KAREN B.

STRIER

Primate Behavioral Ecology: From Ethnography to

Ethology and Back

ABSTRACT Nonhuman primates occupy a special niche in anthropology because of the comparative insights into humans they pro-
vide. Initial anthropological interest in primates targeted the apes for their close phylogenetic relationships with humans, and the
semiterrestrial Old World monkeys for their ecological similarities with hominids adapting to life on the ground. From the earliest an-
ecdotal reports of tool use and hunting to more contemporary quantitative analyses of local "cultural" traditions, nonhuman primates
have challenged deep-rooted concepts of human uniqueness and redefined the boundaries between us and other animals. Yet, despite
the long-standing influence of primate studies in anthropology, approaches to studying primates began diverging from those of earlier
ethnographers. Advances in primatology, particularly during the 1990s, have included a much deeper understanding of how ecology,
phylogeny, and demography affect behavior. Insights into intraspecific, population-level variation represent an important area of con-
vergence between primatology, other areas of anthropology, and conservation biology. [Keywords: primate behavioral ecology, an-
thropocentrism, evolutionary theory, systematic methods, biology]

P RIMATOLOGY IS A COMPARATIVE ENDEAVOR, es-

pecially in anthropology, in which nonhuman pri-
mates have always exerted a powerful influence on defini-
they could offer into human social evolution. U.S. physi-
cal anthropologists were not the first researchers to con-
duct field studies on wild primates, nor were the savanna-
tions of what it means to be human. Humans are more dwelling baboons initially targeted by Washburn and his
closely related to other primates than to other animals, student Irven DeVore the only model for comparisons
and the African apes, particularly chimpanzees and bono- with humans. Even before DeVore began his dissertation
bos, are the most closely related to us of all. Yet, despite research on olive baboons in Nairobi National Park, Kenya,
our shared evolutionary history, deeply rooted cultural Clarence Ray Carpenter (1934, 1940), influenced by psy-
perceptions about nature-culture relationships have influ- chologist Robert Yerkes, had already published mono-
enced the status of other primates, and of primatology, in graphs based on his field studies of mantled howler mon-
anthropology. keys and gibbons. Influenced by Carpenter, Japanese
Primates tend to be grouped categorically with other primatologists had already cracked the code of matrilineal
animals, in opposition to humans, in nature-culture di- kinship in Japanese macaques (Kawai 1958; Kawamura
chotomies, and as intermediate, or "boundary species" be- 1958). In 1960, Jane Goodall began her long-term field
tween humans and other animals along nature-culture study of the Gombe chimpanzees in Tanzania, stimulated
continua (Haraway 1989). Different academic traditions by British paleontologist Louis Leakey's conviction about
that have located primatology in either the social or bio- the comparative insights into hominids that the great apes
logical sciences reflect underlying differences in whether would provide.
primates are perceived as closer to humans or to other ani- During its brief history as a discipline, primatology's
mals (Asquith 1991, 2000; de Waal 2001; Strum and Fedi- relationship to other areas of anthropology has changed
gan 2000). Independent of the ambiguous status of other dramatically. This change has been largely, but not en-
primates, comparative insights into their natures continue tirely, in response to what primates have revealed about
to contribute to our understanding of human nature. themselves. As knowledge from an increasing diversity of
Primatology's development as a subfield within U.S. primates began to accumulate, the emphasis in primatol-
physical, or biological, anthropology dates back to the late ogy began to shift from identifying the most appropriate
1950s, when Sherwood Washburn and his students began "referential" models for comparisons with humans to
studying the behavior of wild primates for the insights identifying the underlying principles that could explain

AMERICAN ANTHROPOLOGIST 105(1)."! 6-27. COPYRIGHT© 2003, AMERICAN ANTHROPOLOGICAL ASSOCIATION

 Strier • Primate Behavioral Ecology 17

patterns of primate behavioral evolution more broadly methodological approaches that have steered primatology's
(Tooby and DeVore 1987). By 1981, when Alison Richard's course from ethnography, to ethology, and back.2
article "Changing Assumptions in Primate Ecology" ap-
peared in the American Anthropologist (1981:517-533), the ETHNOGRAPHIC ORIGINS
future of primatology in anthropology looked exceedingly The early anthropologically oriented field studies focused
grim. Primatologists, for the most part, had by then re- on the comparative perspectives that the behavior of other
placed the descriptive, ethnographic approaches of an- primates could provide about humans. Underlying assump-
thropology with the evolutionary framework and quanti- tions about the primary forces that shaped human social
tative methods of ecology and biology. Primates became evolution dictated which species were targeted for study
increasingly interesting in their own right, as intelligent, and which aspects of primate behavior were of greatest in-
socially complex animals (Rowell 1993, 2000) that could terest. Assumptions about the role of ecology stimulated
be studied with the same methodologies employed by field studies on savanna-dwelling baboons, while assump-
ethologists and behavioral ecologists. tions about the role of phylogeny provided the impetus
As a result of these changes in perceptions and meth- for field studies on chimpanzees. At the time of these in-
ods, primatology embarked on what seemed to be an irre- itial field studies, the mechanisms by which both ecology
versible trend that would lead to its inevitable realign- and phylogeny influenced behavior were only vaguely un-
ment with biology. By the 1980s, it was not uncommon derstood, but they nonetheless set the stage for the paral-
for nonbiological anthropologists to question what prima- lel, and yet mutually informative, paths that ecological
tology could contribute to the rest of anthropology. Even and phylogenetic approaches in primatology have followed.
now, primatologists seeking employment in anthropology
Washburn and DeVore's (1961) initial fieldwork with
departments are well advised to anticipate this question
savanna-dwelling baboons was predicated on the assump-
from prospective colleagues (Fedigan 2000). Yet, while the
tion that baboons and our hominid ancestors found simi-
1970s revelations about primate behavior patterns were
lar social solutions to meet the similar ecological condi-
strongly influenced by biological approaches that pulled
tions they faced. In those days, the decisive first step in
primatology away from anthropology, those of the late
early human evolution was thought to have occurred when
1990s, which emphasized intraspecific, population-wide
variation, have begun to rekindle an interest among pri- the first hominids exchanged the relative safety of trees
matologists in anthropological approaches to explaining for a more terrestrial, and bipedal, way of life. Both the ba-
human cultural variation. boons and early hominids that populated the East African
In this article, I pick up primatology's relationship to savannas would have encountered similar challenges of
anthropology where Alison Richard (1981) left off. Specifi- detecting and avoiding terrestrial predators, and of finding
cally, I consider how the changing assumptions about pri- and defending dispersed resources such as food, water,
mates that occurred in the 1970s affected the expansion of and shelter, all of which necessitated social responses.3
primatology in the 1980s, and how this expansion affected The large, cohesive, multimale, multifemale, hierar-
the development of comparative models of primate be- chical groups of savanna-dwelling olive baboons differed
havioral variation that pivot around ecology, phylogeny, markedly from those of the more relaxed Indian langur
and, more recently, demography. Together with theoreti- monkeys studied by Phyllis Dohlinow (previously, Jay 1968),
cal and methodological transitions, the unit of analysis in another Washburn student, as well from the societies of
primatology has shifted from individual informants repre- forest-dwelling monkeys, including other populations of
senting their respective species to include populations and olive baboons (Rowell 1966) and other species of baboons
dynamic group processes over time. Contemporary prima- (e.g., chacma baboons, Hall 1963). The behavioral differ-
tology is now focused around the dual challenges of un- ences between savanna baboons and the forest-dwelling
derstanding the proximate mechanisms that underlie be- monkeys known at the time were consistent with ideas
havior and of reconciling deterministic, ecological, and about the effects of predators on the size and composition
phylogenetic models of behavior with fluctuating stochas- of primate groups (e.g., Crook and Gartlan 1966) and the
tic demographic processes. Opportunities for understand- evolution of primate societies (Goss-Custard et al. 1972).
ing intraspecific, population-level variation have grown as Male savanna baboons are larger than females in both
the number of long-term studies has increased. Compari- body and canine size, which was presumed to reflect their
sons among primate populations, like those among hu- roles as the leaders and protectors of their groups. The
mans, may be uniquely influential in reinforcing prima- complex social relationships that seemed to preoccupy
tology's place within anthropology.1 adult males as they vied, whether independently or with
I do not attempt a comprehensive review of either the allies, for their positions in the hierarchy were seen as a
history or major advances in primatology, both of which consequence of the constant associations in large groups
are beyond the scope of this article and discussed in other that life on the savanna required.
recent sources (e.g., Rodman 1999; Strier 2002a; Strum Leakey's interest in the behavior of the great apes, in
and Fedigan 2000; Sussman 2000). Instead, I focus on contrast, was predicated on the idea that the best com-
some of the most influential theoretical perspectives and parative models for hominids would be found among our
18 American Anthropologist • Vol. 105, No. 1 • March 2003

closest living hominoid relatives. The closer evolutionary cause they resembled, for the most part, ethnographies.
relationship between humans and apes, as compared to Primate fieldworkers produced rich, descriptive accounts
that of humans and monkeys, was recognized long before of social behavior based on carefully annotated observa-
paleoecological evidence indicated that woodlands might tions and detailed anecdotes. Primatologists were often
have been more likely habitats for early hominid evolu- participatory observers, provisioning their subjects with
tion than savannas. It was also long before modern mo- food to facilitate the habituation process and to create
lecular genetics revealed a much more recent common an- contexts that increased their opportunities to observe so-
cestry, of just six to eight million years, between the cial interactions (Asquith 1989). Observations, for the
ancestors of today's African apes and humans than was most part, were based on recognizable individuals rou-
previously thought (Marks 2002). tinely referred to by name, and the boldest individuals in
The first anecdotal reports of tool use and hunting by these study groups served as "informants" into the social
chimpanzees (Goodall 1968) were particularly influential customs and relationships on which their societies were
in reinforcing chimpanzee-based comparisons with hu- based. Like ethnographers, the early primatologists were
mans. Both tool use and hunting were thought to be prime cognizant of the biases inherent in their methods, but the
movers of human evolution and, therefore, traits that dis- standards for systematic behavioral sampling and quanti-
tinguished humans from other primates. Evidence of simi- tative analyses that characterize contemporary primatol-
lar behavioral tendencies in chimpanzees implied that our ogy had not yet been established.
last common ancestors might have had these tendencies
as well. Shifting Methods and Theories
The societies of apes also deviated from those of the The widespread adoption of systematic, quantitative meth-
increasingly familiar Old World monkeys in ways that ods occurred in the 1970s, in large part because these
were consistent with differences in their respective kinship methods, promoted by psychologists and biologists (e.g.,
systems. In contrast to most of the familiar Old World cer- Altmann 1974; Crook and Gartlan 1966; Hall 1962), re-
copithecines, such as baboons and macaques, none of the duced observer biases and therefore facilitated compari-
apes live in extended matrilocal societies. The fact that sons among studies.4 By sampling behaviors of interest at
chimpanzees, like many extant human foragers, live in pa- predetermined intervals, the relative frequencies or rates
trilocal societies was consistent with ideas about the im- at which social interactions occurred could be compared
portance of male cooperation for large game hunting dur- across the same or different species and studied by the same
ing hominid evolution as well. The matrilocal societies of or different researchers at different times. By sampling a
baboons and macaques came to be regarded as the "typi- wide range of individuals, the variation in behavioral pat-
cal" primate social pattern from which both chimpanzees terns within and between study groups could be quanti-
and hominids diverged. That this "myth of the typical pri- fied and statistically compared. Thus, instead of subjective
mate" prevailed long after contradictory evidence from a assessments by observers about whether one species, or
greater diversity of primates had accumulated is a testi- one sex, is more aggressive than the other, quantitative
mony to the resilience of anthropocentric ideas about the
analyses permitted more objective comparisons of the ac-
distinctiveness of humans, along with their closest phylo-
tual rates at which aggressive interactions occur (Sussman
genetic relatives, compared to the rest of the primate order
and Garber 2002).
(Strier 1994a, 2001a; Sussman 2000).
Researchers' biases continued to influence what kinds
of questions were asked and what kinds of behaviors were
ETHOLOGY AND EVOLUTIONARY BIOLOGY
sampled, both of which have contributed to shifts in our
In addition to dictating which species of primates were in- perceptions of primates as aggressive and competitive to
itially studied, the early ecological and phylogenetic ap- more conciliatory and cooperative (e.g., de Waal 2001;
proaches in primatology carried different sets of assump- Haraway 1989; Silverberg and Gray 1992; Strum and Fedi-
tions about the degree to which the basic components of gan 2000). Presumably, however, any trained observer us-
sociality, such as grouping patterns or kinships systems, ing similar definitions of aggressive or affiliative behav-
responded facultatively to external conditions or were phy- iors, and similar sampling protocols, would obtain results
logenetically constrained (Crook and Gartlan 1966; Gartlan comparable to another's.
1973; Goss-Custard et al. 1972; Struhsaker 1969). Regard- Quantitative analyses of systematic behavioral data
less of which underlying assumptions and corresponding were a powerful tool, not only for interspecific compari-
approaches were favored, anthropological interest in pri- sons, such as those between baboons and chimpanzees,
mates still converged on the comparative insights into hu- but also for intraspecific comparisons, such as those be-
mans they could provide (Fedigan 1982). tween savanna- and forest-dwelling baboons or among in-
The first wave of primate field studies, spanning from dividuals, whether by sex, age, rank, or kinship, within
Carpenter's pioneering work in the 1930s through the single study groups. Previously qualitative descriptions of
various studies on Old World monkeys and apes launched different social patterns in baboons and chimpanzees could
in the 1960s, were accessible to other anthropologists be- be replaced with comparative data on the actual proportion
 Strier • Primate Behavioral Ecology 19

of their time individuals spent in proximity or interacting mises between males and females responding to diverse
with one another. Similarly, anecdotal accounts of differ- conditions of food and mate availability (van Schaik 1983,
ent mothering styles could be tested against predictions 1989; Wrangham 1979, 1980).
based on their correlation with maternal ranks, age, expe- Gaining access to critical resources involves social
rience, or other attributes that distinguish one mother trade-offs, which vary with local ecological conditions.
from another (e.g., Altmann 1980). These trade-offs should be reflected in relative fitness costs
Systematic methods of behavioral sampling had also and benefits, leading to evolutionary compromises in so-
become necessary for evaluating the new evolutionary hy- called optimal behaviors. Models of optimal group size,
potheses about behavior that were being developed at the for example, predicted trade-offs between the costs and
time. Advances in evolutionary theory provided ways of benefits of group living associated with increased competi-
formulating questions about primate sociality in terms of tion for resources and increased predator detection and
the same kinds of selection pressures that lead to the evo- avoidance, respectively (Maynard Smith 1978). Similarly,
lution of other adaptive traits. As adaptations, primate so- models of sociality predicted trade-offs between competi-
cial behaviors have evolved in response to local selection tion and cooperation in acquiring and defending resources
pressures acting on existing genetic variation in their from other group members and other groups of conspecifics.
populations. Variation in behavior, like variation in any Evolutionary theories of kin selection (Hamilton 1964)
other biological trait with a genetic basis, should, there- generated specific predictions about the conditions under
fore, have consequences on individual fitness, as reflected which biological kin should be more inclined to cooperate
by the variance in their genetic contributions to future with one another than with nonkin, while reciprocal al-
generations. truism could explain the conditions under which nonkin
Evolutionary theories about behavior and its conse- might nonetheless behave altruistically toward one an-
quences for the survival and reproductive success of indi- other (Trivers 1971). Evolutionary and ecological models
viduals generated testable predictions, instead of ethno- thus provided a quantitative framework for explaining pri-
graphic-type descriptions. Systematic sampling methods mate social evolution in ways that qualitative compari-
and quantitative analyses were the means by which pre- sons with humans could not.
dictions about behavioral adaptations could be evaluated.
Sexual selection, which dates back to Charles Darwin's
Together, evolutionary theory and quantitative methods
1871 classic, The Descent of Man and Selection in Relation to
for collecting and analyzing data were instrumental in
Sex, was also invoked to understand why males and fe-
transforming primatology into a hypothesis-driven science.5
males look and behave so differently from one another.
Hypotheses about the trade-offs that males and females
Predictive Models
impose on one another while in pursuit of their own sur-
By the end of the 1970s, comparative studies of other ani- vival and reproductive success were predicated on the ir-
mals, including birds, bats, and ungulates, were generat- refutable sex differences in their respective reproductive
ing models about the relationships between ecological biology.6
variables, like food and predator pressures, and social vari-
ables, such as grouping patterns and mating systems Feminism and Primatology
(Bradbury and Vehrencamp 1977; Emlen and Oring 1977;
Jarman 1974). These ways of characterizing, measuring, The adoption of evolutionary theories that emphasized
and relating social behavior to ecological variables in other the biological differences between males and females both
animals were applicable for primates as well, and formed coincided and conflicted with the expansion of feminist
the foundation for a new series of comparative socioe- perspectives in other disciplines (Hrdy 1981, 1986; Tang-
cological models in primatology. Martinez 2000). The development of feminist perspectives
Among the fundamental features of these new models in primatology emphasized the influence of females on
was the differential treatment of males and females based both males and their emergent societies and shifted some
on differences in their reproductive biology that affected of the focus away from the sensational hair-raising dis-
their reproductive potential. Briefly, evolutionary theory plays of large, showy, and often explosive males toward
predicted that both sexes were selected to behave in ways the more subtle behavioral tactics that females employed
that optimized their access to the resources most critical to in their day-to-day interactions with one another and
their survival and reproductive success (Trivers 1972). Dif- with males. Studies focusing on female primates revealed
ferences in the spatial distribution and temporal availabil- them to be autonomous actors whose behaviors impacted
ity of food resources became the focus for interpreting their social environments, often in ways that correlate with
variation in female social relationships and grouping pat- enhanced reproductive success. Female primates could no
terns, while the spatial distribution and temporal avail- longer be regarded as passive "resources" over which males
ability of fertile females became the focus for interpreting competed, and interpretations of male behavior became
variation in male social strategies. The variety of social sys- increasingly dependent on the constraints and compromises
tems primates exhibited was assumed to reflect compro- imposed by females.
20 American Anthropologist • Vol. 105, No. 1 • March 2003

The increased attention paid to female primates sig- THE EXPANSION OF PRIMATOLOGY
nificantly altered the perceptions of primate societies. Despite its growing rift with anthropology, primatology
These enlightened perceptions have often been attributed was stimulated by the theoretical and methodological
to the influx of feminist-oriented primatologists, particu- tools it had imported from biology. Armed with evolu-
larly, but not exclusively, women who entered the field tionary theory, systematic methods, and testable predic-
during the 1970s (e.g., Haraway 1989). However, it is also tions derived from new socioecological models, primatol-
the case that evolutionary theories, including kin selec- ogy was poised to expand.8 This expansion, which took
tion and sexual selection, being adopted at the time were off during the 1980s, occurred along multiple dimensions
similarly influential because of their emphasis on the im- that increased both the taxonomic breadth and temporal
portance of females and the effects of female behavior on depth of primate field studies.
that of males (Emlen and Oring 1977). Socioecological The predictive ecological models of behavior being
models, with their specific predictions about how the be- developed at the time were derived from comparisons
havior of males should map onto that of females, which in among a small subset of familiar Old World monkeys and
turn should map onto the distribution and availability of apes that had so far been studied (Southwick and Smith
food and other resources, converged with feminist per- 1986). Whether or not their predictions were applicable to
spectives in primatology to stimulate interest in the be- other primates required more extensive field studies on a
broader taxonomic diversity of unfamiliar species and a
havior of females and the powerful influence they can ex-
broader ecological array of familiar species. During the
ert in their societies.
1980s, field primatology attracted U.S. graduate students
FROM ETHNOGRAPHY TO ETHOLOGY
from anthropology and biology departments alike. This
new generation of primatologists was deployed across the
Feminist perspectives might have helped to sustain the world's tropics wherever primates could be found. Neither
connections between primatology and other areas of an- the phylogenetic nor ecological relevance to human be-
thropology, in which similar attention was being paid to havioral evolution figured prominently in which species
females and their power in societies. Yet, by accepting the or populations of primates were selected for study because,
influence of sex differences in reproductive biology on the by this time, the goal of testing predictions from the new
behavior of females and males, even the most thoughtful comparative models of primate behavioral ecology had
and articulate primatologists often found themselves at odds taken precedence over studying primates for their insights
with feminist scholars from other disciplines in which bio- into hominids.
logical sex differences were not acknowledged, and, there- Field studies designed to evaluate hypotheses in be-
fore, the influence of biology on behavior was not admis- havioral ecology were also ideally suited to the one to two
sible. Feminist approaches in primatology were rooted in years that graduate students, and the funding agencies
the unifying principles of evolutionary biology, which led that supported them, could afford to dedicate to their
to predictions about sex differences in behavior. However fieldwork. Systematic data on the availability and distribu-
much the empirical data confirmed the social empower- tion of food and other ecological resources could be col-
ment of female primates, the premise that biology under- lected concurrently with behavioral data over the course
lies sex differences was inconsistent with some of the of a 12-24 month study period, and then analyzed to test
other kinds of feminism being practiced by other scholars. hypotheses about the effects of ecology on behavior.
The more general search for unifying principles in pri- A great deal of effort and energy was devoted to char-
matology was itself antithetical to the expansion of cultural acterizing nearly every aspect of primate foods, from their
relativism and postmodernism in cultural anthropology. nutritional and energetic contents to their spatial distribu-
tion and seasonal availability. Predictions from optimal
This was especially true coming, as it did, on the heels of
foraging models (Schoener 1971) about how animals should
E. O. Wilson's (1975) Sociobiology: The New Synthesis and
balance their nutritional and energetic requirements led
the misunderstandings about biological determinism ([sic]
to analyses of primate feeding, ranging, and grouping pat-
genetics) versus biological potential ([sic] genotype—envi-
terns, which were seen as compromises among different
ronment interactions) that sociobiology engendered. An- optima (Emlen 1968; Pyke et al. 1977). Comparative anal-
thropology was still reacting against social Darwinism and yses ranged from those of single groups, whose ecologies
the eugenics movement, and evolutionary ideas about the and behaviors fluctuated across seasons, to those among
genetic basis underlying the behavior of primates, which the same species in different habitats, to those among dif-
by definition included humans, received a critical recep- ferent species. Intraspecific comparisons could focus on
tion (Sahlins 1976). By the mid-1970s, anthropology was how behavioral variation mapped onto local ecological
becoming increasingly hostile, not to primates, per se, but conditions, while interspecific comparisons, which re-
to the primatologists who sought biological explanations, ceived more attention, could examine both ecological and
with an underlying genetic basis, to understand them. 7 phylogenetic influences on behavior.
 Strier • Primate Behavioral Ecology 21

The accumulation of comparative data led to refine- genetic ancestries would imply. At the same time, how-
ments in the socioecological models. Fox example, the ever, ecology was not sufficient to explain why spider
ecological conditions under which females might cooper- monkeys and their closest relatives, woolly monkeys and
ate with one another to defend food resources from con- muriquis, on the one hand, and chimpanzees and their
specifics, or avoid one another to reduce competition, led closest relatives, bonobos, on the other hand, all live in
to different sets of predictions about the relative costs and patrilocal societies.
benefits of cooperation and competition within and be- Populations of woolly monkeys and muriquis that in-
tween groups. Analyses of social relationships and the clude substantial proportions of insects or leaves in their
ways in which kinship and social histories mediated social diets, respectively, live in much more cohesive social
interactions could be used to evaluate the trade-offs be- groups than populations that maintain more frugivorous
tween cooperation and competition. For example, the oc- diets like those of spider monkeys (Di Fiore and Rodman
currence of matrilocal societies across a subset of Old 2001; Moraes et al. 1998; Stevenson et al. 1994; Strier
World monkeys appeared to coincide with ecological con- 1992). Similarly, bonobos rely on terrestrial herbaceous
ditions that favored cooperation among kin, and thus was vegetation and, correspondingly, live in more cohesive
consistent with kin selection's predictions about nepotism groups than chimpanzees (Chapman et al. 1994). Thus,
(van Schaik 1983, 1989; Wrangham 1980). When food re- while ecological variables related to food could account
sources could not be cooperatively defended, or invoked for the differences observed in their grouping patterns, the
intense competition instead, females appeared to avoid phylogenetic relatedness among these three genera of
one another and, most especially, their closest female kin. New World atelins (muriquis, spider monkeys, and woolly
Whether these primates lived in patrilocal societies or in monkeys), on the one hand, and among the two species of
groups without any close kin varied with the degree to Pan, on the other hand, appeared to be a better predictor
which cooperation among males was advantageous in of their similar patrilocal kinship systems (Strier 1994b,
competition against other groups of male kin (van Hooff 1999a; Wrangham 1987).9
and van Schaik 1992). Advances in the development of phylogenetic ap-
The resources over which males cooperated or com- proaches to behavioral adaptations lagged behind those in
peted were fertile females instead of food, so both the ecology. Nonetheless, the increased taxonomic breadth
grouping patterns of females and the timing of reproduc- spanned by primate field studies made it possible to com-
tion emerged as influences on the social and reproductive pare the behavior of primates across phylogenetic groups
options of males (van Hooff and van Schaik 1994). Unlike in increasingly systematic ways (Di Fiore and Rendall 1994).
kinship relationships among females, which could be Phylogenetically controlled comparisons have now be-
monitored with observations of maternity and extended come a standard in primatology and provide important
matrilineal kin, inferences about paternity and patrilineal clues for distinguishing between components of sociality,
kinship were still limited, for the most part, to observa- such as grouping patterns, which can be predicted from
tions of mating behavior and patrilocal residence patterns, local ecological conditions, and those such as kinship pat-
respectively. It was not until the development of methods terns and life histories, which appear to be more phyloge-
for analyzing genetic paternity that questions about the netically conservative (Strier 1999a, 2002b).
fitness consequences of male behavior or nepotism among Phylogenetically controlled comparisons of behavior
patrilineal kin could be assessed (Strier in press a). (or any other trait) seek to identify adaptations as inde-
pendent evolutionary events (Nunn and Barton 2001). For
Ecological and Phylogenetic Approaches Revisited example, if nothing was known about the shared ancestry
The taxonomic diversity of primates studied during the of chimpanzees and bonobos, we might conclude that pa-
1980s expansion influenced primatology's relationship to trilocality evolved independently in each species. Yet, be-
anthropology in at least two important respects. For the cause we know that chimpanzees and bonobos are sister
first time, enough data had accumulated on several species species, it is more likely that both live in patrilocal socie-
of New World monkeys and prosimians, which include le- ties because their last common ancestor did so as well. If
murs, lorises, and tarsiers, to reconsider the respective in- patrilocality also characterized early hominids, then it
fluence of ecology and phylogeny on behavior. For exam- would be treated as a single independent evolutionary
ple, the fluid, fission-fusion, male-bonded societies of event in the taxonomic clade whose living members in-
Central and South American spider monkeys were remark- clude humans and both species of Pan.
ably similar to those of chimpanzees and consistent with In assessing independent evolutionary events, one be-
their mutual preferences for ripe fruits typically found in gins from the tips of phylogenetic trees and works back-
relatively small, indefensible, dispersed patches (Chap- ward toward each successive node until a behavioral dif-
man et al. 1995; Symington 1990). ference that cannot be attributed to shared ancestry is
The strong ecological parallels between spider mon- identified. An accurate phylogeny is clearly necessary to
keys and chimpanzees were clearly much better predictors this method, and advances in molecular genetics have
of their similar grouping patterns than their distant phylo- been critical in refining our understanding of primate
22 American Anthropologist • Vol. 105, No. 1 • March 2003

phylogenetic relationships, particularly among closely re- ciodemography, which require long-term field data from
lated species. multiple populations, were much slower to develop.
To control for phylogeny in behavioral comparisons, The lag in incorporating life histories and their demo-
one also needs to be able to categorize the behavior of in- graphic consequences into models of primate social be-
terest, and to know how the behavior is distributed among havior is understandable. Primates mature more slowly
extant species. The difficulties of classifying continuous and live longer than other mammals of their size, so it
behavioral variables, such as the number of males in a takes a correspondingly longer time to document the ex-
group or the degree of sexual dimorphism in male and fe- tent of fluctuations in demographic conditions and the so-
male body weights, are well-known (Clutton-Brock and cial consequences of these fluctuations over an individ-
Harvey 1984; Moore 1984). However, questions about the ual's lifespan (Charnov and Berrigan 1993). Relatively
information that is lost by reducing intraspecific variation long interbirth intervals and correspondingly slow repro-
into single, species-specific values have only recently been ductive rates also mean that group and population demo-
raised (Strier 1997, 2001b; Struhsaker 2000). graphics change over years instead of seasons, necessitat-
ing generation-length studies to document.
Intraspecific Variation and the Role of Demography By the 1990s, however, sufficient long-term field data
from a wide range of species made it possible, for the first
In contemporary phylogenetic approaches, the species (or
time, to consider the effects of life histories and demogra-
subspecies, when known) is the smallest unit of compari-
phy on behavior from a comparative perspective. It is now
son. Behavioral data from multiple studies of the same
clear that groups, as well as individuals, have life histories,
species are compressed into single, species-specific mean
and that both group and individual life histories simulta-
or median values, which are then evaluated relative to neously influence, and are influenced by, population de-
other species, genera, and so on in each successively inclu- mography (Strier 1999b). The size and composition of
sive clade. Implicit in this practice is the assumption that groups are dynamic entities, not static structures, which
interspecific variation will tend to exceed intraspecific affect the social options of group members over time. For
variation, and, therefore, the latter can be more or less ig- example, long-term behavioral and genetic data on yellow
nored. baboons have shown that a significant proportion of the
There are several dangers to dismissing intraspecific infants born during the four-year reign of a particularly
variation out of hand, but perhaps the most compelling skillful alpha male were paternally related, in contrast to
one is that doing so fails to take into account the dynamic cohorts born during prior and subsequent years, when so-
processes that shape social behavior in the first place. cial instability and frequent turnovers in the male hierar-
While the socioecological models of the 1970s and 1980s chy prevented a single male from monopolizing a dispro-
focused on behavioral responses to deterministic ecologi- portionate share of fertilizations (Altmann et al. 1996).
cal variables, those of the 1990s included the ways in Although the direction of these fluctuations could not
which more facile social variables, often resulting from have been anticipated, the opportunities for interactions
fluctuations in demography, affected behavior patterns as among paternal kin clearly differ among different cohorts
well. in predictable ways.
Long-term data from a variety of studies on a wide Fluctuations in population densities, and stochastic or
range of species now span multiple generations in the pri- strategic swings in sex ratios, also impact individual dis-
mates' lives. Just as comparisons among populations of persal and reproductive opportunities in predictable ways.
the same species have demonstrated that primate behav- Primate responses to these fluctuations can lead to large
ior fluctuates under different ecological conditions (Hill changes in the size and composition of single groups, with
1999; Yamagiwa and Hill 1998), comparisons across years implications for the ways in which behavior patterns are
from single study groups or populations have demon- compared. During the past 20 years, the muriqui group I
strated that primates also alter their behavior under differ- have been studying has tripled in size, with corresponding
ent social conditions. Primate social environments are dy- increases in its members' social options (Strier 2001b).
namic, and they can undergo dramatic changes during an Like the previous examples, it is difficult to interpret the
individual primate's lifetime, as well as from one genera- biological significance of the mean or median group size
tion to the next (Strier in press b).10 during this 20-year period, yet these values have been cal-
The importance of demography for understanding culated and used in comparative phylogenetic analyses of
primate social options was recognized decades ago (e.g., behavior by other researchers. Whether or not such com-
Altmann and Altmann 1979; Dunbar 1979; Rowell 1979), pression of temporal fluctuations or trends into a single
but efforts to model how demography, life histories, and population or species value affects the outcome of the
behavior interact have only recently received comparative analyses is an empirical question that has not yet, to my
attention. While socioecological studies, which could be knowledge, been systematically explored.
completed by dissertators, led to rapid advancements in The dynamics of primate demography also affect the vi-
our understanding of the ways in which ecological vari- ability of populations. Growing interest in conserving the
ables affect social behavior, comparative insights into so- world's endangered primates and advances in conservation
 Strier • Primate Behavioral Ecology 23

biology have converged with the accumulation of demo- mates (Huffman 1984; Huffman and Quiatt 1986; McGrew
graphic and life history data to emphasize the importance 1998, 2001; van Schaik et al. 1999). Ecological conditions
of populations instead of particular groups or species, and that permit social tolerance, a prerequisite for the social
the effects of both ecological and demographic stochastic- transmission of behavior, and advanced cognitive abili-
ity instead of determinism. ties, must clearly be involved in the flexible adoption of
In conservation biology, populations and their char- local behavior patterns for which no genetic basis can be
acteristics are the defining elements that determine a spe- ascribed (van Schaik et al. 1999; van Schaik and Knott
cies' probability of extinction (Strier 1997). Unlike study 2001). Ideas about the effects of local ecological condi-
groups, populations contain the genetic variation on which tions on variation in levels of social tolerance converge
selection pressures can act, and, therefore, the size, com- with ideas about the influence of local demographic con-
position, and geographic distribution of populations affect ditions on varying social options across populations as
their long-term viabilities and, ultimately, those of the well (Mitani and Watts 1999; Strier 2000). Whether such
species to which they belong (Lacy 1993). The importance cases of population variation in behavior are best under-
of populations in analyses of extinction risks has com- stood as local "cultural" traditions may still be controver-
pelled many primate conservationists to split species into sial because primatologists and other anthropologists still
smaller units, or taxa, in order to recognize the intraspeci- disagree about definitions of culture. Nonetheless, it is
fic variation that populations contain (Mittermeier et al. clear that refining prior assumptions about species-typical
2000; Rylands et al. 1997). n behavior to include the role of learning on local behav-
ioral traditions represents a compelling area of mutual in-
Population Variation and the Future Place of terest among primatologists and other anthropologists
Primatology (McGrew 2001).
The shift in primatology to its present, more population- Deciphering how local traditions, whether for food
oriented perspective is a positive step toward reuniting it acquisition or reinforcing social relationships, are trans-
with anthropology. It is ironic, perhaps, that primatol- mitted within populations has a long history in primatol-
ogy's more recent links with conservation biology would ogy. Yet the new examples of local traditions that have
contribute to the new populationist thinking in primatol- emerged in recent years have renewed efforts to under-
ogy and offset, to some extent, the emphasis that phyloge- stand the underlying mechanisms involved. The develop-
netic models put on interspecific comparisons or that evo- ment of appropriate methodologies to systematically
lutionary biology put on ecological determinism. After all, document and compare interpopulation variation in the
population biology employs the quantitative methods of behavior of primates has just begun (McGrew 2001),
other biological disciplines, while both phylogenetic and stimulating primatologists to take into account some of
ecological interests in primates were, at least initially, al- the same kinds of factors that cultural anthropologists
most entirely ethnographically oriented. have long considered. Together with refinements in eco-
It is even more curious that primatologists working logical, phylogenetic, and demographic models of social
within reductionist biological paradigms would be quicker behavior, understanding the processes involved in the so-
to identify population variation than primatologists cial transmission of behaviors may provide clues into un-
trained as anthropologists, whose sensitivity to the vast derstanding the potential of different primates, including
behavioral diversity of humans should have made us more human populations, to adapt.
alert to the possibility and significance of intraspecific
variation in other primates as well. Anthropocentric pre- Reconciling Approaches to Intraspecific Diversity
conceptions about the distinctiveness of humans versus The socially mediated transmission of local behavioral tra-
other primates seem to have extended to include a double ditions is not the only area in which contemporary prima-
standard for evaluating the extent and significance of in- tology and other areas of anthropology intersect. For ex-
traspecific diversity. ample, some of the classic analyses of human societies,
such as those of Robin Fox (1975) involving the interac-
Cultural Primatology tions among patterns of kinship, mating (or marriage),
The renewed interest in primatology among cultural an- and alliances, can serve as templates for evaluating the so-
thropologists and archaeologists may be attributed, at cial constraints and genetic consequences of the diversity
least in part, to the recent comparative analyses of local of dispersal and mating patterns among primates (Moore
"traditions" in chimpanzee populations that cannot be ex- and Ali 1984; Strier 2002b). The distribution of kinship
plained by ecological or phylogenetic differences among systems and their correlates among primates, like those
them (de Waal 1999; McGrew 1998, 2001; McGrew et al. among humans, reflect historical (evolutionary), ecologi-
2001; Whiten et al. 1999). Chimpanzees are not the only cal, and social influences and have obvious social, as well
primates to exhibit population variation in tool use or so- as biological (and genetic), consequences. Conversely, ad-
cial customs, but their behavioral plasticity appears to be vances in the ways in which primates, including humans,
greater, at least so far, than it is in other nonhuman pri- negotiate within their social networks to establish and
24 American Anthropologist • Vol. 105, No. 1 • March 2003

maintain valued relationships (e.g., Aureli and de Waal tural anthropology, such as cultural ecology, medical an-
2000; Noe et al. 2001) represent a convergence of interest thropology, and economic anthropology, can provide per-
by primatologists in questions of long-standing interest to spectives on the factors that affect human patterns of re-
other anthropologists. source use and abuse. Insights from these and other
Contemporary primatology is still coping with the specializations in anthropology bear directly on the future
challenge of sorting out the relative influence of ecology, of other primates, and on the steps that may be necessary
phylogeny, and, more recently, demography on both to protect them.
intra- and interspecific behavioral variation. In primatol- Understanding the tremendous behavioral variation
ogy, efforts to distinguish predictable and unpredictable and adaptive potential of all primates is an urgent chal-
patterns of intraspecific variation have lagged behind lenge for which primatologists and anthropologists must
those to distinguish patterns of interspecific variation. In unite. Now, once again, the place of primatology lies
anthropology, by contrast, characterizing and interpreting within anthropology, but, ironically, this time it is be-
the behavioral diversity of humans is, by definition, an ex- cause of the perspectives on other primates that humans
ercise in understanding intraspecific variation. Merging can provide.
the phylogenetically controlled, systematic methods of pri-
matology with the cross-cultural comparative approaches
KAREN B. STRIER
Department of Anthropology, University of
of anthropology (e.g., Mace and Holden 1999) is just one ex-
Wisconsin-Madison, Madison, WI53706
ample of the many ways in which primatology and other
areas of anthropology can continue to converge.
NOTES
Understanding the relative importance of intra- and Acknowledgments. I am grateful to James Calcagno for inviting me
interspecific variation in primates is also a critical step to- to present a version of this article in the session "100 Years of Bio-
ward understanding the differences and similarities that logical Anthropology" that he organized at the 2001 Annual Meet-
ing of the American Anthropological Association. I thank him and
exist between humans and any other species of primates. Robert Sussman for extensive comments and suggestions on an
It should therefore be of central interest to both biological earlier version of this manuscript, and Claudia Olejniczak for clari-
and nonbiological anthropologists. Whether the range of fications about gorilla behavioral ecology.
intraspecific behavioral variation expressed by humans 1. Populations, which are traditionally defined as the individuals
of a species that share genes, provide the contexts in which behav-
falls within or beyond that expressed by any other species ior—and evolution—occur. Comparative data from multiple popu-
of primates depends, in part, on the behaviors being com- lations of a species are necessary to identify the species-specific
pared. Comparisons among humans, like those among traits that are relevant for comparisons with the human species.
other species of primates, are more persuasive when based 2. This review focuses primarily on the relationship between pri-
matology and other areas of U.S. anthropology. Perspectives on the
on data that have been collected in comparable, stand- culture of primatology in other countries can be found in other re-
ardized ways. cent reviews (e.g., Strum and Fedigan 2000).
3. Sussman (2000) provides a fascinating history of how interest in
Anthropology's Responsibility to Primatology nonhuman primates as models for early hominid behavioral evo-
lution emerged in response to the changing views of hominids,
The convergence of interest in advancing our understand- many of which were presented at the Cold Spring Harbor Sympo-
ing of intraspecific variation among both human and sium of Quantitative Biology held in June 1950 and published in
1951.
nonhuman primates extends beyond intellectual ques-
4. Many other primatologists were using systematic methods of
tions to the much more urgent concerns of conservation. behavioral sampling prior to this time, but standardized methods
Habitat loss and disturbances now threaten nearly one- became widely established with Altmann's (1974) influential article.
third of the world's primates with extinction (Mittermeier 5. Like any scientific discipline, advances in primatology have
et al. 1999; Mittermeier et al. 2000). Despite global conser- been, and continue to be, dependent on collecting the appropriate
data needed to evaluate, and reject, prevailing hypotheses.
vation efforts, the pace at which primate populations and 6. Evolutionary models of behavior have been criticized on a vari-
their habitats are being decimated exceeds the pace at ety of grounds, including, but not limited to, their apparent failure
which biological adaptations, which require the duration to consider the possibility of alternative explanations. For exam-
ple, without knowledge of genetic relatedness, it is difficult to dis-
of entire generations, can occur. The ability of primates to tinguish the preferential treatment of familiar associates, which
adjust their behavior more rapidly on shorter time frames, may also happen to be kin, from nepotism as postulated by kin se-
in response to the new ecological and demographic chal- lection. Similarly, the common use of terms such as strategies to de-
scribe behavior implies a level of intentionality on the part of
lenges they face, will determine which populations, and actors that have little, if any, awareness about the fitness conse-
ultimately which species, will survive. quences of their actions.
Considering that anthropogenic activities account for 7. It is curious that the ecological and evolutionarily deterministic
the most serious threats to the world's primates today, it is approaches adopted by primatologists, and the relativist ap-
proaches adopted by cultural postmodernists, represented such di-
highly appropriate that anthropologists take a greater in- vergent solutions to the same problems of accounting for observer
terest in primatology than they have in the recent past. biases and understanding behavioral variation. Although prima-
Archaeological studies of the impact of prehistoric hu- tologists are in no way unique among anthropologists in their use
of quantitative methods, the more fluent they became in the lan-
mans on their environments provide perspectives on the guage of biology, the less intelligible they were to many nonbi-
impact of contemporary humans. Similarly, areas of cul- ological anthropologists.
 Strier • Primate Behavioral Ecology 25

8. It is important to emphasize that tests of any prediction, no Clutton-Brock, T. H., and P. H. Harvey
matter how carefully stated or theoretically well founded, are only 1984 Comparative Approaches to Investigating Adaptation. In Be-
as powerful as the data on which they are based. havioural Ecology: An Evolutionary Approach. John R. Krebs and
9. The influence of ecology on primate grouping patterns has Niles B. Davies, eds. Pp. 7-29. Oxford: Blackwell Scientific Publi-
been supported by both inter- and intraspecific comparisons across cations.
a wide range of species. For example, mountain gorillas and Vene- Crook, John H., a n d j . S. Gartlan
zuelan red howler monkeys are strikingly similar to one another in 1966 Evolution of Primate Societies. Nature 210:1200-1203.
their behavioral ecologies despite their phylogenetic distance as de Waal, Frans B. M.
hominoids and ceboids, respectively (Sterck et al. 1997). 1999 Cultural Primatology Comes of Age. Nature 399:635-636.
2001 The Ape and the Sushi Master: Cultural Reflections by a Pri-
10. The great potential many primates display to adjust their be- matologist. New York: Basic Books.
havior in response to local or fluctuating variables in their social Di Fiore, Anthony, and Drew Rendall
environments raises a fundamental question about the degree to 1994 Evolution of Social Organization: A Reappraisal for Primates
which behavior is molded by past evolutionary selection pressures, by using Phylogenetic Methods. Proceedings of the National
which may not have been constant or unidirectional. Academy of Sciences, USA 91:9941-9945.
11. Conservationists acknowledge that some of the new taxo- Di Fiore, Anthony, and Peter S. Rodman
nomic designations are based on sparse data but provide a persua- 2001 Time Allocation Patterns of Lowland Woolly Monkeys (Lag-
sive rationale that it is better to err on the side of preserving biodi- othrix lagotricha poeppigii) in a Neotropical Terra Firma Forest. In-
versity than risk its loss through extinction. ternational Journal of Primatology 22:449-480.
Dunbar, R. I. M.
19 79 Population Demography, Social Organization, and Mating
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