multimale groups may copulate with
transient males during the breeding season (e.g., patas; Barbary macaques; Japanese macaques; lemurs). If such copulations are nonreproductive, however, distinctions between social and breeding groups are less critical than if they result in
conceptions (see above; Moore, 1992).
Various functions have been attributed to promiscuous behavior, ranging from
female efforts to confuse paternity among males, to female efforts to avoid male
aggression directed toward themselves, to female efforts to ensure fertilization.
Confusing paternity may be important to ensure infant safety in species with
infanticidal tendencies (Hrdy, 1981), but it may also increase infant caretaking by
males in primates such as callitrichids. Accepting or soliciting male sexual advances may be less dangerous to females, particularly in highly dimorphic species
where male aggression may lead to serious physical injury (Smuts and Smuts,
1993) or constant harassment may lead to interrupted feeding opportunities (e.g.,
gorillas: Wrangham, 1979).
Promiscuity has been carried to extremes in two species, the bonobo and the
muriqui. High frequencies of sexual activity have been associated with prolonged
sexual receptivity in female bonobos (Furuichi, 1989). In muriquis, by contrast,
sexual receptivity is more seasonal (Strier, 1987; Strier and Ziegler, 1994). Promiscuous mating in this species has been associated with egalitarian relationships
between males and females (Strier, 1990; Strier, 1992131, which may be due to the
fact that the sexes are monomorphic, or nearly so, in both body and canine size
(Milton, 1985b; Kay et al., 1988; Rosenberger and Strier, 1989; Lemos de Sa and
Glander, 1993). Male muriquis do not threaten or care for infants, and it is still
unclear whether or not females mate with multiple partners throughout their
ovulatory cycles and whether they do so for reproductive or social advantages.
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Seasonal versus aseasonal breeders
Field reports indicate that some type of birth clustering may be common in the
majority of primates (Lindburg, 1987). The extent of such reproductive seasonality
may be correlated with ecological, demographic, and social variables, and can have
strong effects on the dynamics of primate social and mating systems (Jolly, 1967;
Baldwin, 1970; Kavanagh, 1983; Nash, 1983). Tight reproductive seasonality, and
therefore reproductive synchrony, affects the degree of male-male competition because a s the ratio of estrous females to males rises, females become more difficult
for individual males to monopolize (Cowlishaw and Dunbar, 1991; Strier, 1994; see
above). When matings occur aseasonally, individual females become potentially
defensible resources, but when reproduction is strongly synchronized, male-male
competition tends to be weakest and opportunities for female mate choice rise a s is
the case in capuchins (Janson, 1984) and squirrel monkeys (Boinski, 1987). Female
dominance in lemurs and female codominance in muriquis may be related to their
seasonal reproduction a s well a s to their sexual monomorphism and high energetic
costs (Young et al., 1990; Richard and Dewar, 1991; Strier, 1991a, 1994; Richard,
1992).
Reproductive seasonality may simultaneously limit the degree to which females
can use sex to manipulate their social relationships. Nonetheless, promiscuous
mating during the breeding season can be effective at confusing male confidence of
paternity, thereby reducing the risk of males harming potential offspring. When
male infant care is important to female reproductive success, however, there may
be advantages to actual or apparent fidelity.
Parental care of infants
All female primates, like all other mammals, bear the energetic burden of gestation and lactation. Yet, strong variability exists in the degree to which other
group members participate in infant care. In cercopithecine primates, males may
be protective of infants either to protect their reproductive interests if they are
possible fathers, or to gain female trust and subsequent mate choice if they are not
possible fathers (Whitten, 1987; Smith and Whitten, 1988). Similarly, male infant
carrying has been attributed to both male infant care and male exploitation of
infants as agonistic buffers (Stein, 1984).
Male infant care is most widely observed among the callitrichids, which exhibit
an array of mating systems ranging from monogamous to single-male polygynous
to multimale polygamous to polyandry (Goldizen, 1987). Pronounced examples of
male infant care in callitrichids, as well a s other monogamous New World primates, include males carrying infants up to 90% of the time (Wright, 1990). Traditionally, male parental investment was attributed to paternity certainty in monogamous and single-male polygynous species, and to inclusive fitness benefits in
polyandrous species, where strong associations have been found between the number of males and infant survivorship (Sussman and Garber, 1987). Yet, the fact
that estrous females may mate with extragroup males, even among monogamous
species, implies that male parental care may occur even in the absence of paternity
certainty.
High levels of male infant care have also been attributed to high metabolic
demands of small-bodied female primates (Leutenegger, 1980; Wright, 1984,1990).
Small (1990) found high levels of male alloparenting in the polygamous Barbary
macaques, a species that may also experience metabolic stress due to seasonally
low temperatures. However, nonparental caretakers may benefit directly, either
by gaining essential experience that will increase their skill when they become
parents themselves, or by enabling them to remain in a group where they may
ultimately inherit reproductive positions (Snowdon, 1990a).
Whether metabolic or social demands are responsible for male parental care in
different taxa is still unclear. Nonetheless, the fact that males in some species care
for infants that are evidently not their own further emphasizes the necessity of
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MYTH OF THE TYPICAL PRIMATE
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distinguishing behavior with potential future reproductive pay-offs from that with
immediate ones. This distinction, like that between group membership or the use
of sex for social or reproductive purposes, has important implications for the way
that primate social systems have been modeled.
MODELS OF SOCIAL SYSTEMS
The myth of the typical primate has influenced efforts to classify primate social
systems in much the same way that it has influenced characterizations of primate
social relationships. The ecological models derived from these classificatory systems aim to be predictive a s well as explanatory: If the models are sufficiently
robust, it should be possible to accurately predict the social systems of primates
from a clearly defined and quantifiable set of ecological variables. Yet, such predictions have been limited due to the combined difficulties inherent in identifying
and measuring relevant ecological variables, and in accounting for stochastic ecological and demographic events and the effects of phylogeny on physiology, ontogeny, and behavior.
Ecological models
Early efforts to identify the ecological correlates of primate social systems focused on simple ecological variables, such as diurnal versus nocturnal and terrestrial versus arboreal habits, and on simple descriptions of group composition, such
as monogamous pairbonds, single-male polygyny, age-graded polygyny, and multimale polygamy (DeVore, 1963; Crook and Gartlan, 1966). Dietary classifications
were subsequently appended, distinguishing between insectivory, frugivory, folivory, and omnivory (Clutton-Brock and Harvey, 1977). Anthropocentrism figured
prominently in many of these early models: ecological variables most closely resembling those to which hominids were believed to have evolved were inevitably
associated with more complex social systems. Thus, the age-graded polygynous or
multimale polygamous groups of “typical” diurnal, semiterrestrial, omnivorous
primates were believed to represent the most derived, human-like condition, while
the solitary or single-male polygynous groups of nocturnal, arboreal, insectivores
primates represented the most primitive condition.
As data accumulated and theoretical perspectives expanded, it became evident
that such simplistic ecological and social classifications failed to characterize important variability among and between species. Closely related species, or even
different populations of the same species, exhibit markedly different social systems, while distantly related species may exhibit strikingly similar organizations
(e.g., prosimians: Richard, 1978; Tattersal, 1978; Harcourt and Nash, 1986). Several socioecological analyses have attempted to evaluate the relative importance of
ecology and phylogeny in interspecific comparisons (lemurs: Sussman, 1977; cercopithecines: Struhsaker, 1969; mangabeys: Waser, 1984; atelines: Rosenberger
and Strier, 1989; hominoids: Wrangham, 1987). Until recently, however, the role
of phylogeny has been largely usurped by ecological models which have focused on
two basic questions: Why do most primates live in groups; and why do primates
live in the groups that they do?
Group living is presumably advantageous for three reasons: improved predator
detection and defense; improved food detection and defense; and improved access to
mates. Differences in the social systems among the majority of group living primates, as well as more solitary species, are attributed to variability in predation
pressure and fine-grained differences in the distribution and abundance of food
resources. Thus, primates such as galagos, tarsiers, and orangutans are generally
solitary except for the period when infants are dependent on their mothers and
when males and females come together to mate. In the case of the nocturnal
galagos and tarsiers, solitarity is attributed to cryptic predator avoidance (Nash,
19931, while in orangutans, it is attributed to the combination of immunity from
predators due to their large body size and avoidance of feeding competition for
access to preferred fruit (Rodman, 1984). That orangutans differ socially from the
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YEARBOOK OF PHYSICAL ANTHROPOLOGY
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ecologically similar chimpanzees has been attributed to the mediating effects of
morphology. The costs of locomotion in orangutans are thought to be higher for the
larger, more sexually dimorphic male orangutans than male chimpanzees, accounting for their failure to form cooperative patrols to defend female communities
like male chimpanzees (Rodman, 1984).
The role of predation
Group living confers several potential advantages in primates that are too large
to hide effectively from predators. Groups contain additional eyes and ears to
detect predators, reducing the need for constant vigilance by each individual.
Alarm calls may be highly specific to particular classes of predators, enabling an
individual to respond in an appropriate way without having independently seen
the danger (Seyfarth et al., 1980). Larger groups may be able to mount more
effective defenses against predators, such as mobbing, than an individual could
alone, and the presence of other possible victims may reduce the probability for any
one individual to be taken as prey, a phenomenon described as “the selfish herd’
(Hamilton, 1971).Indeed, the benefits of detecting and escaping from predators are
thought to increase with group size until the costs of feeding competition become
prohibitive; the optimum group size should reflect the compromise between these
benefits and costs (Terborgh and Janson, 1986).
Despite the advantages of group living to predation pressures, the role of predation in shaping primate sociality is highly debated. Some primatologists regard
it as minimal (e.g., Wrangham, 1979), particularly for large bodied primates and
primates inhabiting areas where human activities have eliminated naturally occurring predators (Strier, 1992~).
The latter may reflect relatively recent events,
however, raising the question of how rapidly primate behavior can adapt to changing ecological conditions. Even in less disturbed habitats where natural predators
and primates coexist, the intensity of predation on primates, and its significance
remain difficult to quantify. Successful predation events may be witnessed infrequently (e.g., Stelzner and Strier, 1981), particularly if the presence of human
observers inhibits the approach of unhabituated predators (Stanford et al., 1994).
However, high levels of predation have been documented in Costa Rican and Peruvian squirrel monkeys (Mitchell et al., 1991), and in ringtailed lemurs, where
male dispersal in cohorts instead of individuals is thought to be a response to high
predator pressure (Sussman, 1992). Observations of leopard predations on chimpanzees in the Tai National Forest (Boesch, 1991) and the discovery of chimpanzee
hair in the feces of lions (Inagaki and Tsukahara, 1993) indicate that large bodied
primates, as well as arboreal ones (Terborgh, 1983), are vulnerable prey.
Primates as predators. Even if predation events are more common than previously
thought, what percentage of all mortalities must predation account for before it
can be regarded as a serious selective force? Recently, analyses of 9 years of data
on chimpanzee predations on red colobus monkeys at Gombe National Park, Tanzania, indicate that the chimps have killed a t least 350 red colobus, accounting for
a substantial percentage of mortality in this species (Stanford et al., 1994). Gombe
chimpanzees exhibit higher predation rates than do other populations (Wrangham
and van Zinnicq Bergmann Riss, 19901, and the social organization of red colobus
monkeys at this site is believed to be influenced by chimpanzee predation pressures (Busse, 1977).
The evidence indicating that chimpanzees can be highly successful predators is
significant not only because of its potential role in the social adaptations of primate
prey species, but also because of the importance attributed to meat eating in the
course of human evolution. The transition from a vegetarian diet supplemented by
invertebrates to one involving the exploitation of large vertebrates was believed to
be a critical distinction between nonhuman and human primates. Yet, in their
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MYTH OF THE TYPICAL PRIMATE
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determined, coordinated hunting tactics, their sharing of kills, and the male-bias
in hunting activity, chimpanzees exhibit many of the behavioral traits that have
been associated with cooperation, reciprocity, and the division of labor in humans
(McGrew, 1979, 1981; Boesch and Boesch, 1989). Whether the proportion of meat
in chimpanzee diets is high enough to merit comparisons with the role of meat in
human diets remains controversial. The question provides, nonetheless, an extreme example of the persisting difficulty of characterizing primate diets and the
effects of dietary variables on social behavior.
Characterization of primate diets
Annual proportions. Primate diets have traditionally been characterized by calculating the average proportion of feeding time devoted t o different food types,
which for most primates is some combination of fruits, leaves, flowers, seeds, and
insects or other invertebrates (Hladik, 1981). Species have been classified as insectivorelfrugivores, frugivorelfolivores, folivorelfrugivores, or omnivores based on
the predominant food types in the annual diet (Richard, 198533). These dietary
classifications have been correlated with morphological traits, including body size,
dentition, and gut specializations (Kay, 19841, although recent analyses indicate
that taxonomy is a stronger predictor of diet than body size in many New World
monkeys (Ford and Davis, 1992; Strier, 1992a) and lemurs (Richard and Dewar,
1991). Dietary type has also been linked to behavioral variables including day
range length, home range size, and the degree of intra- versus intergroup feeding
competition (e.g., Milton and May, 1976; Clutton-Brock and Harvey, 1977).
Despite the utility of such classificatory systems, there are numerous limitations
to such simplifications (Rosenberger and Strier, 1989). First, proportions of feeding
time on different food items fail to consider the significance of handling and search
times, absolute food weights, caloric content, or nutritional value (Richard, 1985b).
In a study of red howler monkeys, Gaulin and Gaulin (1982) found that the importance of fruits and leaves in the diet differed markedly depending on which
measure was used.
Second, annual averages fail to take into account the importance of seasonal or
year-to-year variations in food availability and, consequently, diet. From an evolutionary perspective, ecologically stressful periods are likely to play a highly
significant role in selecting for morphological specializations (Rosenberger and
Kinzey, 1976). Pronounced seasonal shifts in food availability have been identified
in nearly all studies where phenological data have been collected, and primates
respond to these fluxes in preferred food availability by either shifting their diet to
more abundant foods or by shifting their behavior, including ranging and grouping
patterns (Wrangham, 1980). Although most researchers regard such dietary or
behavioral shifts as examples of adaptive responses, one result is that inferences
about food preferences generated from morphology may be inconsistent with direct
observations of feeding behavior at any particular time (Rosenberger and Kinzey,
1976).
Finally, distinguishing primate diets by the predominant food type may lead to
inconsistencies in the predicted relationship between diet and behavior. For example, frugivorous primates have been described as following a strategy that maximizes energy intake, in contrast to the strategy of minimizing energy expenditure
followed by folivores (Milton, 1980). Frugivores spend less time resting and travel
longer distances than more folivorous primates, presumably because fruit is both
higher in energy and more patchy in distribution than leaves. Yet, among the New
World ateline primates, which include the frugivorous spider monkey and the
folivorous howler monkey, there is substantial overlap in the annual proportion of
feeding time devoted to fruits and leaves between seasons and between habitats
(Strier, 1992a). Muriquis fall within the range of folivory documented for howler
monkeys, yet in nearly every feature of their behavior, including day range length,
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home range size, group size and composition, and group cohesion, muriqui behavior more closely resembles the energy maximization strategy of spider monkeys.
Such comparisons among closely related species avoid the potentially confounding effects of phylogeny on behavior (Glutton-Brock and Harvey, 1984).
They emphasize the limitations of predicting behavior from broad dietary categories based on annual feeding times alone, and suggest that, if dietary data are
the only information available, then the most meaningful interspecific comparisons are likely to be restricted to sympatric primates confronting similar ecological pressures a t particular times (e.g., Strier, 1992a; Tutin and Fernandez,
1993).
Inconsistencies in the predicted relationship between diet and behavior have
also been documented in comparisons between Costa Rican capuchin monkeys and
African redtail monkeys, further illustrating the difficulties of generalizing about
social behavior from dietary categorizations (Fedigan, 1993). Despite similarities
in the proportion of different food types in the diets of these primates (Robinson
and Janson, 19871, Fedigan (1993) found t h a t capuchin intersexual relations deviated substantially from those observed in redtail monkeys and predicted from
the ecological analogy. She suggests that a more informative description of capuchin monkey foraging strategies, “opportunistic, extractive foraging,” would be
more appropriate to understanding their behavioral ecology than the proportion of
fruits, insects, and leaves in their diets.
Distribution in time and space. Efforts to evaluate the effects of food distribution
on primate behavior have distinguished food types by whether they occur in discrete patches of limited size, such as fruiting trees, or in abundant, even distributions, such as grass and many leaf sources (Wrangham, 1980). Patchy foods are
potentially defensible, with the benefits of such defense depending on the correspondence between patch size and group size. Fruit is also regarded as a preferred
food for most primates because it is higher in readily available energy than leaves
(Wrangham, 1980). Consequently, the size, distribution, and abundance of patchy
fruit resources should determine the degree of intra- and intergroup feeding competition. How primates, especially females, respond to seasonal fluctuations in the
availability of fruit patches should determine their social options (Wrangham,
1980;van Schaik, 1989). When large fruit patches are scarce, females should either
fission into smaller feeding parties to avoid within group contest competition with
one another, or remain together and cooperate in defending whatever large
patches may occur in between group contest competition. In the latter case, i t is
also necessary that they can shift their diets to less preferred but more abundant,
evenly distributed foods to avoid the high costs of intragroup feeding competition.
The physiological ability to accommodate dietary shifts to lower quality foods, a s
well as the relative availability of preferred foods, should determine which of these
strategies females adopt.
While useful in principle, dichotomizing primate diets into patchy, high quality
fruits versus evenly distributed, low quality leaves is somewhat misleading. Differences in leaf quality can be as pronounced as those between fruits and leaves,
and the distribution of leaves that are low in digestion-inhibiting tannins or other
secondary compounds may be as patchy a s that of many fruits (Glander, 1978).
Furthermore, although there is evidence suggesting that protein and other nutrients, as well as carbohydrates, play important roles in primate food preferences, we
still know remarkably little about the digestive physiology and nutritional requirements of the vast majority of primates, on the one hand, and the chemical
composition of most primate foods, on the other (Oftedal, 1992).
Demography, as well as social systems, may be strongly affected by disease as
well as the spatial and temporal availability of primate foods (Coelho et al., 1977).
Sharp population declines have been documented after extended periods of drought
in many Old World monkeys (e.g., yellow baboons: Altmann and Altmann, 1970;
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MYTH OF THE TYPICAL PRIMATE
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olive baboons: Sapolsky, 1986; toque macaques: Dittus, 1979; vervet monkeys:
Wrangham, 19811, and disease has periodically swept through the Gombe chimpanzees (Goodall, 1986) and Panamanian howler monkeys (Collias and Southwick,
1952; Smith, 1977). In addition, human habitat disturbance and poaching have
fragmented many primate populations and decimated their numbers (Mittermeier
and Cheney, 1987). Understanding behavioral responses to both naturally occurring and human-induced fluctuations in group and population size and composition may ultimately provide critical insights into the determinants of primate
social systems (Neville, 1968; Durham, 1971; Anderson, 1983). Even with such
attention to demographic and phylogenetic variables, the question of whether primate social systems can be modeled in a predictive or deterministic way remains
controversial (Rowell, 1993; see below).
Categorical versus continuous variation across primates
Disagreements over the relative importance of predation pressures or food availability and distribution in the evolution of primate social systems, like nearly
every feature of primate social behavior reviewed thus far, illustrate the limitations of imposing discrete categorical alternatives on complex phenomena that are
actually continuous variables (Clutton-Brock and Harvey, 1984). Primates classified as frugivorous eat foods other than fruit, and even reproductive success, the
common currency in all evolutionary theories, is a relative term. While categorical
classificatory systems may be useful a s a first approximation in ordering primate
behavioral diversity, they risk obscuring important similarities and continuities.
Similarly, there has been a tendency to interpret correlations between behavioral and ecological variables as evidence of causality (Clutton-Brock and Harvey,
1984). For example, primate day ranges may decrease as the degree of folivory
increases, but the reason for this apparent relationship is not clear. Are leaves
more densely distributed than other food types, or do folivores tend to live in
smaller groups with lower feeding requirements? Potentially confounding variables, such as group size, are not always so obvious and they may affect different
species to different degrees. Indeed, deterministic models of behavior are particularly problematic when ecological and phylogenetic variables are treated as partially, but not fully overlapping sets (Fig. 4). Comparisons between sympatric
species and between populations of the same or closely related species occupying
different habitats can help to tease apart the dynamic, interacting effects of ecology and phylogeny on social behavior (e.g., Mitchell et al., 1991; Fedigan, 1993;
Kappeler and Ganzhorn, 1993). Without such appropriate comparisons, efforts to
develop and expand comprehensive models of primate behavior risk being overwhelmed by the diversity of primate adaptations.
Intra- versus interspecific variation
Similarities in the social systems of distantly related species, such as chimpanzees and spider monkeys (Symington, 1990) or capuchin monkeys and cercopithecines (Robinson and Janson, 1987; O’Brien, 1991; Fedigan, 1993), have been interpreted as evidence of behavioral convergence in response to similar ecological
pressures. Differences between populations of the same or closely related species,
such a s muriquis from Minas Gerais and Sao Paulo (Strier, l989,1992a), Peruvian
and Costa Rican squirrel monkeys (Mitchell et al., 1991), red and mantled howler
monkeys (Glander, 1992; Crockett and Pope, 1993)or De Brazza’s monkeys (Brennan, 1985) by contrast, have been interpreted as evidence of divergent responses to
local ecological differences. Yet, by focusing on the ways in which ecology affects
behavior, we have remained remarkably ignorant about phylogentically conservative traits and the interaction between phylogeny and ecology, on the one hand,
and ecology and demography, on the other. In addition, proximate mechanisms,
such as individual developmental experiences and physiology, that affect life histories, may be correlated with phylogeny and must be incorporated into our comparative models (Harvey and Purvis, 1991).
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(Phylogeny)
[Vol. 37, 1994
b.
(Gz-)->(-)
(-)
\
d
(-)
C
d.
P hy 1ogeny
Ecology
em ography
Fig. 4. Alternative views of the relationships between ecology, phylogeny, demography, and behavior.
a , b Hierarchical effects with no demographic factors included. c: Phylogenetic and ecological effects on
behavior are mediated by and influence demographic variables. d: Interactive effects between phylogeny, ecology, demography, and behavior are hierarchical and unidirectional; e: Interactive effects of
phylogeny, ecology, demography, and behavior are nested in a dynamic feedback system.
For example, is male-biased dispersal the ancestral primate condition, retained
among extant lemurs and most cercopithecines, but lost among all apes and all but
one New World monkey, or is it a derived condition among both lemurs, perhaps
due to high metabolic requirements in these sexually monomorphic primates, and
cercopithecines, as a way to counteract the effects of male dominance in these
sexually dimorphic primates when ecological conditions permit? Models of primate
behavioral ecology have begun to consider the role of phylogeny, and to incorporate
the growing body of comparative data on diverse taxa (Wrangham, 1987; Strier,
1990; Fleagle, 1992; DiFiore and Rendall, 1993).
How facultative are dispersal and other behavioral systems within primate species? Phylogenetic considerations may offer few insights into the dynamics of intraspecific or intrageneric behavioral variability (but see Harvey and Purvis,
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YEARBOOK OF PHYSICAL ANTHROPOLOGY
260
MYTH OF THE TYPICAL PRIMATE
261
1991). Rather, demographic variables such as sex ratios and birth rates, which
may fluctuate widely over relatively brief timespans, must be considered. Newton
(1988) and Stephen (1989) have emphasized the importance of demography for
interpreting variability in the social systems of Hanuman langurs and tamarins,
respectively. The effects of demography on social relationships have also been
demonstrated in long-term studies, not only of cercopithecines (e.g., yellow baboons: Altmann and Altmann, 1979; gelada baboons: Dunbar, 19791, but also of
prosimians (e.g., ringtailed lemurs: Sussman, 1992) and New World monkeys (e.g.,
mantled howler monkeys: Glander, 1992; muriquis: Strier et al., 1993). As longterm data accumulate from a wider diversity of primates, i t may be possible to
identify patterns in behavioral responses to demographic events, and to evaluate
more thoroughly the interrelationships between ecology, phylogeny, and demography that have affected both nonhuman and human primate behavioral evolution
(Fig. 4).
REVISIONIST PERSPECTIVES FOR PRIMATOLOGY
Within anthropology
The study of complex societies
Primatologists and social anthropologists share the study of complex and highly
variable societies. Yet, their approaches to studying the behavior of nonhuman and
human primates have tended to diverge in at least two important respects. It is
appropriate to consider these differences, and the consequences that incorporating
new knowledge of diversity may have for primatologists and anthropological perspectives on primates.
Primatologists are in two senses reductionists, at least methodologically. First,
the implicit assumption that behavior can be quantified necessitates reducing
complex social aggregations and interactions into their individual components
(Hinde, 1976). These components, or variables, are constantly being refined and
revised, but do we miss important relationships between different variables in the
process? Critics of reductionist approaches regard society or culture as a n epiphenomenon, a whole that is greater than the sum of its parts, and may find hierarchical or dialectical analyses of individual behavior and relationships within society too limiting (see Hinde, 1987; Quiatt and Reynolds, 1993; Rowell, 1993). Yet,
without the quantitative data obtained from reductionist methods, primatology
would revert to the descriptive accounts that characterized the first wave of studies, and we would lose whatever comparative ground we have gained over the
years. Rather, by extending behavioral ecological models to include phylogenetic
and demographic variables, we may be able to identify patterns across diverse and
dynamic behavioral systems. At the same time, however, we must incorporate the
more traditional definition of reductionism, in which complex phenomena, such a s
social behaviors, are understood in terms of lower level processes involving proximate mechanisms. Primatologists working with captive primates have historically examined behavior at multiple levels (Snowdon, 1990a); the continued development of noninvasive techniques to measure proximate variables that affect
behavior will provide additional insights for field primatologists as well.
As evolutionary theorists, primatologists also tend to be “populationists,” interested in individual variability, rather than typological norms that tend to disregard most surrounding variation (Mayr, 1966). However, primatologists have succumbed to the problem of extrapolating from individual cases to generalized
models, resulting in overly simplified myths, such as that of the “typical” primate.
The challenge of incorporating individual diversity, whether between individuals, populations, and species, or across primates, resulted in the search for unifying
principles that govern behavior and that can explain variability. These principles
have been modified and expanded as new, contradictory data emerged, as can be
seen in the development of theories of kin selection and reciprocal altruism in
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YEARBOOK OF PHYSICAL ANTHROPOLOGY
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sociobiology, or stochastic dynamic programming models in behavioral ecology
(Mange1 and Clark, 1988). Without such principles, primatologists would be forced
to adopt a sort of group relativism, similar to the cultural relativism employed by
many contemporary social anthropologists. Primatologists must acknowledge the
coexistence of alternative behavioral strategies, such as that of aggressive versus
affiliative forms of competition among males, which may occur in a population as
a frequency-dependent trait. Rowell (1993:136) suggests that “we lack evidence
that individuals have in any sense decided on a n appropriate social system. . . .
Rather, animals respond to impinging stimuli and we perceive social systems.” If
social systems are not emergent properties, then, as Rowell proposes, efforts to fit
observed variation across primates into simple classificatory systems may detract
from, rather than advance, our understanding of behavior. Yet, a s long as the
pursuit of unifying explanations and testable hypotheses about behavior remains
a priority, primatology will continue to be more closely, and appropriately, aligned
with behavioral ecology than with other subfields of anthropology.
The role of primate models in studying human behavioral evolution
If primatologists are methodologically and theoretically more closely aligned
with behavioral ecologists than with other anthropologists, are nonhuman primates more appropriately viewed a s other animals rather than as human relatives? Social carnivores may provide better models for cooperative hunting
(Schaller and Lowther, 19691, cetaceans may provide better models for complex,
multilevel societies (Moore, 1992), and birds may provide better models for the
ontogeny of vocal communication (Snowdon, 1990b). But if, for example, we would
like to know how humans evolved their vocal tracts, nonhuman primates, and in
particular, our closest panine relatives, are clearly the most suitable study subjects. While general principles that apply to nonprimates, nonhuman primates,
and humans alike are useful in addressing questions of convergence, it is primates
we must look toward in addressing questions of homology (de Waal, personal
communication).
General principles that explain some of the diversity of extant primate behavioral adaptations can provide insights into that of extinct primates, including
hominids (Tooby and DeVore, 1987), but it is important to recognize the limitations
of such inferences. For example, comparative data from nonhuman primates indicate that while those with monogamous mating systems are sexually monomorphic
in body and canine size, some sexually monomorphic primates, such as muriquis,
mate polygamously (Milton, 1985b; Rosenberger and Strier, 1989; Strier, 1987,
199213; Lemos de Sa et al., 1993). We might infer, therefore, that sexual dimorphism among fossil hominids was associated with polygynous or polygamous mating systems, but we could not conclude that sexually monomorphic hominids were
necessarily monogamous. Recognizing that not all principles have transitive properties is as essential to avoiding inappropriate inferences between nonhuman and
human primates as is the fit between our choice of study subjects and the types of
comparative and evolutionary questions we ask (Harvey and Purvis, 1991).
Comparative behavioral ecology
Apart from their phylogenetic relationship to humans, do nonhuman primates
differ from other animals? Or, as Daly (1992:425) has provocatively asked, “Why
does primatology exist?” According to Daly, “The principal effect of this disciplinary boundary seems to be a slowed diffusion of advances from behavioral ecology
and other biological disciplines.” Yet, long-term studies of long-lived, socially manipulative individuals have provided some of strongest examples of the range of
behavioral diversity within and between species (Cheney et al., 1987). Indeed,
primatologists were among, if not the first, behavioral ecologists to recognize and
individually name their study subjects (Asquith, 1991). Insights into the ways in
which social behavior can respond to and compensate for ecological fluctuations
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MYTH OF THE TYPICAL PRIMATE
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are likely to become more instructive as phylogenetic, demographic, and proximate-level factors are increasingly considered.
The merging of phylogeny and demography with behavioral ecology and physiology can provide a context for interpreting behavioral diversity, but it will be
limited unless the communities in which primates occur are also understood. Understanding interspecific competition or mutualistic associations both among primates and between primates and other animals is essential to understanding the
contexts in which primate behavioral adaptations have evolved.
Conservation biology
Is the liberation of primatology from its anthropological biases a n oxymoron? As
long as primatologists continue to search for patterns and principles t h a t may be
relevant to questions about human behavioral evolution, nonhuman primates will
continue to be important anthropological subjects. Yet, primate studies have acquired another, more urgent agenda. Increasing human pressure through hunting
and habitat disturbance over the past century has led a number of primates to the
verge of extinction. Of some 240 species of primates recognized today, nearly onehalf are threatened and nearly one-third are endangered, meaning they will become extinct unless drastic measures are taken to protect them. Habitat preservation is a n obvious form of protection, and primates are obvious “flagship” species
to generate public and political support for conservation efforts. In addition, because they are high on the food chain, primates serve a s good indicators of the
degree of habitat degradation (Mittermeier and Cheney, 1987).
Many of the data that field primatologists routinely collect during their scientific studies are invaluable to informed conservation management efforts. For example, data on mating patterns and paternity of both group and nongroup members can provide critical insights into the genetics of endangered populations,
while data on dispersal patterns can help determine which sex might be the most
appropriate to move in translocation projects (Strier, 1 9 9 2 ~ )Similarly,
.
understanding the relationship between sex and reproduction, and the interactions between reproduction and ecological and demographic variables, will be critical to
monitoring the viability of populations, and by extension, tropical ecosystems.
The expansion of primate field studies throughout the tropics has led to the
discovery of new species and the rediscovery of species that had been thought
extinct. It has also led to the discovery of greater diversity in primate behavior.
Incorporating this diversity into more comprehensive primatological models will
facilitate our ability toward preserving it, without undermining the importance of
primates within anthropology.
ACKNOWLEDGMENTS
This review benefitted from support from NSF grant BNS 8958298, and discussions with Irv DeVore, Jon Marks, J i m Moore, and Chuck Snowdon over many
years. I a m especially grateful to Jim Moore, Jon Marks, Chuck Snowdon, Frans de
Waal, and two anonymous reviewers for their critical reading and comments on a n
earlier draft of this manuscript, and to Ted Steegmann for his patience and encouragement.
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