Primate Behavior Research Paper

1. Early Primate Models Of Ancestral Hominin Behavior

Early primate models for the behavior of ancestral humans were based on either: (a) assumptions of similarity in ecological adaptation between extant savannah-living primates and ancestral humans, or (b) shared behavioral traits within the clade of African hominoids (including humans). Raymond Dart, the discoverer of the Australopithecus specimen at Taung, popularized the hypothesis of a saltatory shift to human bipedalism, tool use, and hunting as a result of moving from forests to savannahs (Dart 1957). Dart drew explicit parallels to baboons as contemporary savannah-dwellers that might share behavioral similarities to early humans. Brief field studies of wild baboons revealed distinct differences from modern humans. Nonetheless, early descriptions of baboon sociality, which emphasized male dominance and aggression as important influences on social structure, were used to typify the human condition (Kinzey 1987). The historical prejudices and methodological weaknesses that gave rise to these models have received considerable critical scrutiny (Cartmill 1993). Despite their methodological weaknesses, these early studies planted the seeds for future primate field studies by asking the following questions: (a) In what way do ecological parameters shape social systems? (b) What were the relevant ecological parameters that shaped early human evolution?, and (c) What can extant primates tell us about human behavior and social evolution?

While ecological affinities led to the baboon model, phylogenetic affinities between human and nonhuman apes prompted field studies of chimpanzees, gorillas, orangutans, and bonobos (Hamburg and McCown 1979). Taking a comparative approach, Louis Leakey sponsored well-publicized field studies of three great ape species. Anthropologists focused most attention on the common chimpanzee, the closest living relative to humans (Sibley and Alquist 1987). Behaviors observed in both humans and chimps were assumed to be phylogenetically conservative and therefore likely to have been expressed in our shared common ancestor. Tool use, hunting/meat eating, and the savannah/woodland habitat of chimps at Gombe reinforced the confidence of some anthropologists in the importance of this suite of characters for the evolution of humans (Kinzey 1987).

Contrary to expectation, these studies revealed that, neither baboon nor chimpanzee models have strong explanatory power in reconstructing the behavior of ancestral humans. First, extant species evolved under unique selective pressures and are not satisfactory typological specimens of ancestral species. Second, there is significant intraspecific variation in the behavior of chimpanzees and baboons, with no adequate criteria for selecting which behaviors are applicable to models of ancestral humans. Third, if behaviors common to chimpanzees and humans are assumed to be phylogenetically conservative, there are significant problems with interpreting morphological evidence from the fossil record that is not shared by either modern chimpanzees or humans (see Potts, in Kinzey 1987).

These criticisms apply to the assumptions and methods employed by these modeling approaches and not to the usefulness of primate behavioral studies per se in elucidating past and current human behavior. Past mistakes have served to refine the approaches by which primate studies are conducted and applied. At the beginning of the twenty-first century, few primate studies make explicit use of typological models. Contemporary studies of primate behavior emphasize a comparative approach in which the functions of behaviors are investigated under different ecological and social conditions. The next section presents important conceptual changes in the study of primate behavior and their influence on the application of primate models to the understanding of human behavior.

2. Conceptual Shifts In Primate Behavior Studies

During the same time that primate behavior was being used to construct models of ancestral hominines, it was also an active area of interest in the zoological sciences, particularly in the subfield of behavioral ecology. Behavioral ecology investigates behavioral adaptations to ecological and social conditions. Although behavioral ecologists directly observe phenotypic traits, they use these observations to test falsifiable predictions generated within an evolutionary framework which states that individuals act in ways that increase their inclusive fitness. For example, studies testing optimal foraging theory use economic costbenefit models to generate predictions of behavioral responses to ecological conditions that affect an individual’s energy budget. Other studies, particularly those that focus on reproductive behavior such as mating and offspring care, examine an individual’s decisions when situated in a particular social milieu (Krebs and Davies 1991). This approach to the study of primate behavior is distinctly different from that which was used previously in two important ways: (a) its goal is to test and further develop general evolutionary principles for behavior rather than create models of specific extinct species, and (b) comparative outgroups can be taken from all animals rather than those restricted to the primate order.

Within the field of anthropology, human behavioral ecologists applied evolutionary concepts to test economic models of the ecology of contemporary human hunter-gatherers. Human behavioral ecologists focused on contingencies that had been found to be important in non-human primates: predation, reproductive opportunities, and the distribution and predictability of resources. However, the application of primate studies to the interpretation of human behavior encountered significant difficulties following the publication of E. O. Wilson’s Sociobiology (1975). Criticism of early sociobiological theory is well documented and expressed two main concerns. First, the effusion of speculations on the application of sociobiological principles to human behavior was untestable and therefore unfalsifiable (Caro and Borgerhoff Mulder 1987). The second body of criticism, which objected to sociobiological depictions of humans as inflexible executants of the interests of selfish genes, stemmed from a poorly explained differentiation between genotypic determinism and the plasticity of behavioral phenotypic expression. Suites of behaviors resulting from complex socioenvironmental conditions (e.g., ‘rape’) were incorrectly treated as simple units of evolutionary analysis (Sunday and Tobach 1985). Disagreement over the application of sociobiological theory to the study of human behavior resulted in a division between cultural anthropologists, who emphasized human uniqueness, and those biological anthropologists who studied primate behavior with an eye toward understanding that of humans. While it is a truism that genetic make-up influences behavior, and genetic relatedness influences to whom particular behaviors may be expressed, genetic determinism has no place in behavioral ecology.

The contemporary use of primate behavior within anthropology has shifted from the use of primates as typological models of human origins to field studies and experiments that test predictions developed within a behavioral ecology framework. Significant methodological changes have accompanied this theoretical shift. First, standard methods for the collection of quantifiable data facilitate interpretable statistical tests of predictions and comparison across primate studies (Altmann 1974). Second, more primate species are studied, thereby providing a larger and more diverse sample for comparison. Third, long-term field studies provide information on seasonal and interpopulational variability in behavior, the ontogeny of and change in relationships among individuals, and the causes and consequences of demographic processes in long-lived species. Fourth, a more diverse representation of scientists expands the field of inquiry to include aspects of social life previously assumed ancillary to social organization, particularly female reproductive strategies and the energetics of offspring care (Altmann 1980, Hrdy 1999). Analyses of the resulting data sets demonstrate rich intra and interspecific variability in behavior and relationships that parallel the intraspecific variability observed in humans.

3. Current Primate Studies In Anthropology

3.1 Social Behavior

Two general principles are commonly invoked to explain group size and composition in birds and mammals. First, female reproductive success is limited primarily by the availability of ecological resources, particularly food. With whom females form groups, and the competitive regime between females within those groups, is a function of the distribution of ecological resources in space and time (Wrangham 1980, van Schaik 1989). Male distribution, on the other hand, is patterned upon that of females (Andelmann 1986). The diversity of grouping patterns observed among primates across a range of environments supports this general framework.

Whether of the scramble or contest type, competition for resources underlies this ecological model (Krebs and Davies 1991). Competition, however, can be expressed in multiple ways. Aggression between group members certainly occurs, and individuals obtain inclusive fitness benefits by aiding kin in contests, but not all competition results in direct conflict. Unrelated individuals also engage in cooperative and affiliative behaviors, and reconciliation often occurs after conflicts (de Waal 1983). Several benefits accrue from affiliative interactions with nonkin. First, individuals who engage in post-conflict reconciliation experience more rapid reductions in stress response than those that do not (Aureli 1992). Second, initiating affiliative behaviors garners favor with powerful group members and develops relationships with potential future allies (de Waal 1983). Third, males who invest in nonsexual affiliative behavior toward females obtain future matings with their ‘friend’ (Smuts 1985). ‘Peaceful’ interactions are essential to the social cohesion of groups and provide an alternative means of exerting influence and eliciting support. Long life spans and the opportunity for repeated encounters between known individuals provide the conditions under which individuals can predicate present behavior on anticipated future social interactions (Byrne and Whiten 1988).

The study of behavioral ecology in humans is likewise concerned with the tactics employed by modern humans to survive and reproduce within a particular socioecological context. Using principles developed in the field of animal behavior, human behavioral ecologists collect data from modern hunter-gatherers to test predictions derived from ecological optimization models (Winterhalder and Smith 2000). Human behavioral ecologists are able to measure directly the economic results of behavioral traits thought to be important to human evolution such as the intersexual division of labor, long juvenile dependence, and females’ lengthy post-reproductive life span. The results of such studies have led to important challenges to the primacy of hunting in human history, suggesting instead that the economics of female provisioning and care of offspring provide a more parsimonious explanation for the evolution of human social systems (Hawkes et al. 1997, O’Connell et al. 1999).

Because of their general applicability, the use of behavioral ecology models raises the question of whether primate studies in particular are any more informative than studies of other taxa. Several lines of evidence combine to produce a positive answer. While studies of all taxa, particularly social mammals, serve to test theories that may be relevant to humans regarding the causes and consequences of social systems, the complex nature of social relationships observed in nonhuman primates make them particularly useful as comparative species for understanding the function of human social relationships. In addition, the use of nonhuman primates as comparison species controls for traits more phylogenetically conservative than behavior that may influence behavioral options (e.g., life history parameters, functional morphology, and physiology). Confining the study of behavioral ecology to humans within the field of anthropology limits the perspective from which to understand human behavior. Cross-cultural studies can demonstrate intraspecific variation, but they do nothing to reveal which traits or behaviors are uniquely human. Interspecific comparative studies among primates reveal the extent and degree to which certain behavioral patterns are confined to humans. Primate studies therefore both focus and expand the field of vision in the study of human behavior.

3.2 Functional Morphology

Anatomists have a rich tradition of inferring the behavior of extinct species based on fossil skeletons, and tooth morphology figures prominently in the reconstruction of hominin diets (Jolly 1970). Interpretation of fossils is only possible, however, with studies of analogous structures and their function in extant species. Recently, anatomists have teamed up with primate behavioral ecologists to combine direct observations of primate feeding behavior with dental morphology. This partnership helps refine the techniques used to determine ancestral diet and feeding patterns. For example, field studies of the feeding ecology of four sympatric Sumatran primates allowed Ungar (1996) to test whether incisor size corresponds with diet. His finding that incisor size and shape best reflect the mode of ingestion rather than diet per se resolves some conflicts in interpretation of the fossil record. Dental microwear analyses can reveal more detailed information about diet than can analysis of gross dental morphology. Recent field studies examine primate feeding behavior, measure the physical properties of foods, and cast the teeth of wild primates in order to better understand the relationship between food type, mode of ingestion, and microwear (Teaford 1994). Similar studies are being conducted on humans (Ungar and Spencer 1999). With further refinement of this new technique, analysis of dental microwear can play an important role in the reconstruction not only of the diet of ancestral hominines, but the use of teeth for non-feeding functions as well (Teaford 1994).

Studies of positional behavior investigate the relationship between postcranial musculoskeletal anatomy and locomotion. The means by which wild great apes travel in their natural environment reveal the function of bone and muscle in the limbs (Fleagle 1999), and comparative anatomy between great apes and fossil hominines provides a basis for inferring locomotor behavior in hominines. This approach has shown that bipedal hominines descended from an arboreal primate that moved primarily by climbing rather than brachiating (Fleagle 1999). Likewise, Australopithecus afarensis, the hominin most likely responsible for the famous Laetoli footprints (Leakey 1987), probably spent a good proportion of the day moving arboreally as well as bipedally (Stern and Susman 1983). Field observations also provide clues to possible sex differences in behavior. In apes, sexual dimorphism corresponds with differential use of arboreal and terrestrial substrates for moving, with males spending more time on the ground than females (Doran 1996). If the sexually dimorphic A. afarensis moved on the ground and in the trees, sex differences in substrate use may have likewise occurred.

3.3 Intelligence Cognition

The comparative study of intelligence and cognition among nonhuman primates in the laboratory spans over half a century (Russon et al. 1996). The discovery of tool manufacture and use in wild chimpanzees (Goodall 1968) put to rest concerns that the development of the cognitive capacities necessary to use tools by laboratory primates was an artifact of intensive interaction with humans. Wild orangutans also manufacture and use tools with considerable complexity (Fox et al. 1999). In contrast, the proficiency with which capuchin monkeys use tools in both field and laboratory settings is significantly lower than that of great apes (Visalberghi and Trinca 1989). Great apes have crossed the line into a domain of intelligence once postulated to be uniquely human; furthermore, the intelligence required for ape-level tool use and manufacture evolved before the orangutan–African ape split (van Schaik et al. 1996).

Tool use behavior, however, is only one demonstration of intelligence. The decision-making processes required for large-bodied apes to travel arboreally is another (Povinelli and Cant 1995). Complexity in social interactions such as deception evinces cognition as well (Byrne and Whiten 1988). Primate studies provide empirical proof that many purported aspects of human uniqueness, such as intelligence and culture, are unique to humans only insofar as they are defined as such (Cartmill 1990). The corpus of work in this field demonstrates that, broadly defined, intelligence has evolved by degrees rather than as a result of a single selective pressure on early hominids. Diverse levels and types of cognitive capacities in an array of primates elicit two questions about humans: (a) is the higher intelligence demonstrated in humans an added degree of intelligence or is it a difference of kind, or both? and (b) what selected for human-level intelligence? Language is an obvious difference between humans and nonhuman primates, and it will undoubtedly figure prominently in answering these questions.

4. Future Directions In Research

Although most primates live in groups, a group is comprised of individuals with interests that often differ from those of their group-mates. In addition, those interests change as individuals grow to maturity, reproduce, and then, in some species, shift to a post-reproductive phase of life. Building upon earlier research, future studies are needed to investigate the complexity of factors that influence individual decisions within the context of group life, in particular: (a) the strategies that individuals employ to satisfy their reproductive interests, even when those interests conflict with other group members, and (b) reproductive decisions that incorporate not just matings or fertilizations, but offspring survival as well.

Male aggression or threat of aggression toward females is observed among most species of primates, including humans (Smuts 1992, Smuts and Smuts 1993). Some of this conflict is with current or potential mating partners. However, significant variation in rates of sexual aggression occurs between and within species. For example, woolly spider monkey females copulate without aggression from their mates or other males, while male sexual aggression in rhesus macaques occurs frequently. In baboons, particular males develop ‘friendships’ with females while others do not (Smuts and Smuts 1993). There is even variation in individual males: some human males with pair-bonded mates force copulations with other females, and some pair-bonded males alternately exhibit affiliative and aggressive behavior toward their mate (Ellis 1989). Despite the seemingly widespread occurrence among primate species, however, extreme forms of direct sexual aggression in the form of forced copulations are uncommon in primates other than humans and orangutans. Some hypotheses to explain this striking contrast have been proposed and deserve further exploration.

What is the function of male sexual aggression? Under what conditions does it occur? Feminist scholars and biological and social scientists have long recognized that conflict between female and male reproductive interests influence individual behavior and shape the social systems in which individuals live (Hrdy 1977, MacKinnon 1989). Theoretical treatments of intersexual mating conflict in human and nonhuman primates provide a basis for predicting the conditions under which male sexual aggression, and conversely female countertactics to thwart males, occur (Smuts 1992, Smuts and Smuts 1993). Recent studies provide some preliminary basis for comparison (Smuts and Smuts 1993), but to strengthen the comparative method more studies conducted across a greater spectrum of primates are necessary. Of particular importance is quantifying the costs of sexual coercion, such as reduced foraging efficiency, in addition to infant or female mortality. New noninvasive hormonal assay techniques for field-collected samples are starting to be used (Whitten et al. 1998) and will allow researchers to measure endocrine response by females who are subject to male sexual aggression. Using these techniques, research can reveal the degree to which male aggression produces physiological effects that may negatively impact female fecundity.

Little is understood about why females resist mating by some males but not others. Equally little is known about female tactics to circumvent male attempts to restrict female reproductive choice. More studies are needed to determine the degree to which females select mates based on variation in quality among males (direct mate choice) or whether other factors, including male aggression, sufficiently constrain females to result in facultative, or indirect, female mate choice (Gowaty 1992, Wiley and Poston 1996). Whether for genetic quality, the quality of services, or constraints placed by males, with whom a female mates has an important reproductive outcome. Females are therefore predicted to exercise tactics, including sperm selection, that optimize their ability to retain control over reproductive choice and the timing of reproduction. Techniques for genetic analysis using noninvasive sampling methods have recently been developed (Borries et al. 1999) and will in the future facilitate evaluation of the success of both male and female reproductive strategies.

Variability among male reproductive decisions is likewise important. In contrast to the previously pervasive view within evolutionary studies and behavioral ecology, a recent shift recognizes that the acquisition of multiple mates is not the sole factor motivating male reproductive decisions. Whether they are excluded by other males, fail to attract mates, or are constrained by the need to allocate time to nonmating activities, male primates are limited in the number of females with whom they can actually mate and produce successful young. Males therefore optimize reproductive effort within operating constraints. While limitations on male mating opportunities have traditionally been viewed in terms of male–male competition and male mating aggression toward females, this is not always the case. Male choosiness for mates is likely to be one important tactic in species that have long periods of infant and juvenile dependency (Altmann 1997). Differences in female fertility, for example, may guide males away from young, females as mates. Furthermore, in primates conception and birth are merely the first steps to reproductive success. Offspring must survive into adulthood in order to reproduce, since reproductive success is most accurately measured in the second generation (CluttonBrock 1988). Offspring survival is critically dependent on maternal competence, including mothers’ ability to obtain access to resources necessary to rear young. Males are therefore predicted to prefer as mates those females who are higher ranking, older, and experienced (Altmann 1997).

Females with insufficient resources to rear young may abandon current offspring in order to invest in future reproductive opportunities. Alternatively, in order to meet the demands of rearing offspring, mothers in some species share the task of offspring care. Fathers sometimes significantly assist females, and the need for paternal care constrains male promiscuity in some primates as it does in many species of birds (Clutton-Brock 1991). Likewise, related or unrelated individuals sometimes assist mothers. Related individuals gain inclusive fitness benefits resulting from the survival of grandchildren, sisters, and cousins, while both related and unrelated individuals may gain needed experience necessary for the survival of their future offspring (Hrdy 1999). Long juvenile dependency and the need for assistance in rearing offspring play an important role in the lives of extant hunter-gatherers, and it figures prominently in models of human social evolution (O’Connell et al. 1999). The function of extended juvenile dependency, how mothers meet the demands of extensive infant care, and the consequences for reproductive success are among the most fascinating questions of human and nonhuman primate life-history. Yet because primate life spans are so long, these questions are also among the hardest to study. As data from uninterrupted long-term field studies become available, questions concerning the fitness advantages to variation in parental and alloparental care can be addressed.

Bibliography:

1. Altmann J 1974 Observational study of behavior: Sampling methods. Behaviour 49: 227–67
2. Altmann J 1980 Baboons Mothers and Infants. Harvard University Press, Cambridge, MA
3. Altmann J 1997 Mate choice and intrasexual reproductive competition: Contributions to reproduction that go beyond acquiring more mates. In: Gowaty P A (ed.) Feminism and Evolutionary Biology. Chapman and Hall, New York
4. Andelmann S J 1986 Ecological social determinants of cercopithecine mating patterns. In: Rubenstein D I, Wrangham R W (eds.) Ecological Aspects of Social Evolution: Birds and Mammals. Princeton University Press, Princeton, NJ
5. Aureli F 1992 Post-conflict behaviour among wild long-tailed macaques (Macaca fascicularis). Behavioral Ecology and Sociobiology 31: 329–37
6. Borries C, Laundhardt K, Epplen C, Epplen J T, Winkler P 1999 DNA analyses support the hypothesis that infanticide is adaptive in langur monkeys. Proceedings of the Royal Society London 266: 901–4
7. Byrne R W, Whiten A (eds.) 1988 Machiavellian Intelligence: Social Expertise and the Evolution of Intellect in Monkeys, Apes and Humans. Clarendon Press, Oxford, UK
8. Caro T M, Borgerhoff Mulder M 1987 The problem of adaptation in the study of human behavior. Ethology and Sociobiology 8: 61–72
9. Cartmill M 1990 Human uniqueness and theoretical context in paleoanthropology. International Journal of Primatology 11: 173–92
10. Cartmill M 1993 A View to a Death in the Morning: Hunting and Nature Through History. Harvard University Press, Cambridge, MA
11. Clutton-Brock T H (ed.) 1988 Reproductive Success: Studies of Individual Variation in Contrasting Breeding Systems. University of Chicago Press, Chicago, IL
12. Clutton-Brock T H 1991 The Evolution of Parental Care. Princeton University Press, Princeton, NJ
13. Dart R A 1957 The osteodontokeratic culture of Australopithecus prometheus. Trans vaal Museum (Pretoria) Memoir 10: 1–105
14. DeVore I, Washburn S L 1963 Baboon ecology and human evolution. In: Howell F C, Bourliere F (eds.) African Ecology and Human Evolution. Aldine, Chicago, IL
15. Doran D M 1996 Comparative positional behavior of the African apes. In: McGrew W C, Marchant L F, Nishida T (eds.) Great Ape Societies. Cambridge University Press, Cambridge, UK
16. Ellis L 1989 Theories of Rape: Inquiries into the Causes of Sexual Aggression. Hemisphere, New York, NY
17. Fleagle J G 1999 Primate Adaptation and Evolution, 2nd edn. Academic Press, San Diego, CA
18. Fox E A, Sitompul A F, van Schaik C P 1999 Intelligent tool use in wild Sumatran orangutans. In: Parker S T, Miles H L, Mitchell R W (eds.) The Mentalities of Gorillas and Orangutans. Cambridge University Press, Cambridge, UK
19. Goodall J v L 1968 The behavior of free-living chimpanzees in the Gombe Stream Reserve. Animal Behaviour Monographs 1: 161–311
20. Gowaty P A 1992 Evolutionary biology and feminism. Human Nature 3: 217–49
21. Hamburg D A, McCown E R (eds.) 1979 The Great Apes. Benjamin Cummings, Menlo Park, CA
22. Hawkes K, O’Connell J F, Blurton Jones N G 1997 Hadza women’s time allocation, offspring provisioning, and the evolution of long post-menopausal life spans. Current Anthropology 38: 551–77
23. Hrdy S B 1977 The Langurs of Abu: Female and Male Strategies of Reproduction. Harvard University Press, Cambridge, MA
24. Hrdy S B 1999 Mother Nature. Pantheon, New York
25. Huxley T H 1863 Evidence as to Man’s Place in Nature. Williams and Norgate, London
26. Jolly C J 1970 The seed eaters: A new model of hominid differentiation based on a baboon analogy. Man 5: 5–26
27. Kinzey W (ed.) 1987 The Evolution of Human Behavior: Primate Models. State University of New York Press, Albany, NY
28. Krebs, J R, Davies N B 1991 Behavioural Ecology. Blackwell Scientific, Oxford, UK
29. Leakey M D 1987 Introduction (to the hominid footprints). In: Leakey M D, Harris J M (eds.) Laetoli: A Pliocene Site in Northern Tanzania. Clarendon, Oxford, UK
30. MacKinnon C A 1989 Toward a Feminist Theory of the State. Harvard University Press, Cambridge, MA
31. O’Connell J F, Hawkes K, Blurton Jones N G 1999 Grand- mothering and the evolution of Homo erectus. Journal of Human Evolution 36: 461–85
32. Povinelli D J, Cant J G H 1995 Arboreal clambering and the evolution of self-conception. Quarterly Review of Biology 70: 393–421
33. Russon A E, Bard K A, Parker S T (eds.) 1996 Reaching into Thought: The Minds of Great Apes. Cambridge University Press, Cambridge, UK
34. Schaik C P van 1989 The ecology of social relationships amongst female primates. In: Standen V, Foley R A (eds.) Comparative Socioecology: The Behavioural Ecology of Humans and other Mammals. Blackwell Scientific, Oxford, UK
35. Schaik C P van, Fox E A, Sitompul A F 1996 Manufacture and use of tools in wild Sumatran orangutans. Naturwissenschaften 83: 186–8
36. Sibley C G, Alquist J E 1987 DNA hybridization evidence of hominoid phylogeny: results from an expanded data set. Journal of Human Evolution 26: 99–121
37. Smuts B B 1992 Male aggression against women: an evolutionary perspective. Human Nature 3: 1–44
38. Smuts B B, Smuts R W 1993 Male aggression and sexual coercion of females in nonhuman primates and other mammals: evidence and theoretical implications. Advances in the Study of Behavior 22: 1–63
39. Stern J T, Susman R L 1983 The locomotor anatomy of Australopithecus afarensis. American Journal of Physical Anthropology 53: 69–80
40. Sunday S R, Tobach E (eds.) 1985 Violence Against Women: A Critique of the Sociobiology of Rape. Gordian Press, New York
41. Teaford M F 1994 Dental microwear and dental function. Evolutionary Anthropology 3: 17–30
42. Ungar P S 1996 Relationship of incisor size to diet and anterior tooth use in sympatric Sumatran anthropoids. American Journal of Primatology 38: 145–56
43. Ungar P S, Spencer M A 1999 Incisor microwear, diet, and tooth use in three Amerindian populations. American Journal of Physical Anthropology 109: 387–96
44. Visalberghi E, Trinca L 1989 Tool use in capuchin monkeys: distinguishing between performing and understanding. Primates 30: 511–21
45. Waal F de 1983 Chimpanzee Politics: Power and Sex Among Apes. Harper and Row, New York
46. Whitten P L, Brockman D K, Stavisky R C 1998 Recent advances in noninvasive techniques to monitor hormonebehavior interactions. Yearbook of Physical Anthropology 41: 1–24
47. Wiley R H, Poston J 1996 Indirect mate choice, competition for mates, and coevolution of the sexes. Evolution 50: 1371–81
48. Wilson E O 1975 Sociobiology. Harvard University Press, Cambridge, MA
49. Winterhalder B, Smith E A 2000 Analyzing adaptive strategies: Human behavioral ecology at twenty-five. Evolutionary Anthropology 9: 51–72
50. Wrangham R W 1980 An ecological model of female-bonded primate groups. Behaviour 15: 262–300